Tuesday, May 04, 2010

Early brain-body impact of emotional arousal


This is a very interesting article from Frontiers in Human Neuroscience. They seem to be confirming Antonio Damasio's version of body-based feelings as the foundation for emotions.

Current research in affective neuroscience suggests that the emotional content of visual stimuli activates brain–body responses that could be critical to general health and physical disease. The aim of this study was to develop an integrated neurophysiological approach linking central and peripheral markers of nervous activity during the presentation of natural scenes in order to determine the temporal stages of brain processing related to the bodily impact of emotions. More specifically, whole head magnetoencephalogram (MEG) data and skin conductance response (SCR), a reliable autonomic marker of central activation, were recorded in healthy volunteers during the presentation of emotional (unpleasant and pleasant) and neutral pictures selected from the International Affective Picture System (IAPS). Analyses of event-related magnetic fields (ERFs) revealed greater activity at 180 ms in an occipitotemporal component for emotional pictures than for neutral counterparts. More importantly, these early effects of emotional arousal on cerebral activity were significantly correlated with later increases in SCR magnitude. For the first time, a neuromagnetic cortical component linked to a well-documented marker of bodily arousal expression of emotion, namely, the skin conductance response, was identified and located. This finding sheds light on the time course of the brain–body interaction with emotional arousal and provides new insights into the neural bases of complex and reciprocal mind–body links.

Keywords: emotion, brain-body, arousal, magneto-encephalography, skin conductance response, principal component analyses

Citation: D'Hondt F, Lassonde M, Collignon O, Dubarry A, Robert M, Rigoulot S, Honoré J, Lepore F and Sequeira H (2010) Early brain-body impact of emotional arousal. Front. Hum. Neurosci. 4:33. doi:10.3389/fnhum.2010.00033

Received: 14 October 2009; Paper pending published: 17 December 2009; Accepted: 31 March 2010; Published online: 19 April 2010.

Edited by:
Olaf Blanke, Ecole Polytechnique Fédérale de Lausanne, Switzerland; University of Geneva, Switzerland

Jane Aspell, Ecole Polytechnique Fédérale de Lausanne, Switzerland
Thomas Koenig, University Hospital of Psychiatry, Switzerland

Copyright: © 2010 D'Hondt, Lassonde, Collignon, Dubarry, Robert, Rigoulot, Honoré, Lepore and Sequeira. This is an open-access article subject to an exclusive license agreement between the authors and the Frontiers Research Foundation, which permits unrestricted use, distribution, and reproduction in any medium, provided the original authors and source are credited.

*Correspondence: Maryse Lassonde, Département de Psychologie, Université de Montréal, CERNEC, 90 Vincent d'Indy, CP 6128, succ. Centre-Ville, Montréal, Québec H3C 3J7 Canada. e-mail: maryse.lassonde@umontreal.ca
Here is the introduction to the article, which does a much better job of explaining what they are looking at here:


The classical approach to mind–body interactions considers that psychological processes modulate general health and physical disease. An integrative neurophysiological approach whereby central and peripheral markers of nervous activity are recorded could therefore help unveil the mechanisms linking brain and body in connection with a specific mental state, and this information could be used to improve health outcomes (Critchley, 2009; Lane et al., 2009). Thus, emotion appears to be a key link between mental states and physical disease (Lane et al., 2009).

This assumption first appeared in the late nineteenth century following the well-known debate between the James–Lange and Cannon–Bard theories of emotion. The James–Lange theory proposes that emotional stimuli first induce peripheral physiological variations, which occur without consciousness of affect. These bodily responses are further interpreted by the brain to produce the feeling state of an emotion (Critchley, 2009). In contrast, the Cannon–Bard theory states that the perception of emotional stimuli evokes brain responses that simultaneously but separately induce bodily responses on the one hand and subjective feeling on the other (Friedman, 2009). From this debate have emerged fundamental questions about the time course of brain and body responses to emotion as well as their role in generating feelings.

Although the James–Lange theory and its temporal aspects are counterintuitive and hardly testable, the debate it has generated versus the Cannon–Bard theory has influenced research on emotion (Lang, 1994). Importantly, a recent study suggested that peripheral physiological responses can occur before the feeling of self-generated emotions, providing support to reconsider the James–Lange theory (Damasio et al., 2000). Damasio proposed a distinction between emotions and feelings whereby emotions are “collections of responses” corresponding to external and measurable reactions expressed via the musculoskeletal system as well as internal and measurable reactions of neurovegetative, neurohormonal, and neuroimmune systems controlled by the central nervous system (Damasio, 2000). Feelings, however, correspond to the subjective experience of these emotional responses (Damasio, 1999). Damasio’s theory states that a subjective feeling emerges through the integration of these peripheral and central components of nervous activity. Emotional stimuli are processed by the anterior affective structures, including the amygdala, the temporal pole, the orbitofrontal cortex, and the ventromedial prefrontal cortex (Rudrauf et al., 2009). In these cerebral areas, amygdala activation causes bodily reactions that are mediated by changes in autonomic nervous activity (see Davis and Whalen, 2001 for a review). These body signals (or somatic markers) in turn inform the brain about changes in the internal environment, by means of a “body-loop” involving the medial prefrontal cortices, which consider these somatic markers and select the appropriate behavior in response to the environmental stimulation. Nevertheless, somatic markers can also represent the expected body reaction, involving cerebral somatosensory maps, and can more rapidly and efficiently inform the brain for decision-making purposes than the cognitive processes can (Damasio et al., 1991; Damasio, 1994, 1996, 1999).

In recent decades, the central and peripheral components of emotional processing have been extensively examined, in particular using emotional scenes taken from the International Affective Picture System (IAPS, Lang et al., 2005). This system is based on a model of emotions proposed by Lang in which emotions are defined as a function of two main dimensions: (1) arousal, which indexes the level of intensity of a given emotion, whether pleasant or unpleasant, and (2) valence, or the level of pleasantness/unpleasantness experienced (Lang et al., 1993). In response to IAPS pictures, neuroimaging studies have typically found activation in the amygdala (Lane et al., 1999; Paradiso et al., 1999; Liberzon et al., 2000, 2003; Taylor et al., 2003; Phan et al., 2004; Sabatinelli et al., 2005; Britton et al., 2006; Kensinger and Schacter, 2006) and in the medial prefrontal cortices (Lane et al., 1997, 1999; Taylor et al., 2003; Anders et al., 2004; Phan et al., 2004; Britton et al., 2006; Grimm et al., 2006; Kensinger and Schacter, 2006). At the body level, studies on the peripheral impact of emotions have shown that these emotional pictures provoke changes in autonomic activity, reflected in different physiological indices (Lang et al., 1993; Bradley et al., 2001a). In particular, skin conductance response (SCR) is central to Damasio’s somatic marker hypothesis (Critchley, 2009). During emotional stimulation, SCR amplitude increases with the subjective assessment of the emotional arousal of the stimulus, regardless of valence (Lang et al., 1993; Bradley et al., 2001a). SCRs therefore constitute a reliable autonomic marker of central activation, indexing emotional arousal and its somatovisceral impact (Sequeira et al., 2009).

We hypothesized that if body responses are involved in generating emotional feelings, this process would require detecting the emotion regardless of the valence of the visual stimulus. This emotional detection would occur at the early stages of affective visual processing, before consciousness of affect. This raises the question of the activity time course in brain areas involved in affective visual processing and the associated bodily responses. Although this information could be very useful in determining brain–body interactions during emotional processing, only rarely (e.g., neuroimagery: Fredrikson et al., 1998; Critchley et al., 2000; Liberzon et al., 2000; Williams et al., 2001; Anders et al., 2004; electrophysiology: Amrhein et al., 2004; Keil et al., 2008) have researchers concomitantly recorded central and peripheral measures of nervous activity. Importantly, only a few studies have used a high temporal resolution functional method to explore cerebral activity. For instance, Rudrauf et al. (2009) observed that early cortical responses were stronger for unpleasant stimuli, while heart beats in the first 500 ms post stimulus showed longer intervals for unpleasant than for neutral stimuli relative to the preceding beat. However, although their study explored the temporal order of brain and body responses to emotional stimulation, it did not directly correlate these responses. Moreover, the pattern of heart rate fluctuations in response to emotional stimulation presents a more complex association with affective reports than with SCRs, and appears to be affected by both emotional dimensions, namely arousal and valence (Lang et al., 1993; Bradley et al., 2001a; Critchley, 2009). Finally, the relative contributions of the sympathetic and parasympathetic nervous systems to the heart rate fluctuations observed during emotional processing are unclear (Lang et al., 1993; Bradley et al., 2001a; Ribeiro et al., 2007; Sequeira et al., 2009). Consequently, the aim of the current study was to use a high temporal resolution functional method with fairly good spatial resolution to determine the temporal stages of brain processing that are specifically related to the bodily impact of emotions, indexed by a robust peripheral marker of emotional activation. Hence, we used SCRs as they reflect the specific responses of the sympathetic nervous system to the arousal dimension of emotional processing, without direct influence of the parasympathetic system (Critchley, 2009; Sequeira et al., 2009). Thus, we combined for the first time recordings of whole head magneto-encephalogram (MEG) data with SCRs during the presentation of emotional and neutral IAPS pictures in healthy human adults.
You can read the whole article online.

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