"Mental Notes" from the Mind & Life Institute

Posted below are two articles from the Mind and Life Institute blog, both of which are slightly related. The first one features Evan Thompson's work with neurophenomenology and the second one looks at Richard Davidson's work with meditation and compassion as it relates to theory of mind.

Grey Matters

Mind and Life’s resident neuroscientist on the past, present, and future of neurophenomenology.

By Wendy Hasenkamp | September 18, 2014

What is the human mind, and how can we develop it to its greatest potential?

There are many ways of trying to answer this age-old question. As a neuroscientist, I was trained within a theoretical system that largely equates the mind with the physical structure of the brain. Operating from this perspective, science has made incredible strides, giving us insights ranging from the molecular array of genes and proteins to the electrical firing patterns of individual neurons and neuronal assemblies. Yet, until recently, a central element of the human mind was largely missing from neuroscientific investigations: lived experience.

However much neuroscience can tell us about the brain, if we are to have a complete picture of the mind, conscious experience must ultimately be incorporated into our investigations. As a way to illustrate this, imagine reading a detailed description of the neural circuitry that underlies vision—the many processes that result in detecting color, contrast, shape, and motion. While such a description could provide a thorough account of the biological substrates involved in, say, observing a sunset, it is a different thing entirely to gaze at the sun dipping below the horizon and experience its gradations, beauty, stillness, as well as the emotions or memories that arise. A similar case can be made for the majority of mental processes since most have an experiential component.

To access lived experience in scientific studies, researchers must take into account what is referred to as the “subjective perspective”—the participant’s first-person point of view on their own experience, usually reported through narrative, questionnaires, scales, or novel interfaces with measurement instruments. For many decades, however, the use of subjective report in psychological and cognitive research was considered unreliable, in part due to studies showing that memories can be inaccurate, and that introspection can be influenced by factors such as expectation or denial. As a result, subjective data was largely abandoned in favor of more “objective,” third-person measures such as behavior or physiological data. Experience was thus relegated to a black box, inaccessible to science.

Fortunately, cognitive science has begun to return to first-person approaches with renewed interest. Concerns about the reliability of subjective report remain important; at the same time, recent research continues to prove the value of subjective information. The National Research Council, for example, just released a report formally urging researchers to seek information on subjective well-being, which they describe as “the self-reported levels of contentment, stress, frustration, and other feelings people experience throughout the day and while performing different activities.”

Mind and Life’s own history is related to this shift in thinking, and an emphasis on subjective experience remains central to our mission. In the 1990s, Francisco Varela, cognitive neuroscientist and one of Mind and Life’s cofounders, proposed the scientific approach known as neurophenomenology, which seeks to integrate valid first-person subjective information with third-person objective measures. Varela, along with Mind and Life Fellow Evan Thompson, believed that relating moment-to-moment subjective experiences to dynamic activity in neural networks represents an enormous opportunity for cognitive research, and will yield a more comprehensive understanding of the human mind. Areas where this approach is highly relevant include investigations into perception, attention, memory, the self, motivation, volition, emotion, spontaneous cognition, mind wandering, and craving and addiction—all fields in which Mind and Life has sponsored research.

Of course, as cognitive neuroscience continues to advance as a discipline, the development of rigorous methods to probe the subjective contents of the mind will be increasingly essential. Standard questionnaires, for example, often do not offer enough opportunity for individualized answers, and responses are framed within a priori assumptions. Interviews are more detailed, but the resultant information is qualitative in nature and complicated to code and score in a systematic way. Further, untrained participants may be unable to introspect at a high level of detail about their internal experiences, making their reports unreliable or unclear.

To encourage exploration of both the challenges and potential of neurophenomenology, I recently joined with Evan Thompson to host a special issue in the journal Human Frontiers in Neuroscience devoted to the theme of “examining subjective experience.” This issue, now complete and available online for free, contains 18 innovative articles furthering the goals of neurophenomenology. Both primary research reports as well as theoretical and methodological papers are featured, highlighting creative new approaches for probing subjective experience in real-world and laboratory settings, and for eliciting more refined and informative first-person reports. Topics include investigating the experience and neural correlates of selflessness, detailed interview methods that can be used with untrained participants, perspectives on dreaming and hypnosis, and studies of real-time biofeedback in meditators using fMRI.

In the quest to understand the mind—and in so doing, discover ways to alleviate suffering and promote flourishing—subjective experience can serve as a guiding beacon, illuminating scientific findings in a new and meaningful light. Editing this collection of articles, I have been pleased and encouraged to see the high quality of cutting-edge research that also embraces the richness of subjective experience. It is our hope that this issue will help advance the field of neurophenomenology, and serve as a resource as we continue to study the complexities of human experience in an integrative way.



WENDY HASENKAMP, PhD, serves as senior scientific officer at the Mind & Life Institute. As a neuroscientist and a contemplative practitioner, she is interested in understanding how subjective experience is represented in the brain, and how the mind and brain can be transformed through experience and practice to enhance flourishing. Her research examines the neural correlates of meditation, with a focus on the shifts between mind wandering and attention. She has also contributed to neuroscience curriculum development, teaching, and textbook creation for the Emory-Tibet Science Initiative, which aims to integrate science into the Tibetan monastic education system in India.

* * * * *

Theory of Mind

Contemplative science begins to unpack the critical elements of caring

By Wendy Hasenkamp | September 18, 2014

One of the central elements of caring involves the capacity to see things from another person’s point of view. In psychology, this ability is referred to as “theory of mind.” If we want to be able to respond to someone compassionately, we must first understand what he or she may be thinking, feeling, or perceiving—we must have a theory of his or her mind.

In order to do that, we must shift from our own perspective and “put ourselves in their shoes.” In that process, however, we don’t completely abandon our own view. Since we can’t observe others’ minds directly, we instead make use of personal memories and experiences, intuiting what another person is going through by way of analogy. If you think about it, this is actually a complicated set of cognitive operations, but we make this shift effortlessly, many times each day.

Not surprisingly, the brain mechanisms for processing self-related experiences are also used for interpreting the mental states of others. Neuroscientific research has implicated a region called the temporoparietal junction (TPJ) as important for theory of mind. The TPJ is also involved in processing self-related information (e.g., the spatial unity of self and body, or “embodiment”), and is key for distinguishing between self and other. Several medial frontal and parietal areas appear to work with the TPJ to form a brain network that underlies theory of mind.

So, if we want to become more caring, the first question we might ask is whether it’s possible to enhance our theory of mind? In psychology, theory of mind has not historically been viewed as a skill that might vary among the population, or be trainable. Until recently, theory of mind has been viewed as a capacity that is either “normal” or grossly impaired, as has been suggested in autism. However, psychology research is now beginning to examine differences in theory of mind ability in healthy adult populations. For example, it was recently shown that people who read literary fiction have improved scores on theory of mind tests.

Researchers have not yet examined whether meditation affects theory of mind ability directly, but some contemplative practices appear to target exactly this capacity.

Richard Davidson and colleagues at the University of Wisconsin studied expert and novice meditators, scanning their brains while they performed a compassion-based meditation. During the scans, participants were also exposed to emotional sounds. The study showed that both during meditation and in response to the sounds, expert meditators had greater brain activation than novices in several areas including the TPJ. In fact, more than any other area, activity in the TPJ was most strongly related to meditative expertise. This suggests that experienced meditators might be more primed to share emotion with, or take the perspective of, another person.

Another study, at Emory University, tested people’s ability to infer others’ emotions by looking only at their eyes, a standard test of “empathic accuracy” that is closely related to theory of mind. Compared to a control group trained in healthy living, participants trained in compassion were more likely to improve their accuracy on the test, indicating they were better able to judge the emotions of other people based on subtle cues. In addition, the improvement in scores correlated with increased brain activity in frontal cortical regions known to be involved in empathic accuracy and theory of mind.

Finally, a recent longitudinal study of brain structure at Harvard found that the TPJ and other regions implicated in theory of mind had increased grey matter density after eight weeks of mindfulness training. It is generally assumed that increases in grey matter (neurons) result from repeated activation of a brain region, through a process of experience-dependent neuroplasticity. This study suggests that just eight weeks of training may induce neural rewiring in brain structures important for social cognition.

Taken together, these studies indicate that meditation impacts brain areas that are critical for theory of mind. However, when interpreting such results, it is important to remember that all of these brain regions are also involved in other mental processes. For example, the TPJ has been implicated in various forms of attention, as well as aforementioned self-related processes. Of course, one can argue that these other functions are important for developing theory of mind. Still, conclusions about the specific cognitive implications of these brain changes must remain tentative until more standard behavioral and cognitive testing is applied. In future studies, it would be fascinating to examine whether people who practice meditations that involve perspective-taking show changes in basic theory of mind tests, as well as related neural alterations.

Based on all we know about how the brain changes with repeated practice of any skill, it is reasonable to assume that theory of mind can be improved through intentional exercises. In some ways however, we don’t need brain scans to show this; you can engage in these kinds of contemplative practices and see if there are effects in your own life. Can you more easily imagine how others might be feeling? Are you moved toward caring and compassion? These will be the true indicators of meaningful change.

Childhood Abuse and Neglect - The Objective Effects and the Subjective Experience

The two articles below are complimentary in their description of the impact of childhood maltreatment (CM: abuse and/or neglect). The first is only available as an abstract (paywall, of course) and the second comes from Psych Central, a nice resource for lay readers in psychology.

Together these articles show the impact of CM on the function and structure of the brain and the subjective suffering that can result from CM years later. This is the "conclusion" of the first article:

Maltreatment was associated with decreased centrality in regions involved in emotional regulation and ability to accurately attribute thoughts or intentions to others and with enhanced centrality in regions involved in internal emotional perception, self-referential thinking, and self-awareness. This may provide a potential mechanism for how maltreatment increases risk for psychopathology.

In the adults molested as children (AMAC) clients I work with, I see these two processes playing themselves out in their lives every week. The limited affect regulation and the strong tendency toward inaccurate attribution of intentions to others creates a near-constant state of hypervigilance and a general sense of being unsafe with anyone, anywhere.

Likewise, the accentuated interior focus creates a self-sustaining cycle of anxiety, depression, self-blame, and rumination on past wounding. This too can be very debilitating. 


Full Citation:
Teicher, MH, Anderson, CM, Ohashi, K, and Polcari, A. (2013, Aug 15). Childhood Maltreatment: Altered Network Centrality of Cingulate, Precuneus, Temporal Pole and Insula. Biological Psychiatry; 76(4): 297–305. DOI: http://dx.doi.org/10.1016/j.biopsych.2013.09.016

Childhood Maltreatment: Altered Network Centrality of Cingulate, Precuneus, Temporal Pole and Insula

Martin H. Teicher, Carl M. Anderson, Kyoko Ohashi, Ann Polcari

Background

Childhood abuse is a major risk factor for psychopathology. Previous studies have identified brain differences in maltreated individuals but have not focused on potential differences in network architecture.

Methods

High-resolution T1-weighted magnetic resonance imaging scans were obtained from 265 unmedicated, right-handed 18- to 25-year-olds who were classified as maltreated (n = 142, 55 men/87 women) or nonmaltreated (n = 123, 46 men/77 women) based on extensive interviews. Cortical thickness was assessed in 112 cortical regions (nodes) and interregional partial correlations across subjects were calculated to derive the lowest equivalent cost single-cluster group networks. Permutation tests were used to ascertain whether maltreatment was associated with significant alterations in key centrality measures of these regions and membership in the highly interconnected “rich club.”

Results

Marked differences in centrality (connectedness, “importance”) were observed in a handful of cortical regions. Left anterior cingulate had the second highest number of connections (degree centrality) and was a component of the “rich club” in the control network but ranked low in connectedness (106th of 112 nodes) in the network derived from maltreated-subjects (p < .01). Conversely, right precuneus and right anterior insula ranked first and 15th in degree centrality in the maltreated network versus 90th (p = .01) and 105th (p < .03) in the control network.

Conclusions

Maltreatment was associated with decreased centrality in regions involved in emotional regulation and ability to accurately attribute thoughts or intentions to others and with enhanced centrality in regions involved in internal emotional perception, self-referential thinking, and self-awareness. This may provide a potential mechanism for how maltreatment increases risk for psychopathology.

* * * * *
This article comes from Psych Central's World of Psychology blog.

Consequences of Emotional Abuse

By Archana Sankaran
August 1, 2014

I come from a family where abuse has had a generational continuity. My grandfather abused my grandmother. My grandmother abused her son, daughter-in-law and other people. (She threw food at me once.) My father bullies his wife and daughter. My mother is emotionally violent to me. I go crazy and can break stuff around my mother.

Overall it is a very disturbing home environment. No one knows how to get out of the situation and we continue to harm each other. At times it feels like a spiraling battle to death. My grandpa passed away recently, ending his part.

Abuse has many forms. Sometimes it involves power over decision-making, where some people’s opinions do not count in matters related to them. Sometimes the emotional reactions of one person are projected onto others, shifting responsibility. It also can be physically violent, involving breaking things, hitting or cutting. Gossip and social shaming was one of my grandmother’s favorite ways to get control over my father.

I think that abuse is basically a perverted mechanism for control when the healthy ways to influence people seem infeasible. Often with dysfunctional families there is a repetitive nature to these conflicts.

After a few weeks with my family, my body seems to be permanently ready for attack. My shoulder hunches up and there is constant fear in the pit of my stomach. It feels like every person around me who I let into my territory is out to harm me. And no one will choose to spend time with me if they know me fully.

For years the only places I could feel safe or relax in were ashrams and meditation halls. I spent a lot of time by myself in nature. That would eventually calm me down. I was greatly anxious in social interactions, even of a functional nature such as asking for a room to rent.

My father told me a few years ago that every man I am with would leave me. I could not believe that he had used those words on me, knowing that I hurt terribly on this topic. I had just come out of four dark years of matrimony-related sorrow. There was a sense of being boxed in and bashed up.

My father, in his anger, tuned into my wounds and stabbed me where it always hurt most. It took me a while to understand this. I reacted in shock, numbness, severe depression at times. At other times I screamed at him and he released more toxic words.

Always there was a need in me to go closer, to understand the abuse and resolve it. Not one situation resolved. I am being forced to see that there is no healthy closure available to these situations. It is wounded people reacting and damaging others from their woundedness.

Family dynamics harmed me even in less-dramatic situations. For example, I do not recall being able to relax at home with family as a child. Any time I sat down with people at home, I had to perform — an activity such as cleaning the table, or listening to a story or dreaming up projects to do.

That made me always tense when I sat down with people in social situations. How should I entertain them? Often in a group of friends this behavior of mine was not received as my insecurity but as my need to show off.

As a child, positive social stamping was extremely important to me. It was the one way to get attention from my father. I could get warmth and respect from my family and from society if I was a successful person. Social regard became a very important part of my psyche’s feel-good mechanism. I didn’t realize that they would turn completely against me if they perceived me as a failure, which happened later.

In India’s strictly traditional society, I remained unmarried. I was not able to dismiss the social rejection and shaming easily. It was a painful lesson — not only but my society is extreme. Arranged marriages still account for the majority of Indian marriages. Most of the population is married and there is little acceptance of any other choice of living.

I believe that life is a series of lessons that we have to learn and graduate from. Most of us remain broken, wounded individuals trying to cope with our ceaseless desires. May we awaken to an awareness of our wounds. May we find our path to wholeness.

~ Archana Sankaran is an artist and therapist who lives in south India. She writes on alternative health, psychology and gardening. Her blog is at http://energyclinic.wordpress.com

Interesting little film . . . and here is the filmmaker's "spiel" about his work:

After ten months in the making, hoovering smoke, breaking mirrors, hundreds of hours of hard thought and hard work; behold! A short documentary entitled ‘Simon Says: Psychosis’.  One that I’m truly proud of making and one I urge and wish you have the time to view. I’ve written a small spiel to entice you into watching it below this very paragraph. Be sure to check out the Psychotic guide to viewing the film, “What is that?” you retort? Click here to find out, or here. Or here.

So here is the spiel…

Contrary to certain short sighted slogans, mental health isn’t just about those who have a problem. We all have mental health and thus the potential to develop mental ill health. Therefore it is vital that we take the time to understand, explore and talk about it as much as possible.

How absurd is it, that school teachers can talk about war, death, sex, drugs, violence, crime and other graphic subjects but not mental health? A circumstance of our own anatomy. Purely because at present time, it is not in the curriculum and they risk losing their jobs by straying from it.  As a society, we are constantly being bombarded by organisations and campaigns that tell us we have to ‘understand’. But how often and how well do they actually offer anything to actually help people to ‘understand’?

By making this documentary as ‘one creature beyond’ a mere information video (endeavouring to sneer at such). I hope the viewer to feel as entertained as they are moved, as captivated as they are enlightened and as illuminated as they are confronted with any morsel of ignorance they may have around Psychosis. Which if you are like me (in terms of limb count etc) might be substantial.

Which, brings me to that word, one that I was given by a model created by those who have never experienced psychosis but are largely responsible for defining it. With that in mind, if you are looking for a more primary source on what ‘psychosis’ is? how it feels? or what it means? then look no further. Personal stories convey a lot more than a medical definition. I challenge anyone to dispute this, even more so after watching the film.

So, if you’ve gotten this far, you not only owe it to your anatomy, you owe it to your species to watch and take a step to ‘understand’. Plus, there lies some cool animations, newsreel footage and funny stuff in wait, for the uninitiated to feast on. In all seriousness though, I promise that this is unlike any ‘mental health video’ that you may have seen before. On top of that, it’s a hot topic right now, so what have you got to lose?

A large exertion has been made to make the film as detailed as possible, such a complex subject demands a certain amount of layering beyond the spoken word; visually, structurally, symbolically and thematically. In an effort for these… efforts to not be banished to subtlety,  a ‘psychotic guide’ has been written for the viewer. To be found in the download pack below or by itself here. If your intrigued or bewildered at what is meant by the term ‘Psychotic guide’ there is only one way to find out.

Free download pack follow this link  and click “slow download” at the bottom of the page. Pack includes:

• A ready to burn DVD image
• Psychotic guide to viewing the film
• Illustrations from Helen Ahpornsiri
• A ‘shocking’ list of stigmatising mental health headlines (cited and referenced)
• Fragments of the filmmaking process
• Full satirical articles from the spinning newspapers (easier reading than pausing the film)

To download just a movie file follow this link and click “slow download” at the bottom of page.

Please note; the film exists for free as a resource and tool for the purpose of education more than anything else. Nevertheless, let it be stated that it may not be used for any commercial purposes in full or in part.

What’s it Like to Experience and Recover from Psychosis?

By Sandra Kiume

Simon Says: Psychosis is a fantastic documentary featuring three people who’ve experienced psychosis, talking about what it’s like, and their recovery journeys assisted by the Early Intervention in Psychosis Service provided by the Sussex Partnership NHS Foundation Trust in the UK.

The film was created by John Richardson, a person with lived experience of psychosis, giving it special insight, empathy, and an insider perspective. For more background about the filmmaker’s process and intent, follow this link.

You can follow the filmmaker on Twitter at @insipidmedia, and also interact with a special account for the film, @sisaysPSYCHOSIS. Please ask questions and share your feedback on this unique and important project.

The title says it all - this article argues for the use of psychoanalytic techniques to create differing states of consciousness with the intent to map those states with brain imaging. The authors...

argue that viewing psychoanalysis as a method for elucidating subjective experience best motivates collaboration between neuroscience and psychoanalysis. Sketching the crux of contemporary neuropsychoanalysis, we highlight the relative merits of a crosstalk with the critical neuroscience movement of neurophenomenology.

It's a short but interesting article.

Full Citation:
Cusumano EP and Raz A. (2014, Apr 29). Harnessing psychoanalytical methods for a phenomenological neuroscience. Frontiers in Psychology: Psychoanalysis and Neuropsychoanalysis; 5:334. doi: 10.3389/fpsyg.2014.00334

Harnessing psychoanalytical methods for a phenomenological neuroscience

Emma P. Cusumano [1] and Amir Raz [2]

1. Department of Cognitive Science, McGill University, Montreal, QC, Canada
2. Department of Psychiatry, McGill University, Montreal, QC, Canada

Psychoanalysis proffers a wealth of phenomenological tools to advance the study of consciousness. Techniques for elucidating the structures of subjective life are sorely lacking in the cognitive sciences; as such, experiential reporting techniques must rise to meet both complex theories of brain function and increasingly sophisticated neuroimaging technologies. Analysis may offer valuable methods for bridging the gap between first-person and third-person accounts of the mind. Using both systematic observational approaches alongside unstructured narrative interactions, psychoanalysts help patients articulate their experience and bring unconscious mental contents into awareness. Similar to seasoned meditators or phenomenologists, individuals who have undergone analysis are experts in discerning and describing their subjective experience, thus making them ideal candidates for neurophenomenology. Moreover, analytic techniques may provide a means of guiding untrained experimental participants to greater awareness of their mental continuum, as well as gathering subjective reports about fundamental yet elusive aspects of experience including selfhood, temporality, and inter-subjectivity. Mining psychoanalysis for its methodological innovations provides a fresh turn for the neuropsychoanalysis movement and cognitive science as a whole – showcasing the integrity of analysis alongside the irreducibility of human experience.
 

Introduction

This paper illustrates how the marriage of phenomenology and psychoanalysis can inform the scientific study of consciousness. In particular, we outline the potential psychoanalysis holds as a tool for fostering different states of awareness and gathering experiential accounts for the purposes of cognitive neuroscience. Methods for elucidating the structures of phenomenal experience are scantily present in the landscape composing the cognitive sciences. This lacuna – a palpable gap between subjective and objective techniques – calls for expert methods to discern and describe experience from first and second person perspectives. While readily embracing psychodynamic theory, proponents of the neuropsychoanalysis movement have largely overlooked the methods inherent to analysis. A central aspect of the psychoanalytic approach, the unstructured narrative interaction forms the backbone of analysis. Though unconventional in the context of experimental neuropsychology, to disparage the narrative dynamic would cripple the research potential of psychoanalysis (Bazan, 2011). For example, cognitive scientists stand to benefit from narrative approaches to guide participants to uncover unconscious aspects of their experience, cultivate meta-awareness, and elicit descriptive firsthand reports. Here we argue that viewing psychoanalysis as a method for elucidating subjective experience best motivates collaboration between neuroscience and psychoanalysis. Sketching the crux of contemporary neuropsychoanalysis, we highlight the relative merits of a crosstalk with the critical neuroscience movement of neurophenomenology. We conclude by discussing how the development of new phenomenological techniques may leverage psychoanalytic methods in the clinical and experimental study of consciousness.
 

Neuropsychoanalysis in Flux

Neuroscientists, as well as psychoanalysts, are still trying to determine the nature of their collaboration in the burgeoning field of neuropsychoanalysis. Controversy regarding the relationship between psychoanalysis and the natural sciences dates back to Freud’s time, and continues to garner much attention today (Cohler and Galatzer-Levy, 2007). While some scholars consider neurobiology and psychoanalysis to be epistemologically and terminologically irreconcilable (Borch-Jacobsen and Shamdasani, 2011), the organic basis of mental life is one of the founding tenets of psychoanalysis (e.g., Freud, 1910b, p. 209). Freud (1895) had anticipated a future in which the psychological and neural sciences would coalesce. Since the 1990s, this vision has gradually come to fruition: while neuroscientists and cognitive psychologists have rekindled their interest in psychoanalytic ideas, analysts have increasingly turned toward the biological sciences (Fotopoulou et al., 2012). Overarching arguments continue to suggest that neuropsychoanalysis binds neuroscience and analysis by facilitating a crosstalk on topics of mutual interest (Solms and Turnbull, 2011). These global accounts inspire leading contemporary scholars to follow this intuitive lead and expound on the details of this cooperation.

Most research under the label of “neuropsychoanalysis” seeks to situate the concepts of psychoanalysis within the framework of contemporary neuroscience. Early collaboration, in the spirit of Freud, centered on understanding neuropathology from a psychodynamic perspective (Kaplan-Solms and Solms, 2000). This manner of clinically oriented investigation has since expanded to include studies of pathological behavior (e.g., depression and anxiety, Zellner et al., 2011), the neural mechanisms of psychodynamic psychotherapy (Gerber, 2011), as well as attempts to find biological measures for therapeutic outcomes (Shedler, 2010). Other research in neuropsychoanalysis fits with the preclinical cognitive neuroscience of consciousness. These investigations aim to develop models of the brain that accommodate and illuminate psychoanalytic phenomena such as repression (Bazan and Snodgrass, 2012), libido (Pfaff and Fisher, 2012), the dynamic unconscious (Shevrin et al., 1996; Berlin, 2011; Solms and Zellner, 2012), and dreaming (Zellner, 2013). As the investigatory domain of contemporary neuropsychoanalysis grows, so does the variety of empirical approaches: from neuroimaging techniques to experimental behavioral methods and animal studies (Fotopoulou et al., 2012).

Some analysts view neuropsychoanalysis as a weight on psychoanalytic discourse. Such clinicians see the movement as perpetuating the view that psychoanalysis needs biological bolstering to be complete, legitimate, and relevant (Blass and Carmeli, 2007). Other scholars have been especially critical of neuropsychoanalysis, suggesting that it could taint quality, and understanding of analysis among clinicians (Hoffman, 2009). These claims likely emerge in response to studies that purport to investigate the “scientific validity” of psychoanalytic theories (cf dream theory in Shirley, 2011). Alas, such scientism runs counter to the very epistemology set forth by the founders of neuropsychoanalysis, who encourage a balance between scientific objectivity and the subjective insights of psychoanalysis (Fotopoulou et al., 2012). Other critics argue that neuroscience is irrelevant to clinical practice, as the latter emphasizes uniquely personal accounts that are scantily amenable to scientific generalization (Pulver, 2003; Mechelli, 2010). Proponents of neuropsychoanalysis typically respond that while the entire spectrum of neuroscientific studies may be less clinically relevant to psychoanalysts, some studies undoubtedly are, for example animal studies that shed light on primal emotional behavior (Panksepp and Solms, 2012). And while concerns about the integrity of clinical practice remain an important issue, analysts also warn against an insular psychoanalysis that fails to engage in a constructive and critical dialog with the larger scientific community (Safran, 2012).

The collaboration between neuroscience and psychoanalysis reflects greater questions about the nature of scientific research, discourse, and validation (Aron, 2012). By incorporating phenomenological domains into traditional experimental paradigms, neuropsychoanalysis are reshaping the boundaries of science. Findings from neuroscience, moreover, increasingly govern our popular conceptions concerning behavior, psychopathology, and what it means to be human (Thornton, 2011; Young, 2011). Neuropsychoanalysis, therefore, joins the critical neuroscience movement in engaging the scientific community with discussions about culture, meaning, and the irreducibility of human experience (Choudhury and Slaby, 2011). Within this overarching search to unravel the relationship between the mind and body, a central question looms: can the objective third-person methods of cognitive science account for the first-person experience of subjective mental life?
 

Neurophenomenology and the Problem of Consciousness

The question of how and why humans are conscious – known amongst philosophers as the “hard problem” of consciousness – has provoked major debate concerning the nature of scientific inquiry. Most scientists posit that biological mechanisms subserve conscious experience, albeit little knowledge informs the details of such mechanisms (Chalmers, 1995, 2002). Neurologists have long recognized that we seem able to account for the workings of the human brain without recourse to influences beyond the laws of physical science (Eccles, 1965). Subsequently, many thinkers feel hard-pressed to speculate on the evolutionary and functional role of consciousness (Harnad, 2002). Such questions have led some philosophers to the conclusion that consciousness is an illusory heuristic (Churchland, 1981). These thinkers argue that conscious experience just is the neurobiological correlate of consciousness – a position that most neuroscientists hold as their “spontaneous philosophy” (Varela, 1998, p. 31; Dennett, 2001). Others disagree and argue that a description of mind that refers only to biological substrates and processes necessarily leaves something out. These scholars insist that consciousness is irreducible to information processing in the brain (Velmans, 2009) and emphasize that our conscious experience presupposes “every statement, model, or theory” of natural science (Thompson, 2004, p. 394). Such philosophical discord persists, reflecting and motivating practical challenges in the study of consciousness at the experimental level.

One response to the puzzle of consciousness comes from neurophenomenology, a movement founded by Varela et al. (1992). According to Varela, the hard problem is established on a deeply ingrained, falsely dualistic understanding of mind and brain. Instead of trying to philosophically “solve” the hard problem, he proposed that cognitive scientists take a methodological approach (Varela, 1996). In order to elucidate how and why experiences arise from neural processes, scientists require careful descriptions of experience to match the refined objective descriptions of brain functioning (Jack and Shallice, 2001; Lutz, 2002); however, researchers have largely eschewed such first-person methods. This trend partly owes to the recent focus in cognitive science on imaging of the living human brain alongside a long-standing ambivalence towards introspective reports (Nisbett and Wilson, 1977). Thus, while researchers are now equipped with many advanced methods for imaging and modeling the brain in fine-grained detail, sophisticated methods for describing and discriminating subjective experience continue to lag behind. Varela advocated bridging this methodological gap by incorporating the experiential techniques of phenomenology into a circulating dialog with the third-person methods of cognitive science. His neurophenomenology seeks to give an “explicit and central role to first-person accounts and to the irreducible nature of experience, while at the same time refusing both a dualistic concession or a pessimistic surrender” (Varela, 1998, p. 32). In doing so, neurophenomenology does not solve, but rather “dis-solves” the hard problem (Varela, 1998).

Proponents of Varela have realized the neurophenomenological project in different forms and under a variety of labels. Some scholars focus on the philosophical details of the collaboration between phenomenology and cognitive science (Gallagher, 2003). These theorists tease apart difficult phenomenological issues, such as the nature of indexing the self (Zahavi and Roepstorff, 2011), and conducting investigations into experiential realms pertinent to clinicians, including the phenomenology of psychopathology, (e.g., Sass et al., 2011). Neurophenomenology is also a growing scientific research program that seeks to modify and complement traditional methods of neuroscience for better phenomenological inquiry. For example, cognitive scientists have adapted a neuroimaging paradigm to allow for periodic “experience sampling” of subjects during experiments (Christoff et al., 2009). Some investigators utilize experimental participants who are already expert at observing and describing their experience, such as Buddhist meditators (Farb et al., 2007; Lutz et al., 2008). Other scholars have proposed that researchers may harness hypnotic and posthypnotic suggestion to alter subjective experience and encourage particular states of awareness (Lifshitz et al., 2013, 2014). One group of researchers in neurophenomenology focuses on developing first-person methods (Depraz et al., 2003; Vermersch, 2009) as well as second-person interviewing techniques for aiding subjects in attending to and articulating their experience (e.g., Petitmengin, 2006). Across all approaches, both theoretical and applied neurophenomenologists aim to bind first-person approaches with the techniques of modern cognitive science to uncover the basic structures of consciousness (Gallagher and Schmicking, 2010).

Psychoanalysis seems apposite to the goals of neurophenomenology; yet neurophenomenologists have largely overlooked psychoanalytic techniques and theories. Instead, neurophenomenologists have turned to two main sources of inspiration: Western Phenomenology (e.g., following philosophers such as Heidegger, Husserl, and Merleau-Ponty; see Schmicking, 2010) and Eastern contemplative traditions including Buddhist practices (Thompson, 2006; Schmicking, 2010). Research in neurophenomenology centers on training or guiding participants to discern and describe their experience with awareness and impartiality (Petitmengin and Bitbol, 2011). The neurophenomenology approach encourages individuals to reflexively observe consciousness from their first-person perspective and to recount accurate and detailed subjective reports (Lutz and Thompson, 2003). Although the inclusion of psychoanalysis in the neurophenomenological toolbox has yet to occur, Western Phenomenology, and psychoanalytic theory do overlap (Karlsson, 2010; Csordas, 2012). Indeed, the existential psychiatry movement of the early 20th century bridged the two disciplines in letter as well as in spirit (Halling and Dearborn Nill, 1995). Moreover, current efforts in neurophenomenology such as the “explicitation interview” harken to psychoanalytic techniques. The explicitation interview is a practice of “guided retrospective introspection” that incorporates inter-subjective guidance and non-leading suggestions to promote awareness of processes that typically remain implicit and un-seen within the field of experience, also known as “meta-awareness” (Maurel, 2009; Vermersch, 2009). Similarly, analysts describe the therapeutic process as “making the unconscious conscious” and commonly gage the completion of analysis by when the patient can freely articulate whatever comes to mind (Freud, 1910a; Wachtel, 2012). Thus, psychodynamic methods already suffuse established neurophenomenological protocols for cultivating meta-awareness in untrained participants.

The motives and objectives of neurophenomenology resonate with the call to neuropsychoanalysis. Both movements point to the need for a psychological theory in neuroscience that avoids fracturing or reducing human experience into a collection of functions and abilities. Just as neurophenomenologists emphasize the “embodied mind” (Clark, 1999; Thompson and Varela, 2001), neuropsychoanalysts urge scholars to reimagine the “minded brain” (Panksepp and Solms, 2012). Both groups argue that without a theoretical framework that operates at the level of the subject, neuropsychology fails to capture the psychological at all (Bazan, 2011), as well as stress the need for a “neurophenomenal level of analysis” in experimental neuropsychology (Panksepp and Solms, 2012). Like its phenomenological counterpart, neuropsychoanalysis can be seen as a direct effort against the implicit biological reductionism in cognitive neuroscience. Current research in the neuropsychoanalysis community appears biased toward the traditional methods of cognitive neuroscience. To analysts, collaboration with cognitive neuroscience runs the risk of reducing psychoanalytic “meaning” to neural “cause.” In line with the outlook Varela espoused, a turn toward the methodological in neuropsychoanalysis could help assuage these concerns, shifting the emphasis from psychoanalytic theory (e.g., testing the scientific validity of psychoanalytic concepts) to psychoanalytic methods (e.g., incorporating technical aspects of the therapeutic process into experimental protocols). However, while both neurophenomenology and neuropsychoanalysis call for a theory of experience at the subject level, only the former has generated an empirical program for incorporating that theory in practice. In closing, therefore, we propose that neuropsychoanalysis may present a new incarnation of neurophenomenology.

Concluding Remarks

The practical realization of neuropsychoanalysis-as-neuropheno-menology presents many challenges. For example, is it possible to harness elements of the intuitive therapeutic process in an experimental context? Whereas Varela called upon Western phenomenology and Eastern contemplative traditions for their systematic treatment of firsthand experience, analysts often cite one of the hallmarks of psychoanalysis as the “imprecise” treatment of firsthand experience (Bazan, 2011, p. 2). Written accounts of therapeutic methods (e.g., the specific strategies that an analyst employs to bring out the unconscious stories of their patients) tend to take the form of case studies. Descriptions of more universal or underlying therapeutic techniques are sparse; analysts train in vivo, by engaging in clinical internships and undergoing analysis themselves. While philosophers and analysts have considered the mechanism of psychoanalytic insight and the relation between psychoanalytic insight and the structures of experience as described by cognitive and phenomenological science, these topics remain largely pristine on the proverbial “To Do” list of neuropsychoanalysis research (Strachey, 1934; Karlsson, 2010). And yet, phenomenology and psychoanalysis both draw on the premise that the vague nature of experience hardly precludes its careful articulation, analysis, and interpretation. A dialog between neuropsychoanalysis and neurophenomenology, therefore, would engender more precise ideas concerning the specific psychoanalytic techniques that can inform a correlation between firsthand descriptions of experience and third-person data.

One approach would advocate for including individuals who have undergone analysis as neurophenomenology participants. In the same way we treat seasoned meditators or phenomenologists, we can exploit the process of discerning and describing the psychoanalytic experience. This idea is scarcely new among analysts: “(One) might manipulate different neuropeptides, in research participants who are themselves psychoanalysts, and then have them describe their subjective states, using their expertise in doing so (with reference to the theoretical concepts that we use). Approaches such as this are rather radical, but they have huge potential, and appear to be remarkably underappreciated” (Solms and Turnbull, 2011, p. 9). To consider analysts and analysands experiential experts on par with, say, trained meditators raises many a problem. And yet, experiments involving either psychoanalytically trained individuals or Buddhist monks would both necessarily involve a second-person component – such as the explicitation interview – thereby exploiting a similar experimental approach.

Spanning an array of literature from clinical science and consciousness research, here we show how neurophenomenology casts a fresh light on the neuropsychoanalysis movement. While proponents of neuropsychoanalysis emphasize the importance of bringing a subject-oriented approach to cognitive neuroscience, these scholars have largely neglected the task of incorporating psychodynamic methods in an experimental setting. Cognitive scientists, however, stand to benefit from drawing on psychoanalytic techniques. Given their expertise in calling the unconscious mind to awareness, analysts could help researchers promote meta-awareness and gather subjective reports that effectively describe the structures of experience. At the same time, focusing on the possibilities of methodological exchange between neuroscience and psychoanalysis offers an answer to concerns within the neuropsychoanalysis community. Rather than foisting neuroscientific methods and models onto the theories of psychoanalysis, mining analysis for its phenomenological capabilities would ensure the integrity of the psychodynamic identity in a domain increasingly tinged with neuro-reductionism. Such an approach would allow neuropsychoanalysis to flourish because of, rather than despite, the different perspectives of its comprising disciplines.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
 

References available at the Frontiers site.

Mind wandering has been a hot topic in neuroscience and consciousness research for the past decade or so. In essence, mind wandering is exactly what it sounds like - it is what happens when we are not focused on a task or a specific stream of thought. Often, it is what the mind does when we are engaged in a task, which is the opposite of mindfulness.

Here is a brief summary definition from Wikipedia:

Mind-wandering (sometimes referred to as task unrelated thought) is the experience of thoughts not remaining on a single topic for a long period of time, particularly when people are not engaged in an attention-demanding task. It is the topic of research in the study of attention and consciousness, as it relates to attentional lapses, or digression due to lack of focus on the task in hand[1][2]. 

Mind-wandering tends to occur during driving, reading and other activities where vigilance may be low. In these situations, people report having no memory of what happened in the surrounding environment while pre-occupied with their thoughts. This is known as the decoupling hypothesis.[2] Studies using event-related potentials (ERPs) have quantified the extent that mind-wandering reduces the cortical processing of the external environment. When thinking is not focused on the task in hand, the brain processes both task relevant and unrelated sensory information in a less detailed manner.[3][4][5] 

Mind-wandering appears to be both a stable trait of people and a transient state. Studies have linked performance problems in the laboratory[6] and in daily life.[7] Mind-wandering has been associated with a risk of road traffic crashes.[8] Mind-wandering is also intimately linked to states of affect; studies indicate that task-unrelated thought is common in states of low or depressed mood.[9][10] Mind-wandering is also common when drunk through the consumption of alcohol.[11] 

It is common during mind-wandering to engage in mental time travel—the consideration of personally relevant events from the past and the anticipation of events in the future. Poet Joseph Brodsky described it as a “psychological Sahara,” a cognitive desert “that starts right in your bedroom and spurns the horizon.” The hands of the clock seem to stop; the stream of consciousness slows to a drip. We want to be anywhere but here.[12] 

Studies have demonstrated a prospective bias to spontaneous thought because individuals tend to engage in more future than past related thoughts during mind-wandering.[13]

For additional thoughts on mind wandering, see this Psychology Today article.

In this new study published at Frontiers in Human Neuroscience, the researchers looked at published first-person subjective reports of mind wandering (MW) and dreaming and found many similarities. In both the MW and dreaming states, "content is largely audiovisual and emotional, follows loose narratives tinged with fantasy, is strongly related to current concerns, draws on long-term memory, and simulates social interactions." Both states are also characterized by a relative lack of meta-awareness.

Full Citation: 

Fox KCR, Nijeboer S, Solomonova E, Domhoff GW and Christoff K. (2013, July 30). Dreaming as mind wandering: Evidence from functional neuroimaging and first-person content reports. Frontiers in Human Neuroscience, 7:412. doi: 10.3389/fnhum.2013.00412

Dreaming as Mind Wandering: Evidence from Functional Neuroimaging and First-Person Content Reports

Kieran C. R. Fox [1], Savannah Nijeboer [1], Elizaveta Solomonova [2,3], G. William Domhoff [4] and Kalina Christoff [1,5]

1. Department of Psychology, University of British Columbia, Vancouver, BC, Canada2. Dream and Nightmare Laboratory, Center for Advanced Research in Sleep Medicine, Hôpital du Sacré-Coeur de Montréal, Montréal, QC, Canada3. Individual Studies, Université de Montréal, Montreal, QC, Canada4. Department of Psychology, University of California at Santa Cruz, Santa Cruz, CA, USA5. Brain Research Centre, University of British Columbia, Vancouver, BC, Canada

Isolated reports have long suggested a similarity in content and thought processes across mind wandering (MW) during waking, and dream mentation during sleep. This overlap has encouraged speculation that both “daydreaming” and dreaming may engage similar brain mechanisms. To explore this possibility, we systematically examined published first-person experiential reports of MW and dreaming and found many similarities: in both states, content is largely audiovisual and emotional, follows loose narratives tinged with fantasy, is strongly related to current concerns, draws on long-term memory, and simulates social interactions. Both states are also characterized by a relative lack of meta-awareness. To relate first-person reports to neural evidence, we compared meta-analytic data from numerous functional neuroimaging (PET, fMRI) studies of the default mode network (DMN, with high chances of MW) and rapid eye movement (REM) sleep (with high chances of dreaming). Our findings show large overlaps in activation patterns of cortical regions: similar to MW/DMN activity, dreaming and REM sleep activate regions implicated in self-referential thought and memory, including medial prefrontal cortex (PFC), medial temporal lobe structures, and posterior cingulate. Conversely, in REM sleep numerous PFC executive regions are deactivated, even beyond levels seen during waking MW. We argue that dreaming can be understood as an “intensified” version of waking MW: though the two share many similarities, dreams tend to be longer, more visual and immersive, and to more strongly recruit numerous key hubs of the DMN. Further, whereas MW recruits fewer PFC regions than goal-directed thought, dreaming appears to be characterized by an even deeper quiescence of PFC regions involved in cognitive control and metacognition, with a corresponding lack of insight and meta-awareness. We suggest, then, that dreaming amplifies the same features that distinguish MW from goal-directed waking thought.

“The implication is that fantasy and dreams are part of a single continuing fantasy process which is subject to certain transformations imposed by physiological and stimulus events. It is unnecessary to sleep in order to generate dream-like ideation, and, apparently, it is unnecessary to be awake in order to produce relatively coherent, undream-like ideation”–Eric Klinger (1971, p. 57).

Introduction

Dreaming and daydreaming (or “mind wandering”) seem to have had an enormous influence on human civilization through the ages: they are alleged to have inspired René Descartes's revolutionary view of the mathematical unity of nature (Baillet, 1691; Browne, 1977) and major scientific breakthroughs including discovery of the Benzene ring by Kekulé (Benfey, 1958), formulation of the periodic table by Mendeleev (Strathern, 2000), and Nobel prize-winning research on the chemical basis of neurotransmission by Loewi (1960)—to cite only a few examples. Psychological research into the subjective content of these states has revealed an intriguing, if less sensational, picture of dreaming and mind wandering (MW) as complex integrations of sensorimotor imagery, emotions, memories, and future planning, in which problem-solving can also occur (Domhoff, 2003). Yet these simultaneously mundane and exceptional mental states remain difficult to understand and study, in part because they are subjective and “spontaneous” in nature: undirected, unpredictable, and poorly characterized from both the personal and scientific perspectives.

Even after decades of scientific research, both behavioral and neurophysiological (reviewed in Hobson et al., 2000; Smallwood and Schooler, 2006; Klinger, 2008; Kussé et al., 2010; Schredl, 2010; Christoff et al., 2011; Gruberger et al., 2011; Zadra and Domhoff, 2011; Christoff, 2012), the sheer diversity of findings and perspectives on dreaming and MW can be overwhelming. MW has been characterized as an unwelcome detriment to professional (Smallwood et al., 2011) and educational (Smallwood et al., 2007) performance, as well as personal affect (Killingsworth and Gilbert, 2010), but has also been suggested to have an adaptive role in goal-directed planning (Christoff et al., 2009; Baird et al., 2011; Andrews-Hanna, 2012), deliberation on current concerns (Klinger, 1971, 2008), and creative insight (Baird et al., 2012). Views on dreaming similarly span a broad spectrum: dream mentation is considered by various researchers to be equivalent to brain delirium (Hobson, 1997) and schizophrenic psychosis (Solms and Turnbull, 2002), or to be entirely epiphenomenal (Flanagan, 1995). Others, however, have seen in dreaming a wellspring of individual growth and inspiration (Bulkeley, 2010), a source of creativity, insight and problem-solving (Schredl and Erlacher, 2007), an opportunity for emotional adaptation (Cartwright et al., 1998; Lara-Carrasco et al., 2009), and an expression and potential means of memory consolidation (Nielsen and Stenstrom, 2005; Wamsley and Stickgold, 2011).

Whereas specific beneficial (or conversely, disruptive) roles remain largely speculative, however, similarities between both the subjective and neurophysiological aspects of MW and dreaming have recently been explored in some detail (Pace-Schott, 2007, 2011; Christoff et al., 2011;Domhoff, 2011). In order to further address this question, we outline the general understanding of what dreaming and MW are, then discuss similarities in the subjective experience and neural basis of both states. Finally, we conduct and compare meta-analyses of positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) studies of dreaming (rapid eye movement or “REM” sleep) and MW (DMN activity) in order to examine potentially overlapping neural substrates.

What are Dreaming and Mind Wandering?

“Dreaming” is usually understood as subjective mental experiences during sleep. Although most famously (and strongly) associated with REM sleep (Aserinsky and Kleitman, 1953; Dement and Kleitman, 1957), dream-like thought is also reported during other sleep stages (see Methods).

For several reasons, by “dreaming” we will generally be referring to subjective reports drawn from REM sleep: for one thing, the majority of “dream” reports have been elicited from REM sleep-stage laboratory awakenings; further, only REM sleep shows a particularly strong correlation with dream mentation (~80% of awakenings from REM sleep result in dream reports: Hobson et al., 2000). For the purposes of the present paper, then, “dreaming” refers to mentation reports from REM sleep.

“Undirected” thought is a similarly complex construct, and can be divided into several different categories (Christoff, 2012). “Mind wandering” (MW) and “stimulus-independent thought” (SIT), for instance, are typically defined as thinking that deviates from a particular task a subject is meant to be completing (McGuire et al., 1996; Mason et al., 2007; Christoff et al., 2009). “Spontaneous thought,” on the other hand, is characterized rather by its undirected, effortless nature—more akin to the everyday concept of “daydreaming” (Singer, 1966; Klinger, 1990; Christoff, 2012); no particular task, or deviation from it, is required. Subtle differences are apparent: MW, for example, might be initiated deliberately (as when a subject decides to “tune out” during a boring task) rather than being “spontaneous.” Nonetheless, these terms are often used interchangeably or with only minimal definition. Fluidity of terminology seems inevitable, however, in a relatively young field of inquiry (Christoff, 2012); moreover, the subjective content and neural basis of these states appear highly similar (compare, e.g., Singer and McCraven, 1961; Christoff et al., 2004, 2009; Stawarczyk et al., 2011). We therefore use these terms relatively interchangeably throughout this paper. MW, spontaneous thought, or daydreaming, then, all refer to subjective reports of undirected thoughts during wakefulness (whether deviating from, or in the complete absence of, a task).

The Default Mode Network (DMN) and REM Sleep

Though specific neural correlates of both daydreaming and dreaming remain somewhat elusive, these mental states, and their associated subjective content, are strongly correlated with the “resting state” and REM sleep, respectively (Aserinsky and Kleitman, 1953; Dement and Kleitman, 1957; Maquet et al., 1996; Mason et al., 2007; Christoff et al., 2009; Andrews-Hanna et al., 2010; Vanhaudenhuyse et al., 2010;Christoff, 2012; Hasenkamp et al., 2012).

The default mode network (DMN) was discovered somewhat serendipitously as a pattern of brain deactivations associated with the difference between brain activity during a quiet, resting state (the typical baseline condition for early fMRI studies) and a goal-oriented, directed task (Raichle et al., 2001). Particular regions were consistently more activeduring “rest” than during goal-directed tasks of many kinds, suggesting a “default mode” network of regions active when a subject was “doing nothing” (Raichle et al., 2001; see Table 3 and Figure 2 for core regions of the DMN). It quickly became clear, however, that physical “rest” by no means implied mental inactivity. With no explicit task, subjects almost immediately engaged in spontaneous thought, including daydreaming, planning for the future, recalling memories, and so on (Gusnard et al., 2001). Subsequent research has tied the subjective experience of MW to core DMN regions (Christoff et al., 2004, 2009; Mason et al., 2007;Andrews-Hanna et al., 2010; Vanhaudenhuyse et al., 2010; Hasenkamp et al., 2012). Although regions beyond the DMN appear to also be recruited during MW (e.g., Christoff et al., 2009), the DMN still remains the most commonly used neural proxy for spontaneous thought (see also Methods).

REM sleep is initiated by a network of cells in the pons and nearby portions of the midbrain (Siegel, 2011), but involves a widespread recruitment of higher cortical brain regions (see our meta-analytic results, below, for regions of this theoretical REM network: Table 2 and Figure 1). REM sleep recurs, in increasingly lengthy periods, approximately every 90 mins throughout the sleep cycle, overall constituting about 1.5–2 h of an average night of sleep. Whereas non-REM (NREM) sleep stages are generally characterized by deactivation of many regions as compared to wakefulness (e.g., Kaufmann et al., 2006), REM is unique in that many brain regions are clearly more active than during wakefulness (Table 2, Figure 1). REM also appears to be the most active state from the subjective point of view, with longer, more emotional, and more frequent dream mentation in REM than any other sleep stage (Hobson et al., 2000). REM therefore appears to be by far the best neural marker of dreaming, though it nonetheless remains problematic (see Methods).

FIGURE 1 

 

Figure 1. Neural substrate of REM sleep vs. waking rest. Significant meta-analytic clusters contributing to the neural substrate of REM sleep (as a proxy for dream mentation). Axial slices are displayed in Talairach space, with 3 mm skip. Color bars indicate likelihood that peaks represent actual peaks of difference at a given voxel. Activations (REM > waking rest) are in red-yellow, deactivations (REM < waking rest) in blue-green.

Subjective and Neural Similarities between Dreaming and Mind Wandering

A number of similarities in the subjective experience of dreaming and MW have previously been noted (see Section First-person Reports of Content from Mind Wandering and Dreaming for a detailed overview). The possibility that the neural substrate of the DMN might be involved in, overlap with that of dreaming/REM sleep has also been raised (Fosse and Domhoff, 2007; Pace-Schott, 2007, 2011; Ioannides et al., 2009; Nir and Tononi, 2010), but these comparisons too have remained qualitative: a quantitative meta-analysis has yet to be applied to the question of the similarity in neural substrates between DMN/MW and REM sleep/dreaming. While major reviews and meta-analyses of the DMN have allowed for a tentative consensus regarding its neural basis (e.g., Buckner et al., 2008), a meta-analytic evaluation of brain activity during REM sleep has yet to be undertaken, making a direct comparison between brain activity in the two states difficult. The execution of such a meta-analysis of REM sleep was therefore a major goal of the present review. 

Aims of the Present Review and Meta-Analysis

Here we aim to build on prior qualitative comparisons of both the experiential and brain basis of dreaming and spontaneous thought with a more definitive, quantitative assessment of the similarity in brain activity. A strong reliance on first-person reports of subjective experience has guided much research on both MW and dreaming, and led to breakthroughs in the understanding of their respective neural correlates. Accordingly, we present a detailed discussion of first-person content reports from both states in Section First-person Reports of Content from Mind Wandering and Dreaming. We outline our methods of meta-analysis of functional neuroimaging data in Section Methods. In Section Neuroimaging of Mind Wandering and Dreaming: Meta-analytic Results, we meta-analyze results from functional neuroimaging (PET) studies of REM sleep (see Methods). We compare these results to an authoritative meta-analysis of DMN regions (Buckner et al., 2008) to determine to what extent the neural substrate of REM sleep overlaps with that of the DMN. Finally, we present a discussion of findings, limitations, and future directions, and propose a preliminary model of dreaming as “intensified” mind wandering.

First-Person Reports of Content From Mind Wandering and Dreaming

Similarities in subjective content have been noted since the beginning of such research. For instance, the dreamlike nature of relaxed waking thought was documented in two early studies of what is now called MW, which were carried out in a sleep laboratory using EEG to monitor wakefulness. In both studies, participants were randomly asked to report anything that was going through their minds at the time of the probe. In the first study, Foulkes and Scott (1973) found that 24% of thoughts could be categorized as visual, dramatic, and dreamlike. In a replication study,Foulkes and Fleisher (1975) discovered that 19% of reports were dreamlike.

The qualitative characteristics of dreaming have been intensively studied over the past century, yielding a considerable body of research from which some firm conclusions can be drawn regarding subjective content. Though qualitative data on the content of MW is not nearly as comprehensive, a tentative overview is nonetheless possible. Although a comprehensive review of the literature is beyond the scope of this article, we highlight consistent findings regarding the subjective content of dreaming and MW. We focus on similarities in subject matter across several key areas, including sensory, emotional, fanciful, mnemonic, motivational, and social aspects, as well as addressing the presence or absence of cognitive control and metacognition. Various disparities and inconsistencies are addressed here, as well as in the Discussion. 

Sensory Aspects

The broadest similarity between dreaming and MW is perhaps also the most basic: the sensory building blocks of spontaneous thought in both waking and dreaming are overwhelmingly visual and auditory (though experiences in other sensory modalities are by no means precluded). 

Dreaming

The largely audiovisual nature of dreaming was noted over two millennia ago by Artemidorus in his Oneirocritica (Harris-McCoy, 2012) and has been often replicated in contemporary research. For instance, a recent review of dream content (Schredl, 2010), based on more than 4000 dream reports from both laboratory awakenings and home dream diaries, found that visual content was present in 100%, and auditory content in ~57%, of all reports (Table 1). Other sense modalities (tactile, olfactory, gustatory, and nociceptive experiences), by contrast, were present in ~1% or less of all reports. Indeed, the next most prominent modality after vision and audition was the vestibular sense: ~8% of reports contained experiences of flying, floating, acceleration, etc. (Schredl, 2010). Intriguingly, a comparison with studies of dream reports from more than a century ago shows a very similar trend: in the late nineteenth century, dream reports also almost always featured visual elements, followed by auditory imagery as the next most dominant aspect, and with the remaining senses accounting for very small percentages (~1–7%) (Schwartz, 2000). This suggests that the sensory aspects of dreaming may be consistent cross-culturally (or at least, cross-temporally).

TABLE 1 

 

Table 1. Sensory perception in dreaming.

The apparent predominance of audio-visual content in dreams may underestimate other sensory modalities, however. A number of studies sampling other sensory data revealed that, when prompted specifically for sensations such as pain (Nielsen et al., 1993; Raymond et al., 2002;Solomonova et al., 2008) or bodily orienting movements (Solomonova et al., 2008), participants often reported more information. To our knowledge, similar targeted sensory-content probes have not yet been undertaken during MW, precluding a more detailed comparison. 

Mind wandering

Content findings from mind wandering are not usually directly comparable, since MW researchers have tended to focus on the intensity (rather than the prevalence) of audiovisual imagery, but available evidence suggests similar trends. For example, factor analysis of nearly 1500 experience reports found that visual and auditory intensity are two of eight dimensions significantly characterizing spontaneous thoughts (Klinger and Cox, 1987). A more recent study similarly found a very high prevalence of self-reported visual and auditory imagery during spontaneous thoughts (mean ratings of 4.22 and 4.02, respectively, on a 7-point Likert scale) (Stawarczyk et al., 2011). Along these lines, a recent review concluded that the average spontaneous thought is moderately visual, contains at least some sound, and is very likely (74% of reports) to contain some form of interior monolog or “self-talk” (Klinger, 2008). 

Positive and Negative Emotionality 

Dreaming

It appears that most dreams (~70–75% or more in adults) contain some emotion, though affect in dreams may not always be particularly strong, or appropriate to the context (see Domhoff, 2011, for a discussion). A number of studies have found a relative predominance of negative emotions in dreams, particularly when dreams are scored by judges rather than by dreamers (see Schredl, 2010, for a review). Other studies, however, have found a balance of emotions in REM sleep dream reports, and one study (Fosse et al., 2001) found that joy/elation was in fact the most frequently reported emotion. An interesting study directly compared self-reports of dreaming vs. waking events, finding that negative emotion (particularly fear) was more prevalent during dreaming, and positive emotions more common in waking (Nielsen et al., 1991).

It may be, however, that more intense and negatively toned dreams are better remembered, and thus over-reported. Additionally, sampling techniques (e.g., laboratory awakenings vs. home dream journals) may contribute to differences in findings. Irrespective of these differences and methodological limitations, however, it is evident that both positive and negative emotions are ubiquitous during dreaming. 

Mind-wandering

Though not yet extensively studied, emotion appears to be similarly ubiquitous during MW. One recent study, for instance, involving thousands of reports, found that the majority (69%) of spontaneous thought reports involved emotion (positive emotion in 42.5% of reports, negative emotion in 26.5%), whereas only 31% of reports were reported to be emotionally neutral (Killingsworth and Gilbert, 2010). Though data are generally lacking, it is interesting to note that, in contrast to dreaming, positive emotion appears to predominate during waking MW, and that many more waking spontaneous thoughts appear to be characterized by relatively flat (neutral) affect. Also of interest is that the temporal focus of MW content appears to be more directed toward the past when negative mood has been experimentally induced (Smallwood and O'Connor, 2011). 

Implausibility and Bizarreness

Though the typical spontaneous thought or dream is a relatively plausible simulation or elucidation of past memories, current events, or future plans, generally in line with the current concerns of the subject (see “Motivational Aspects,” below), nonetheless implausible and bizarre elements are common to both states—though their precise frequency remains disputed (Snyder, 1970; Dorus et al., 1971; Zadra and Domhoff, 2011). Examples are physically impossible or socially unlikely situations, fanciful locales and characters, large discontinuities of time and/or space, and so on. 

Dreaming

Depending on scoring criteria, it has been estimated that between 32% (Schredl, 2010) and 71% (Stenstrom, 2006) of dream reports feature bizarre or impossible elements. Despite widely varying estimates, however, there is general agreement that bizarre, incongruous or impossible elements are features of at least a substantial proportion of dreams. Differences in precise estimates are likely due to differing scoring procedures, as well as differences between dreamer- or judge-rated scores. 

Mind-wandering

Though many MW episodes contain relatively realistic simulations of plausible events in the external world, nonetheless a substantial number (~20% of reports) contain elements that are bizarre, implausible, or fanciful (defined as “departing substantially from physical or social reality”) (Klinger and Cox, 1987; Kroll-Mensing, 1992; Klinger, 2008). A more recent study has provided a general replication of earlier results: analyzing thousands of thoughts reported by 124 subjects, Kane et al. (2007) found that the average thought during MW contained a moderate level of fantasy (a mean of 3.77 on a 7-point scale).

In a rare study examining both waking fantasy and dream reports in thesame 12 subjects, Williams et al. (1992) found that bizarre elements were about twice as prevalent in dreams vs. waking spontaneous thought. In a similar vein, dream and daydream bizarreness have been studied in relation to “thick” vs. “thin” boundaries (Kunzendorf et al., 1997): though thin boundary personality was associated with more bizarre dreams and daydreams than thick boundary, dreams were scored more bizarre than daydreams across both personality types. 

Mnemonic Features: Contributions of Episodic and Semantic Memory

Both dreaming and MW draw on episodic and semantic memory sources as building blocks for novel subjective experiences. In this section we discuss the prevalence of past-oriented thoughts during both wakefulness and dreaming, and the potential contributions of both episodic and semantic memory to these states. 

Dreaming

There is an intriguing literature suggesting that sleep, especially NREM sleep, may have a role in memory consolidation (Walker and Stickgold, 2006; Born and Wilhelm, 2012), including specific roles for REM sleep in consolidation of procedural (Smith et al., 2004) and emotional episodic (Nishida et al., 2009; Groch et al., 2013) memories. A dynamic model of sleep-dependent memory consolidation and reconsolidation has recently been proposed, suggesting a complex relationship between sleep stages, memory types and their contribution to cognitive stability, flexibility and brain plasticity (Walker and Stickgold, 2006, 2010).

It is now well documented that dream content borrows from both temporally proximal and distal memories (Nielsen and Stenstrom, 2005). The most proximal memories (those from the previous day) are generally known as “day residue” (Freud, 1908), whereas the recurrence of elements 5–7 days following an experience is referred to as the “dream-lag” effect (Nielsen and Powell, 1989). Personally relevant and emotionally salient events appear to manifest themselves in dream content as day residue and dream lag effects, but can also surface many years after initial encoding (Grenier et al., 2005). The presence of emotional and personally relevant content in dreams may be related to the fact that emotional and impactful events are preferentially consolidated in memory (McGaugh et al., 2002;Nishida et al., 2009). While dreaming contains clear episodic autobiographical elements, memories only rarely get “replayed” in dream content (~1–2% of reports: Fosse et al., 2003). 

Mind-wandering

MW appears to involve roughly equal percentages of thoughts about the past and future (Fransson, 2006), though some studies suggest a “prospective bias” toward future-oriented thoughts (Smallwood et al., 2009; Andrews-Hanna et al., 2010; Stawarczyk et al., 2011), and also a past-bias inducible by negative mood (Smallwood and O'Connor, 2011). Overall, however, it is clear that memories, particularly episodic ones, play a large role in spontaneous thought. Many studies have reported a high prevalence (~20% or more of reports) of past-focused MW (Fransson, 2006; Smallwood et al., 2009; Andrews-Hanna et al., 2010; Smallwood et al., 2011). Indeed, one of the first studies to explore “resting state” activity using PET noted the similarities between such activity and episodic memory recall, as well as the fact that subjective reports of “rest” actually involved a large amount of past recollection and future planning (Andreasen et al., 1995). Similar to dreaming, memories incorporated in waking MW tend to be of emotional and personally relevant material, and are often related to people's current concerns (see section below on “Motivational Aspects”).

In summary, dreaming and MW both contain specific traceable episodic and semantic memory sources, but very rarely reproduce memories in their entirety. Rather, memories tend to reappear in novel, re-contextualized thoughts and scenarios (Nielsen and Stenstrom, 2005). 

Motivational Aspects: Current Concerns

Reports from both dreaming and MW show a strong proclivity to reflect the ongoing concerns of subjects, as well as elements of anticipating and planning for the future. 

Dreaming

A wealth of data supports the notion that dreaming reflects ongoing waking concerns, desires, and experiences, in line with the “continuity hypothesis” of dreaming and waking mental activity (see, e.g., Domhoff, 1996, Ch. 8). For example, transient stressful situations, such as divorce (Cartwright et al., 1984) and grief (Kuiken et al., 2008) are also often present in dream reports in a general form.

Although dream content is often found to be thematically and emotionally consistent with the waking state of the dreamer, certain activities prevalent in waking are only rarely found in dreams. These include cognitive activities such as reading, writing, and using a phone or a computer (Schredl, 2000). 

Mind-wandering

Similar to dreaming, the content of waking MW also centers heavily on subjects' current concerns (Klinger and Cox, 1987; Klinger, 2008; Andrews-Hanna, 2012).

Further, when the temporal focus of MW is examined, a large percentage (~40% in one recent study: Andrews-Hanna et al., 2010) of spontaneous thoughts center around the present time ±1 day, supporting the notion that MW strongly involves current concerns and experiences. Future-oriented thought is also incredibly common during MW (Smallwood et al., 2009;Andrews-Hanna et al., 2010; Stawarczyk et al., 2011), further supporting a role for MW in future-planning and potentially problem-solving. Intriguingly, in one of the few neuroimaging studies to directly examine periods of MW, MW was associated with activations not only in the DMN but also in key executive prefrontal areas, including the dorsal anterior cingulate cortex and dorsolateral prefrontal cortex (Christoff et al., 2009). Such results are consistent with the prevalence of current concerns and unresolved issues in first-person content reports, and may reflect an ongoing (if unconscious) effort to address them (Christoff et al., 2009; see also Discussion). 

Imagined Social Interaction 

Dreaming

Similar to waking life, dreaming is nearly always organized around interactions with others. Most dreams include other characters in some kind of relationship with the dreamer, or a generalized social situation (Hall and Van de Castle, 1966; Nielsen et al., 2003; Schredl et al., 2004; Zadra and Domhoff, 2011). Social interactions in dreams follow a multitude of patterns, including threatening (Valli et al., 2005) and otherwise emotionally-charged situations (Cartwright et al., 1984). Occasionally, recognizable dream characters may change appearance or appear as a generalized entity, fused with features of other individuals. Also of interest is the prevalence of “mentalizing” or use of “theory of mind” in dreaming—i.e., thinking about others' thoughts, emotions and motivations (even though the “others” are of course merely imagined) (McNamara et al., 2007). In general, meaningful interactions with others may be one of the key factors guiding the progression of the dream narrative. 

Mind wandering

First-person reports of MW often involve imagined social interactions with others, as well as thoughts about the intentions and beliefs of other people (Klinger, 2008). This has led to the general notion that “mentalizing” (i.e., thinking about the thoughts and minds of others) and the consideration of hypothetical social situations may be key components of spontaneous thought (Buckner et al., 2008; Andrews-Hanna, 2012). Supporting this idea, numerous studies have found that brain activity underlying “theory of mind” and mentalizing overlaps significantly with DMN regions (see Buckner et al., 2008, for a review). 

Cognitive Control and Metacognition 

Dreaming

A singular aspect of dreams is the seemingly total lack of metacognitive awareness in the dream state. One experiences a complex simulation of oft-bizarre experiences, but without the overt capacity to reflect on the bizarre state of affairs the mind and body are actually in see, e.g., Rechtschaffen (1978). Intriguingly, it appears that well-trained, or talented, individuals can develop metacognitive awareness of the dream state, becoming “lucid” in the dream and sometimes even directing its course and content (Dresler et al., 2012). The exceptional nature of “lucid” dreaming, however, serves to prove the rule of the general lack of control and metacognitive awareness in ordinary dreaming, a characteristic likely attributable to the deactivation of numerous prefrontal cortical regions during REM sleep (see our results in Table 2 and Figure 1; also Hobson et al., 2000; Muzur et al., 2002).

TABLE 2 

 

Table 2. Core cortical components of the neural network underlying REM sleep.

Mind wandering

A lack of explicit goals, and an unawareness that one is even daydreaming or has deviated from the task at hand, are typical of MW (Schooler et al., 2011). But although MW tends to be less characterized by intentional thought and self-reflective awareness, this is not always the case. A recent study from our group, for instance, found that subjects who were probed at random intervals reported being unaware that they had been mind wandering about half (45%) of the time. One's impression of the “controllability” of a segment of MW also varies widely, from a sense of being able to end it at any time, to being completely absorbed in and swept along by a daydream (Klinger, 1978, 2008; Klinger and Cox, 1987; Kroll-Mensing, 1992; Klinger and Kroll-Mensing, 1995). Collectively, these results suggest that cognitive control and metacognitive awareness in MW lie somewhere between the relative lucidity and self-reflectiveness of normal waking thought and behavior, and the near-total lack of control and metacognitive nescience characteristic of regular (i.e., non-lucid) dreams. See the Discussion for an elaboration of this theme.

Methods

Study Selection for Neuroimaging Meta-Analysis

Dreaming

Though the two phenomena have often been seen as synonymous since Aserinsky and Kleitman's discovery of the association between the REM sleep and dreaming (Aserinsky and Kleitman, 1953), dream-like mental activity occurs in all sleep stages (Nielsen, 2000), including briefly at sleep onset (NREM1) (Mavromatis, 1987; Hori et al., 1994; Nielsen et al., 2005) as well as in NREM2 (Antrobus et al., 1995; Fosse et al., 2004), particularly later in the night (Cavallero et al., 1992). Mentation from NREM3/4 sleep, also known as Slow Wave Sleep (SWS), has also been reported, albeit more rarely (Cavallero et al., 1992). In line with the markedly different patterns of brain activity throughout the sleep cycle (Kaufmann et al., 2006), the length, bizarreness, and emotionality of dream reports from various sleep stages appear to differ significantly, though these disparities remain controversial, with some researchers arguing that the important issue is level of cortical activation, not sleep stage (Antrobus et al., 1995; Cicogna et al., 1998; Foulkes, 1999).

There is also strong evidence from neuropsychological lesion work that the neural mechanisms underlying REM sleep and dreaming are doubly dissociable (Solms, 1997, 2000, 2011; Oudiette et al., 2012). Nonetheless, we use neuroimaging studies of REM sleep only as a neural proxy for the brain basis of dreaming in the present study, for several reasons: (1) NREM1, far from being a uniform state, can be subdivided into at least 8 sub-stages (Hori et al., 1994). Hallucinatory, dream-like mentation is only strongly associated with particular sub-stages, especially those with strong EEG theta rhythms (Hori et al., 1994). To our knowledge, however, no neuroimaging study has yet examined these brief epochs in isolation. Data collapsed across all phases of NREM1, then, is an unsuitable neural marker for dream-like mentation. (2) Of the few functional neuroimaging studies of sleep, NREM2 sleep is rarely explicitly divided into early and late stages based on the ultradian changes in its EEG microarchitecture (Roth and Roehrs, 2000). Since only late NREM2 is even moderately correlated (~0.40) with dream mentation (Nielsen, 2000), data collapsed across all phases of NREM2 (which is all that is currently available) is likewise unsuitable. (3) Despite the apparent dissociability of REM sleep and dreaming, the two remain extremely highly correlated, with roughly 70–90% of awakenings from REM sleep yielding dream reports (~83% on average: Nielsen, 2000). So while other sleep stages clearly give rise to dream-like mentation, we contend that REM is “the best and most frequent trigger” for dreaming (Domhoff, 2005; p. 5) and is therefore the best objective neural indicator of strong dream mentation at the present time.

We therefore reviewed all functional neuroimaging (PET or fMRI) studies of REM sleep to date (14 studies; Table A1). In order to minimize the confounding effects of various tasks and baseline conditions, only studies employing a baseline of resting wakefulness (either pre- or post-sleep) were included. A total of 6 studies were included, and 8 excluded, from the meta-analysis (detailed in Table A1). Other reasons for exclusion included the addition of extraneous factors (e.g., auditory stimulation during REM sleep), inclusion of clinical populations, failure to provide information for peak foci of activation, or lack of an appropriate baseline (e.g., studies comparing REM sleep during phasic rapid-eye-movement events with regular tonic REM sleep). 

Mind wandering

Very few papers to date directly examine periods of mind wandering vs. non-mind wandering (Christoff et al., 2009; Vanhaudenhuyse et al., 2010;Hasenkamp et al., 2012). Though numerous other studies have addressed mind wandering indirectly, they tend to assume an a priori link between DMN activity and MW (e.g., Mason et al., 2007; Andrews-Hanna et al., 2010). It appears, however, that this assumption is at least somewhat warranted: Christoff et al. (2009) and Hasenkamp et al. (2012) indeed found stronger activity in major hubs of the DMN (as well as in other regions beyond the DMN) during MW, and Vanhaudenhuyse et al. (2010)similarly found that self-reported intensity of internally-directed thinking correlated with stronger activity in pre-defined DMN regions of interest (ROIs) (e.g., anterior and posterior cingulate cortices, as well as parahippocampal cortices). Direct meta-analysis of regions active in MW was not executed, however, because only Christoff et al. (2009) have used normal subjects, whole-brain (WB) analyses, and direct, online measures of MW. Though Hasenkamp et al. (2012) used direct, online MW measures and WB (vs. ROI) analyses, they exclusively employed a specialist population (long-term meditation practitioners); Vanhaudenhuyse et al. (2010) also used online MW measures and normal subjects, but employed a priori ROIs in their analyses. These considerations render the comparability of the three studies questionable, and a meta-analysis of MW-related brain activations premature. As with REM sleep and dreaming, then, we utilize DMN activity as an imperfect neural marker for spontaneous thought/MW/daydreaming. 

Identifying core regions of the default mode network

As a meta-analysis of MW brain activations was precluded by the above considerations, we consulted a recent comprehensive review of DMN functional neuroanatomy (Buckner et al., 2008) in order to highlight cortical regions thought to be key hubs of the DMN (and by extension, spontaneous thought). There are numerous ways of determining DMN activity: early studies used blocked time periods of task vs. rest, whereas more recent studies have generally used event-related study designs or functional connectivity analysis. Notably, there is high convergence across these several techniques (see Figure 2). The final summary of key DMN regions that we employ here (Table 3) involves the combination and convergence of data from all three methods, and was gleaned by Buckner et al. (2008) from the review of 18 data sets employing hundreds of subjects.

FIGURE 2 

 

Figure 2. Multiple fMRI methods defining the default mode network. Key cortical areas contributing to the default mode network, as revealed by distinct fMRI methods and study designs. Data are based on a meta-analysis by Buckner et al. (2008) that included 4 blocked design fMRI studies, 10 event-related fMRI studies, and 4 studies of functional connectivity. Colors for each panel of images denote the number of studies finding significant effects at a given voxel (see color bars and numeric labels at right). Note the similarity in the pattern of regions recruited, regardless of method (A), and the strong convergence across all methods (B). Reproduced with permission from Buckner et al. (2008); originally adapted from Shannon (2006). ER, event-related; HFC, hippocampal functional connectivity.

TABLE 3 

 

Table 3. Core cortical components active in the default mode network.

Activation likelihood estimation (ALE) meta-analysis

We used a quantitative, random-effects meta-analytic method known as activation likelihood estimation (ALE) (Turkeltaub et al., 2002; Laird et al., 2005; Eickhoff et al., 2009, 2012) implemented in the software program GingerALE 2.1 (San Antonio, TX: UT Health Science Center Research Imaging Institute). The most recent ALE algorithm tests for above-chance clustering of peak foci from different experiments included in the meta-analysis (Eickhoff et al., 2009, 2012) by comparing actual activation foci locations/clustering with a null distribution created by distributing the same number of foci randomly throughout the brain, through several thousand iterations. Included activation foci were smoothed using a full-width half maximum (FWHM) Gaussian kernel dependent on the sample size (subjects) of the experiment from which foci were drawn [larger sample -> smaller smoothing kernel—empirically determined by (Eickhoff et al., 2009, 2012)]. Resulting statistical maps show clusters where convergence between activation foci is greater than would be expected by chance (i.e., if foci from each experiment were distributed independently).

For REM sleep, we meta-analyzed a total of 67 foci drawn from 6 studies (Table A1), which yielded 17 meta-analytic results (Table 2; 10 activations, 7 deactivations). Statistical maps were thresholded using a false discovery rate (FDR—Genovese et al., 2002) of q = 0.05 and a cluster threshold of k= 100 mm3. To display results, we used template brain images from GingerALE 2.1 displayed in the “Mango” software package (San Antonio, TX: UT Health Science Center Research Imaging Institute). No ALE meta-analysis of MW was undertaken (for reasons given in “Study Selection,” above). 

Neuroimaging of Mind Wandering and Dreaming: Meta-Analytic Results 

ALE Meta-Analysis of REM Sleep

We observed 8 significant cortical clusters of activation (REM sleep > waking rest) associated with REM sleep, as well as 2 subcortical clusters in the brainstem (pons) and caudate nucleus (Table 2 and Figure 1). Of the 8 cortical clusters, 7 overlapped with key regions of the DMN (Table 2: convergences in bold font; compare with Table 3). We also observed 7 significant cortical clusters of deactivation (REM sleep < waking rest). Except for one area of overlap with the DMN in the mid/posterior cingulate cortex, almost all deactivations were in prefrontal areas. 

Core Cortical Components of the Default Mode Network

We identified 8 core cortical regions of the default mode network (Table 3and Figure 2) based on a recent authoritative review (Buckner et al., 2008; see also Methods). 

Discussion: The Stream of (Spontaneous) Thought and its Functions

“Imagery [i.e., spontaneous thoughts and fantasies] thus needs to be seen within this context–it is not simply produced under conditions of demand by tasks of learning or recall, but it almost continuously emerges into consciousness, probably as a feature of the very nature of the brain's function and of man as a plan-making organism”—Singer and Antrobus (1972, p. 176–177).

The appellation “daydreaming,” often used interchangeably with “mind wandering,” highlights the folk psychological similarity between MW and dreaming evident even in our language. Here we have provided evidence that both quantitative meta-analysis and qualitative comparisons support this ostensibly facile analogy. Our results suggest significant similarities in both the subjective content and neurophysiological signatures of these two apparently distinct states, amplifying observations and theoretical accounts of our own (Christoff et al., 2011; Domhoff, 2011) and others (Pace-Schott, 2007, 2011).

The idea that dreaming and MW may lie on a single continuum has a number of precedents. Freud (1908), for instance, saw dreams, daydreams and creative endeavors as reflections of the same underlying processes. More recently, we have explored the idea that dreaming may share the same associative mechanisms and recruit the same neural networks (particularly the DMN) as daydreaming (Christoff et al., 2011; Domhoff, 2011). Others have also proposed an uninterrupted mental continuum between very focused waking thought, waking MW, and fully immersive dreaming (Hartmann, 1996; see also Windt, 2010). Below, we expand on this idea of a continuum in our discussion of our qualitative and meta-analytic results. We also address limitations of the present meta-analysis, potential functions of spontaneous thought in both waking and dreaming, and future directions. 

Meta-Analysis of Cortical Activity During REM Sleep

To our knowledge, the present paper is the first to conduct a quantitative meta-analysis of functional neuroimaging studies of REM sleep. Based on data from six studies of essentially “pure” REM sleep (no extraneous stimuli or tasks, healthy non-clinical populations, comparison to waking baseline), we found 10 meta-analytic clusters of significant activation (REM > waking rest). As noted by the authors of the original studies, activated regions are highly consistent with the subjective aspects of dreaming. Clusters were observed in numerous high-level visual areas, such as the parahippocampal place area, fusiform gyrus, and lingual gyrus, consistent with the ubiquitous, immersive visual imagery characteristic of dreams. Regions implicated in long-term and episodic memory, as well as in imagining future scenes and situations (Schacter et al., 2007), are also active, including parahippocampal cortex, hippocampus, and entorhinal cortex. Finally, multiple clusters were observed in mPFC regions, which, most relevant to the present results, have been strongly implicated in self-referential thought and affective decisions (Raichle et al., 2001; Buckner et al., 2008; Andrews-Hanna et al., 2010). We also found several (7) clusters of deactivation, mostly in the frontal lobe—consistent with prior accounts (e.g., Muzur et al., 2002). 

Overlapping and Non-Overlapping Patterns of Brain Activity in the DMN and REM Sleep

When we compared our meta-analytic results for REM sleep to core regions of the DMN, we found substantial overlap. Specifically, of the 8 significant cortical clusters of activation identified in our ALE meta-analysis of REM sleep, all but one overlapped to at least some extent with core regions of the DMN. The most complete overlap is apparent in regions of mPFC and medial temporal lobe (MTL) structures, including parahippocampal, hippocampal, and entorhinal cortices (Table 2 and Figure 1). Importantly, other sleep stages show mostly deactivations compared to waking baselines, and generally in regions outside the DMN (e.g., Kaufmann et al., 2006). This suggests that the observed overlap with the DMN is not common to all sleep stages, but specific to REM sleep—the only sleep stage truly reliably associated with dream mentation.

The overlap is of course far from perfect (compare Table 2 and Figure 1with Table 3 and Figure 2). Several regions beyond the DMN are evident in our results (fusiform gyrus, parahippocampal place area [PPA], and lingual gyrus). Conversely, several regions of the DMN are represented poorly (posterior cingulate cortex [PCC]) or not at all (inferior parietal lobule [IPL], lateral temporal cortex [LTC]) in our tentative REM sleep map. The most easily explained discrepancy is that numerous REM clusters extend beyond DMN regions to include cortical regions well known to be involved in high-level visual processing, such as the fusiform gyrus, PPA, and lingual gyrus. Such results are consistent with the highly visual nature of dreaming, and with our hypothesis (see below) that dreaming can be considered an intensified version of spontaneous waking thoughts (which are only moderately visual in nature—see Section First-person Reports of Content from Mind Wandering and Dreaming). Another discrepancy is in PCC. REM sleep meta-analysis revealed a large (656 mm3) cluster of activation in the area of the right PCC, but this cluster extended largely into the lingual gyrus (BA 19), and was more lateral than typical activations in DMN (e.g., Buckner et al., 2008) and during MW (e.g., Christoff et al., 2009). We also found a large (752 mm3) cluster of deactivation in the area of the mid/posterior cingulate cortex. Further, the IPL was not observed at all in our meta-analytic REM sleep results.

Due to their rich reciprocal anatomical connections and strong functional connectivity with MTL structures, the PCC and IPL have been hypothesized to be involved in accessing episodic/autobiographical memories during spontaneous thought (Andrews-Hanna et al., 2010). These parietal regions may direct attention to such memories and make them available to higher cortical (e.g., prefrontal) regions, whereby they reach conscious awareness. If tenable, this putative role for PCC and IPL in spontaneous thought may in part explain the observed discrepancies in brain activation between REM sleep and the DMN. Though dreaming clearly draws on both long-term and recent memories (Section First-person Reports of Content from Mind Wandering and Dreaming), dream mentation almost never involves replay of particular episodic memories (Fosse et al., 2003). Moreover, the general lack of self-knowledge in dreams and the frequent failure to note abnormalities that an intact memory might easily notice (such as the appearance of deceased relatives), are well known phenomena. Finally, dreams are notoriously difficult to recall, even with regular practice, and especially after any significant delay. All the above considerations are consistent with a general disconnect during dreaming between highly active memory centers in the MTL and relatively quiescent hubs in the PCC and IPL of the parietal lobe.

Another possibility is that DMN regions we failed to detect in our meta-analysis (in particular, IPL and LTC) are indeed active during REM sleep, but are simply no more active than during waking rest—the baseline condition with which REM sleep was compared. Because studies of REM sleep have relied on simple contrasts (REM > waking rest), these regions could be just as active during REM sleep as during waking rest (and therefore, presumably, spontaneous thought). The lack of significantly greater activity, however, would prevent their detection either in the original REM sleep studies or in our meta-analysis (though this would not explain the cluster of deactivation we observed in mid-PCC). At present, available data cannot address this possibility, but one option for future research would be to carefully examine functional connectivity between regions active in REM sleep, to determine whether other areas (possibly IPL and LTC) are implicated. This strategy has been used to further explore regions involved in the DMN, and has led, e.g., to the conviction that, despite earlier ambiguity, medial temporal lobe structures are indeed a critical component (Buckner et al., 2008).

Aside from comparing overlap between regions key to both REM sleep and DMN activity, also of interest is the converse comparison: examining brain regions unrelated to dreaming and their potential overlap (or lack thereof) with DMN areas. In an exhaustive study relating brain lesion locus to dreaming in 332 neuropsychological patients, Solms (1997) found that 200 patients reported no changes in dream mentation. In support of our central hypothesis, lesions among these patients were primarily in sensorimotor cortices and dorsolateral PFC (Solms, 1997), none of which appear to be key to REM sleep (Table 2) or DMN functioning (Table 3).

Finally, we observed a number of significant clusters of deactivation (REM < waking rest), nearly all of which were in lateral PFC regions, including left RLPFC and bilateral orbitofrontal cortex. These regions have been strongly implicated in top-down regulation of emotion, cognitive control, and metacognitive monitoring (e.g., Christoff and Gabrieli, 2000), and are among the key areas that become more active with a variety of effortful, top-down tasks, as compared to the resting state. This suggests a trend of decreasing PFC activity from waking thought, through MW, to dreaming (see below, and Figure 3).

FIGURE 3 

 

Figure 3. Tentative model of dreaming as intensified mind wandering. A preliminary model of dreaming as an intensified version of waking mind wandering. Intensity of audiovisual imagery, number of bizarre or implausible elements, and activity in DMN regions all appear to increase from waking, goal-directed thought, through waking spontaneous thoughts, to dream mentation. The opposite trend may hold for activity levels in prefrontal executive regions such as anterior cingulate cortex and dorsolateral prefrontal cortex, which are highly active in goal-directed waking thoughts and tasks, only somewhat active during mind wandering (Christoff et al., 2009), and mostly quiescent during dreaming/REM sleep (Table 2). Solid lines represent subjective, experiential elements; dashed lines represent brain activity levels as measured by regional cerebral blood flow using PET, or BOLD (blood-oxygen-level-dependent) signal using fMRI. DMN, default mode network; PFC, prefrontal cortex.

Dreaming as Intensified Mind Wandering: Evidence From First-Person Reports

In many ways, first-person experiences in both states are similar: dreams and spontaneous thoughts are both likely (~20–30% of reports) to contain bizarre or implausible elements, to contain positive or negative emotion (~60–80% of reports), to draw on proximal and distal memory sources, to relate strongly to subjects' current concerns, and to involve simulated social interaction. Differences are apparent in other respects, however, and we argue that each difference suggests a greater preponderance or “intensity” of a given element in dreaming. First, the sensory aspects of dreams are far more immersive and intense than during waking spontaneous thought. Waking spontaneous thoughts tend to be tinged with audiovisual aspects, which typically coincide with some level of awareness of the external environment and sensory inputs. In dreaming, conversely, external sensory inputs are almost entirely blocked, and the audiovisual content can take on the aspect of an immersive, three-dimensional simulated reality. Second, the potential for bizarre or impossible content seems not only more common but more intense in dreams, though the debate over how to measure “bizarreness” makes strong claims impossible in this respect. Third, dreams appear to be temporally extended, fairly cohesive narratives spanning several minutes or longer, whereas waking MW thoughts typically only last for several seconds (Klinger, 1978). Fourth, a recent study examining the memory sources of dreams found that a substantial amount of dream content that was traceable to waking experience (~39% of memory sources) was in fact “replay” or recall of waking thoughts, as opposed to perceptions or other experiences (Fosse et al., 2003), further suggesting that dreaming amplifies and intensifies waking thoughts. Taken together, these findings (as well as our meta-analytic neuroimaging results—see next section) support the idea that dreaming can be seen as an intensified version of waking spontaneous thought—or conversely, that MW during wakefulness could be seen as an attenuated, waking form of dreaming (or, as its colloquial moniker suggests, “daydreaming”) (see Figure 3). 

Neural Evidence for Dreaming as Intensified Mind Wandering

To ensure a consistent picture of REM sleep brain activity, we only included in our meta-analysis studies that used relaxed wakefulness (instead of, e.g., other sleep stages) as a baseline condition. Thus the activations observed in REM sleep (Table 2) are in contrast to quiet, waking rest, which—though not directly examined in the studies in question—would very likely have resulted in spontaneous thought/MW at the subjective level, and recruited DMN brain regions. Since the observed foci of activation generally represent t-tests contrasting REM sleep > waking rest, it seems probable that our meta-analytic results actually represent regions showing greateractivity during REM sleep than during DMN activation/MW. Because so many significant clusters for REM sleep activation overlapped with DMN regions, these results suggest that brain activity in REM sleep does not simply parallel DMN activity, but rather represents an intensified version of it (Figure 3). The finding of greater cerebral blood flow in DMN regions during REM sleep vs. probable waking DMN activity is consistent with the many qualitative, first-person results discussed above (Section First-person Reports of Content from Mind Wandering and Dreaming), which suggest that mentation during REM sleep is in many ways a longer, immersive, more intensive version of waking spontaneous thoughts and daydreams (Figure 3).

Also of interest are prefrontal cortical (PFC) regions, involved in executive processes like cognitive control and goal-directed thought. It is well known that numerous such regions, particularly the anterior cingulate cortex (ACC) and dorsolateral PFC (DLPFC), are consistently engaged by effortful, goal-directed tasks (Duncan and Owen, 2000). Though executive PFC regions are not part of the canonical DMN (Table 3; Buckner et al., 2008), more direct, online assessments of MW, using first-person reports combined with fMRI, show that executive PFC areas, alongside core DMN areas, may also be activated during MW (Christoff et al., 2009). Though MW-related activity was not observed in some other PFC regions, robust activation was found in dorsal ACC and DLPFC (Christoff et al., 2009), suggesting that executive processes may to some degree be ongoing during MW. REM sleep, in contrast, shows no such activations; indeed, we found numerous executive PFC regions to be deactivated (Table 2, Figure 1). We propose the tentative notion that waking thought, waking MW, and dream mentation may lie along a continuum of intensity with respect to executive function, as well: executive regions are most active during waking goal-directed thought, undergo a large (but probably not total) diminution during waking rest/MW, and become relatively quiescent, perhaps even actively suppressed, during REM sleep (Figure 3; see also Christoff et al., 2011). 

Putative Functions of Spontaneous Thought During Wakefulness and Sleep

Numerous reviews have recently examined potential functions of spontaneous thought/DMN (Buckner et al., 2008; Klinger, 2008; Christoff et al., 2011; Andrews-Hanna, 2012) and dreaming/REM sleep (e.g.,Domhoff, 2003; Deseilles et al., 2011, Ch. 6), so we offer only a brief overview of key ideas here. Despite sparse empirical data overall, discussion of functionality seems to us necessary because brains, particularly those as large as the ones possessed by homo sapiens, are very metabolically expensive organs to maintain, consuming an egregiously disproportionate share of the body's energy when compared to their relative mass (roughly 15–20% of the body's basal metabolic energy expenditure for a mere ~2% of its body mass: Aiello and Wheeler, 1995). The large amount of time spent in REM sleep (~1.5–2 h per night) and the prevalence of MW during wakefulness (~30–50% of waking thought) collectively suggest that a non-trivial proportion of this metabolic energy is dedicated to spontaneous thought in one form or another, inviting the question of what biological-evolutionary function the latter might serve.

One major theory is that spontaneous thought involves goal-oriented (if still somewhat “undirected”) processing of current concerns and planning for the future (Buckner et al., 2008; Klinger, 2008; Baird et al., 2011;Stawarczyk et al., 2011; Andrews-Hanna, 2012; Mooneyham and Schooler, 2013). This notion is consonant with the large amount of subjective content focused on imagined future scenarios and with the high prevalence of subjects' current concerns in content reports of both dreams and waking MW (Section First-person Reports of Content from Mind Wandering and Dreaming). On this view, a major function of the brain when not strongly occupied by external stimuli is to address current issues and plan for future events, both expected and hypothetical. This process would likely involve the recombination of episodic and semantic memories to yield plausible future scenarios, explaining in part the large proportion of past-oriented thought evident in both waking and sleeping spontaneous thought.

A second possibility, complementary to the first, is that of offline memory consolidation and reconsolidation (Christoff et al., 2011). Memory traces are known to be reactivated during REM sleep, both in terms of replay of neural activity sequences as observed with single-cell recordings in rats (Wilson and McNaughton, 1994), and reactivation of regions shown to be active during learning, as revealed by fMRI in human subjects (Maquet et al., 2000). Intriguingly, very similar results have been found during periods of wakefulness after training, again at the single-cell level in rats (Sutherland and McNaughton, 2000; Foster and Wilson, 2006) and at the regional level with fMRI in humans (Peigneux et al., 2006). Collectively, these results suggest that the subjective experiences of wakeful MW and dream mentation may represent, at least in part, the phenomenal side of an underlying brain process involving memory consolidation and reconsolidation (see Christoff et al., 2011, for a more detailed discussion).

A third idea, oft-reported anecdotally but difficult to demonstrate experimentally, is that dreams and daydreams serve to facilitate creativity, insight, and problem-solving, sometimes explained via the mechanism of “incubation” (Schredl and Erlacher, 2007; Baird et al., 2012). Though intriguing, support for this idea remains mostly anecdotal (see Introduction; also Csikszentmihalyi, 1996). Experimental studies have begun to address this question, however (e.g., Baird et al., 2012), and a recent fMRI study from our group found higher activity in DMN regions (hippocampus, parahippocampus, and inferior parietal lobule—all bilaterally) during the generation of creative artwork (Ellamil et al., 2012). 

Limitations

Several limitations of the present review and meta-analysis should be acknowledged. First and most important is the use of DMN and REM sleep brain activity as neuromarkers for MW and dreaming, respectively. Though both pairs of states are tightly coupled, as outlined in detail above, it should be stressed that they are by no means identical. We therefore anticipate that in the future, more specific neuroimaging work will directly target MW and dreaming, as distinct from DMN and REM sleep activity, respectively, both extending and improving upon the present preliminary results. This issue is considered in greater detail in the Methods section above.

Second, though the meta-analytic neural substrate of dreaming overlaps considerably with that of the DMN, many activation clusters extend beyond DMN hubs. These discrepancies may be due in part to noise attributable to the small sample size of REM studies (6 reports), but they likely also reflect real brain substrate differences between these two states. In our view, some of these differences are consonant with the aforementioned “intensity” hypothesis; others, however (e.g., minimal PCC, and total lack of IPL and LTC activations in REM sleep) may point toward either genuine differences in neural substrate, or possibly very similar levels of activity indistinguishable by subtraction contrasts (REM > waking rest, or waking rest > REM).

Third, despite many experiential and neural similarities, dreaming is predictably engaged in for long periods each night (several minutes to over an hour) throughout the sleep cycle, particularly during REM sleep (Aserinsky and Kleitman, 1953; Dement and Kleitman, 1957), whereas daydreaming tends to be more sporadic and short-lived, and is most commonly occasioned by low external task demands (Antrobus et al., 1966), among other factors (Smallwood and Schooler, 2006). The mechanisms of initiation, and/or impetus for the content reaching conscious awareness, may therefore be distinct.

Fourth, the neurochemical dynamics of REM sleep differ markedly from those of normal waking (Solms, 2002). It may be that the neurochemistry of MW and/or quiet waking rest differs from that of normal waking, and might even resemble that of REM sleep—or lie somewhere between the two. To our knowledge, this remains a largely unexplored question (though see Christoff et al., 2011, for a discussion), but it seems probable that the neurochemical basis of waking rest and/or MW will differ in important ways from the exceptional neurochemistry of REM sleep.

Fifth, all the studies in our meta-analysis of REM sleep employed PET imaging (the incredible noise created by fMRI scanners make sleep studies difficult), whereas all the studies included in the meta-analysis of Buckner et al. (2008) to identify core regions of the DMN (Table 3) employed fMRI. Although this presents the possibility of systematic confounding differences, data from both modalities is routinely pooled together in meta-analyses and reviews. Further, for the DMN at least, studies have been conducted using both modalities with similar results. Indeed, the early work (e.g.,Andreasen et al., 1995; Raichle et al., 2001) upon which all subsequent investigation of the DMN has been based used exclusively PET imaging; much subsequent work with fMRI, however, has largely confirmed these early PET results (see Buckner et al., 2008), reinforcing the idea of a certain degree of comparability across these two modalities. 

Future Directions

The relation between brain activity across sleep stages, the associated subjective content related to each stage, and the potential involvement of the DMN remain open and intriguing questions for future research. Interestingly, other sleep stages (beyond REM) show evidence for dream-like mentation to varying degrees, with late-night NREM2 and a brief epoch at sleep onset (NREM1) of particular interest, whereas other stages (early-night NREM2 and NREM3/4 or SWS) are associated with little subjective experience. Intriguingly, some studies have shown decreased DMN functional connectivity across various NREM sleep stages (Horovitz et al., 2009; Sämann et al., 2011), consistent with our central hypothesis; others, however, find more complex relationships among subsets of the DMN (Koike et al., 2011). Research also continues apace into functional connectivity among various other brain regions and networks (other than the DMN) throughout the sleep cycle (e.g., Horovitz et al., 2008; Larson-Prior et al., 2009), further complicating the picture.

One particular case allows for a fairly straightforward prediction, however: late-night/early-morning NREM2 laboratory awakenings give rise to more, and more dream-like, mentation reports than awakenings from NREM2 cycles early in the night (Antrobus et al., 1995; Cicogna et al., 1998). Though REM is the predominant sleep stage later in the night, presenting a potential confound, these qualitative results nonetheless suggest that late- vs. early-night NREM2 sleep may show distinctive patterns of brain activity, though to our knowledge this has yet to be examined with functional neuroimaging. Based on first-person reports and the present meta-analytic results, we hypothesize that late-night NREM2, if isolable, may show brain activity similar to the DMN and REM sleep (see also Domhoff, 2011).

Comprehensive testing of the various theoretical accounts of putative functionality for spontaneous thought and dreaming is also important. Though at least some spontaneous thoughts seem of undeniable value to individuals, there appear too to be many less-than-useful thoughts, and incoherent dreams. Future work can address this issue by exploring differential neural correlates and subjective qualities of dreams and spontaneous thoughts related to any number of factors of interest, such as creativity and planning for the future (see, e.g., Andrews-Hanna et al., 2010; Stawarczyk et al., 2011).

Clearly, much work remains to be done in elucidating the connections between MW, dreaming, REM sleep and the DMN. In particular, future work should further examine spontaneous thoughts from both wakefulness and sleep stages in the same subjects to allow for direct comparisons of first-person reports. Ideally, such studies could also compare DMN activity and REM sleep activation in the same subjects, as well.

Though subjective content reports have long suggested similar neural processes underlying dreaming and waking MW, here we have presented the first strong neuroimaging evidence that this is indeed the case. We hope that subsequent behavioral and neuroimaging research, ideally conducted in conjunction with detailed first-person reports, will increase our knowledge of these still poorly understood mental states, and amplify the present finding of their shared neural basis.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. 

Acknowledgments

The authors would like to thank two independent reviewers for thorough, thoughtful, and constructive critiques of the original manuscript. We also thank Dr. Randy L. Buckner for his kind permission to reproduce an excellent figure (Figure 2 in this paper). Last but not least, we extend our gratitude to Dr. Keith Lohse for a careful reading of, and conscientious comments upon, the manuscript. This work was supported in part by a grant from the Natural Sciences and Engineering Research Council (NSERC) of Canada to Kalina Christoff, and an NSERC Vanier Canada Graduate Scholarship to Kieran C. R. Fox. 

References available at the Frontiers site.