Correlating Objective Third-Person Brain fMRI Measures with Subjective First-Person Identification of Specific Somatosensory Sensations

This is a seriously geeky paper that seeks to identify and correlate objective brain imaging with subjective experiences of focused attention. Here is the major finding:

These results provide evidence that the frontopolar prefrontal cortex has dissociable functions depending on specific cognitive demands; i.e. the dorsal portion of the frontopolar prefrontal cortex in conjunction with primary somatosensory cortex, temporopolar cortex, inferior parietal lobe, hippocampus, insula and amygdala are involved in the processing of spontaneous general subjective somatosensory experiences disclosed by focused and sustained attention.

Translation: They found that a specific area of the prefrontal cortex (the dorsal portion of the frontopolar prefrontal cortex) works with other higher level brain regions (primary somatosensory cortex, temporopolar cortex, and inferior parietal lobe) as well as elements of the limbic system (hippocampus, insula and amygdala) to process focused attention on subjective somatosensory experiences.

This might seem like a whole lot of who cares, but understanding these processes might lead us to better and more effective models of somatic therapy for trauma. In trauma survivors, the connections between the limbic system (emotional processing) and the prefrontal cortex (executive functions such as planning, understanding eventual outcomes to current actions, and so forth) is often compromised in some way. Mindfulness of bodily experiences can help repair this, but knowing which other brain regions are involved might help us refine our tools to make them more effective.

Full Citation: 
Bauer CCC, Barrios FA, Díaz J-L. (2014, Aug 28). Subjective Somatosensory Experiences Disclosed by Focused Attention: Cortical-Hippocampal-Insular and Amygdala Contributions. PLoS ONE; 9(8): e104721. doi:10.1371/journal.pone.0104721

Subjective Somatosensory Experiences Disclosed by Focused Attention: Cortical-Hippocampal-Insular and Amygdala Contributions

Clemens C.C. Bauer, Fernando A. Barrios, José-Luis Díaz

Abstract

In order to explore the neurobiological foundations of qualitative subjective experiences, the present study was designed to correlate objective third-person brain fMRI measures with subjective first-person identification and scaling of local, subtle, and specific somatosensory sensations, obtained directly after the imaging procedure. Thus, thirty-four volunteers were instructed to focus and sustain their attention to either provoked or spontaneous sensations of each thumb during the fMRI procedure. By means of a Likert scale applied immediately afterwards, the participants recalled and evaluated the intensity of their attention and identified specific somatosensory sensations (e.g. pulsation, vibration, heat). Using the subject's subjective scores as covariates to model both attention intensity and general somatosensory experiences regressors, the whole-brain random effect analyses revealed activations in the frontopolar prefrontal cortex (BA10), primary somatosensory cortex (BA1), premotor cortex (BA 6), precuneus (BA 7), temporopolar cortex (BA 38), inferior parietal lobe (BA 39), hippocampus, insula and amygdala. Furthermore, BA10 showed differential activity, with ventral BA10 correlating exclusively with attention (r(32) = 0.54, p = 0.0013) and dorsal BA10 correlating exclusively with somatosensory sensation (r(32) = 0.46, p = 0.007). All other reported brain areas showed significant positive correlations solely with subjective somatosensory experiences reports. These results provide evidence that the frontopolar prefrontal cortex has dissociable functions depending on specific cognitive demands; i.e. the dorsal portion of the frontopolar prefrontal cortex in conjunction with primary somatosensory cortex, temporopolar cortex, inferior parietal lobe, hippocampus, insula and amygdala are involved in the processing of spontaneous general subjective somatosensory experiences disclosed by focused and sustained attention.

Introduction

Before attempting to explain how and why neurophysiological processes relate to consciousness traits, it seems necessary to find consistent correlations between subjective phenomenological features and brain activity patterns [1]. For example, it is now possible to correlate introspective evaluations of sensory aspects of subjective experience with imaged local brain activations [2]. Such neurophenomenological program depends on the development of dynamic approaches to cerebral activity in conjunction to standardized and rigorous measurements of subjective experience obtained from first-person reports [3], [4]. A particular difficulty concerning the subjective character of conscious experience is the neural substrate of sensorial qualia features such as color, sound, scent, taste, touch, pain, and the like [5]. It has been suggested that the ventral prefrontal cortex is necessary, but not sufficient, for the generation of subjective experiences [6]–[8] and that there may be different areas involved depending on their specific character (e.g. auditory, tactile, emotional) [9], [10]. Other studies also report signal increases in frontopolar prefrontal cortex during different self-referential processing tasks [11]–[13] and the magnitude and time course of its activation predicts whether information is consciously perceived or slips away unnoticed [6].

Bilateral activations of temporopolar cortex were found during object encoding, tactile perception and self-related processing [14]–[16]. Furthermore, the phenomenal character of perceiving some objects as different from others is associated with right temporopolar activation [15].

The ability to voluntarily direct, concentrate, and sustain attention can bring into focus and enhance bottom-up qualitative processes of either a somatosenory/external or proprioceptive/internal nature [17]–[21]. A form of insight meditation requiring sustained awareness of subtle somatic sensations spontaneously arising from different body parts increases parieto-occipital gamma activity, a marker for enhanced sensory awareness [22]. Tactile attention also biases the processing of selected stimuli relevant features by amplifying somatosensory cortex responses [23]. Attention towards particular somatic stimuli, in turn, selectively enhances domain-specific cortical representations that probably are determinant for their conscious perception [21], [24].

Based on previous studies implicating several brain regions in the generation of subjective experiences [6]–[8], [14], [15] and the evidence that top-down attention control can be used to define particular sensory targets [21], [22], [24], we hypothesized that focusing attention on subtle pre-reflective somatosensory experiences would activate frontopolar prefrontal and temporopolar cortices, and, specifically, that the objectively measured brain activity within these regions would correlate with subjective sensory experience reports.

Materials and Methods

Subjects

All subjects gave written informed consent for the experimental procedure, and the protocol follows the principles expressed in the Declaration of Helsinki and was authorized by The Bioethics Committee of the Neurobiology Institute (Comité de Bioética del Instituto de Neurobiología, Universidad Nacional Autónoma de México). After standard exclusion criteria for functional magnetic resonance imaging (fMRI) were applied, 37 healthy volunteers participated in the study (16 female and 21 male, mean age 35.58 years, SD 7.97, 14 left handed and 23 right handed). Subjects were evaluated with digital versions of the Symptom Checklist 90 and Edinburgh Inventory to exclude psychological and/or psychopathological symptoms, and to evaluate handedness [25], [26]. All subjects gave informed consent for the experimental procedure, and the protocol had IRB approval.

Experimental design

Brain activation was examined during covert focused attention directed towards either the right or left thumb under two experimental conditions: (a) External-Stimulus Condition (manual caressing of either thumb with a 2-cm sponge brush at 1–2 Hz and stimulation aftereffect) and (b) Spontaneous-Sensation Condition in absence of any external stimulation (Figure 1). Resting periods without attention tasks separated both experimental conditions. Subjects were instructed to focus their attention on either thumb during the two experimental conditions and to abstain from moving it during the whole experiment. The instructions emphasized that, in the absence of touch stimuli, the subjects should focus their attention on the spontaneous sensations arising from either thumb rather than visualizing or imagining this body part. The protocol consisted of a block design paradigm alternating between focusing of attention towards the External-Stimulus of either thumb (60 sec blue block in Figure 1) or focusing of attention towards Spontaneous-Sensation of the same body part in the absence of external stimuli (60 sec yellow block in Figure 1). The length of the blocks was decided after a pilot study where the response showed that the subjects started to feel clear and distinct sensations ~20–40 sec after the instruction. Right and left thumbs were run in separate procedures and the order of the thumb was randomly counterbalanced (Left thumb first 52%). The External-Stimulus block was further divided into a 30 sec Touch-Stimulus Condition (shown as a dark-block in Figure 1) and a 30 sec Stimulation Aftereffect Condition (shown as a light-blue block in Figure 1). External-Stimulus and Spontaneous-Sensation conditions were separated by 30 sec resting intervals to ensure no overlapping brain activity. Each run lasted 540 sec and consisted of three epochs. One epoch was a 180 sec sequence of Rest, Touch-Stimulus, Stimulation Aftereffect, Resting, and Spontaneous-Sensation. While in the scanner, the subjects received a previously agreed one-word instruction (“attention” or “rest”) via MRI compatible audio equipment (NordicNeuroLab, Bergen, Norway) directing them to focus their attention on the target thumb, or to rest. Subjects had their eyes closed during the whole experiment.

Figure 1. Single run experimental paradigm for either thumb.
Touch-Stimulus (TS, in dark-blue), Stimulation-Aftereffect (SA, in light-blue) and Spontaneous-Sensation (SS, in yellow). Focusing attention (FA, in grey) was required during every condition. No attention task was required during resting periods between conditions (gaps). doi:10.1371/journal.pone.0104721.g001

Immediately after the scanning procedure all subjects were submitted to a Phenomenology Questionnaire to assess first-person Subjective Sensations experienced during the Spontaneous-Sensation Condition. The Phenomenology Questionnaire was designed to reflect the participant's subjective assessment of their experience through all the blocks. It consisted of a qualitative free description of the experienced sensations followed by a quantitative section where attention strength and intensity of specific sensory qualia experienced across all Spontaneous-Sensation blocks were assessed by means of a 1 to 5 Likert scale (see below and Table 1 in Results section for details).

Table 1. Phenomenology Questionnaire.
doi:10.1371/journal.pone.0104721.t001

During the scanning an examiner closely monitored the subject's thumb to ensure there was no motion. If there was any perceptible movement the run was discarded. Only six runs from 3 subjects (all right handed) were discarded due to involuntary thumb movement, and the results presented were obtained from the remaining 34 subjects.

Imaging protocol

fMRI imaging was performed on a 3.0T GE MR750 instrument (General Electric, Waukesha, WI) using a 32-channel head coil. Functional imaging included 35 axial slices, acquired using a T2*-weighted EPI sequence with TR/TE 3000/40 ms, a 64×64 matrix and 4-mm slice thickness, resulting in a 4×4×4 mm³ isometric voxel. High-resolution structural 3D-T1-weighted images were acquired for anatomical localization (resolution of 1×1×1 mm³, TR = 2.3 sec, TE = 3 ms) covering the whole brain. The images were acquired with an acceleration factor = 2.

Quantitative evaluation of the Phenomenology Questionnaire

Attention strength towards each thumb was assessed with a Likert scale ranging from weak attention (1) to strong attention (5). Subject's subjective sensations scores for attention strength were used as covariates to model the attention regressor. A pilot study performed where volunteers were instructed to focus their attention on either thumb and generate an unrestricted phenomenological description revealed that the most frequently used adjectives were: pulsation, vibration, enlargement, heat, cold, shrinkage, itching, stinging, and numbness. Thus, these were the adjectives used in the subjective sensations Likert scale assessment ranging from no sensation (1) to intense sensation (5). The mean subjective sensation for all these nine somatosensory sensations was used as the covariate to model the qualia regressor (see row in Table 1 in Results section for details).

Image processing and statistical analyses

Functional image datasets were processed and analyzed with FSL 4.1.5 (FMRIB's Software Library, www.fmrib.ox.ac.uk/fsl) [27].

Preprocessing.

The skull and other non-brain areas were extracted from the anatomical and functional scans using the script brain extraction tool (BET) of FSL, motion correction using MCFLIRT [28], spatial smoothing using a Gaussian kernel of FWHM 6 mm, mean-based intensity normalization, and nonlinear highpass temporal filtering. Extracted brains of all participants were linearly registered into the brain-extracted MNI152template using a linear spatial transformation function.

First-level fMRI analysis.

Statistical analysis was performed with FMRI Expert Analysis Tool using FMRIB's Improved Linear Model (FEAT FILM) Version 5.98 with local autocorrelation correction contrasts with a significance threshold criterion of Z>2.3 with a cluster significance threshold of P<0.05 corrected for multiple comparisons [29] and using the canonical hemodynamic response function (HRF) convolved with a function longer in duration to model the entire blocks and its time derivative as basic functions. The model included the following regressors with their corresponding HRF and their temporal derivatives: Touch-Stimulus and Spontaneous-Sensation as well as stimulation-aftereffect per thumb, with motion parameters controlled for in the model. The Touch-Stimulus regressor was modeled to fit a transient response curve in accord with previous somatosensory habituation reports [30], [31] where somatosensory cortex activation peaked around 6 sec after the onset of the stimulation and then exponentially returned to baseline for the rest of the block. In this manner it was ensured that only the touch-related processes were identified and measured. The Spontaneous-Sensation regressor was modeled to fit the last 30 sec of the block, as this would have stronger correspondence to the subjective ratings (see Experimental design), and the first 30 sec were modeled as dummy condition and discarded. Although all four conditions were considered in the GLM, only the response obtained for the Spontaneous-Sensation Condition of the last thumb of each participant was assessed and correlated with the subject's Subjective Sensation scores obtained from the Phenomenology Questionnaire. The rationale is that, although two functional runs were conducted (one for each thumb), the Phenomenology Questionnaire was only conducted once at the end of the session. Due to the recency effect, responses to this Questionnaire are more applicable to the last thumb stimulated, so only data acquired from the last functional run were analyzed with the Questionnaire data.

Group-level Subjective-Sensation analysis.

To identify activations at the group-level related to attention strength and subjective-sensation for somatosensory experiences, a subjective-sensation analysis using FLAME (FMRIB's Local Analysis of Mixed Effects) was conducted using subject's subjective sensations scores as covariates to model both attention and somatosensory experience regressors (see the Quantitative evaluation of the phenomenology questionnaire and rows A and of Table 1). All group Z statistical images were thresholded at Z>2.3 (p<0 .05) to define contiguous voxel clusters. The FSL cluster correction for multiple comparisons (Gaussian-random field theory based) was set at p<0.05, whole brain correction (http://www.fmrib.ox.ac.uk/fsl) [29]. Because we did not find any frontal activation at this threshold as previously hypothesized (see Introduction), we additionally performed an exploratory whole-brain group-level analyses using an uncorrected p-value of p<0.001 with a minimum cluster size threshold (k) of 15 voxels [32], [33]. This statistical threshold is in line with the recommendations for such complex and subtle cognitive processes, as used in previous social and affective neuroscience studies [33]. Subsequently, except where indicated, and due to the documented importance of the frontopolar prefrontal cortex in the integration of multiple separate cognitive processes in the service of higher-order behavioral goals like self referential processes (i.e. mentalizing) and attention [11], we specifically explored this region using a small-volume-correction through a region of interest (ROI) approach. The frontopolar prefrontal ROIs were based on the peak activation of this exploratory whole-brain group-level analyses and the results reported in the meta-analysis in Gilbert et all 2006 that specifically relate to left frontopolar cortex activation either during attention [34]–[37] or during self referential processes (i.e. metalizing) [11]–[13]. The ROIs were defined by merging individually created ROIs of 5 voxel (10 mm) diameter spheres (~131 mm³) around each of the documented peak coordinates and our own results in order to obtain oblong ROI volumes for a) Attention of k = 725 voxels (1450 mm³) and b) Subjective Sensation of k = 500 voxels (1000 mm³) covering the left frontopolar prefrontal cortex associated with these processes (ROIs were constructed in the 2 mm MNI-152 template). The statistical significance for the ROI analysis were corrected for multiple comparisons using the false discovery rate (FDR) correction as implemented in FSL [38]. The FDR procedure ensures that on average no more than 5% of activated voxels for each contrast are expected to be false positives. The resulting peak voxel activation for either regressor was used to calculate the percent changes of BOLD signal in each subject using Featquery (part of FSL 4.1.5). These signal changes were then correlated with the subject's individual specific subjective attention strength or mean somoatosensory qualia scores of the Lickert scale using Spearman's rank correlation coefficient (see rows A and of Table 1). Results were projected onto the surface representation of the MNI-152 template with the Freesurfer suite (http://surfer.nmr.mgh.harvard.edu/) [39] for visualization purposes.

Results

Qualitative evaluation of the phenomenology questionnaire

Subject's answers for the Phenomenology Questionnaire during the Spontaneous-Sensation Condition are shown in Table 1. All subjects experienced and spontaneously expressed their subjective sensations.

Spontaneous-Sensation analysis

Sixty-eight runs (34 right thumb and 34 left thumb) from 34 subjects were included in the analysis. Figure 2 shows that, compared with the resting task-free condition (neither external touch-stimuli nor spontaneous sensations), focusing of attention to Spontaneous-Sensation showed a group activation where the peak MNI coordinates for the right thumb (Figure 2B) were found in the left primary somatosensory cortex (BA 3b: X = −58 mm, Y = 6 mm, Z = 14 mm), bilateral secondary somatosensory cortices (SII: 34, 2, 20 and −42, −2, 12), left premotor cortex (BA 6: −2, 6, 52), left parietal lobe (PL: −26, −48, 26), left Broca's area (BA 44: −48, 4, −2), anterior cingulate cortex (BA 32: −18, 14, 28) and right insula (BA 13: 38, 10, 2). Focusing attention on Spontaneous-Sensation of the left thumb (Figure 2A), showed activations in the left primary somatosensory cortex (BA 3a: −46, 4, 16), left premotor cortex (BA 6: −56, 10, 42), and left Broca's area (BA 44: −50, 6, 8). Coordinates of peak activation, cluster size and z-values for this and all subsequent contrasts are shown in Table 2.

Figure 2. Spontaneous-Sensation analysis: Overall activations associated with focusing of attention during the different phases of the experimental paradigm. A) Focusing attention on Spontaneous-Sensation of the left thumb. B) Focusing of attention on Spontaneous-Sensation of the right thumb. All statistical maps had a significance threshold of Z>2.3, with a cluster significance threshold of p<0.05 (corrected for multiple comparisons). Images are presented in radiological convention and mapped to the MNI-152 template. doi:10.1371/journal.pone.0104721.g002

Table 2. Peak voxel activation for all experiments. doi:10.1371/journal.pone.0104721.t002

The activations found during the Touch-Stimulus Condition and their relation to the activations during the Spontaneous-Sensation Condition are detailed in a separate communication [21]. It is relevant to mention here that the contralateral activation of the somatosensory cortex (BA 3a/b corresponding to the hand area) obtained during the Touch-Stimulus Condition was also observed during the Spontaneous-Sensation Condition. Additionally, a left parieto-frontal activation was detected in the first-level analysis in the right-handed subjects during the Spontaneous-Sensation Condition. This prompted us to include a sample of 14 left-handed individuals for a statistically suitable comparison, but no differences between right and left-handed subjects were found after analyzing right and left thumbs separately and between groups for details please refer to [21]. Thus, we considered both hand-dominance groups as statistically similar and the left parieto-frontal activation as a result of top-down attentional mechanisms for a discussion on this please see [21].

Subjective-Sensation analysis

Attention.

left frontopolar prefrontal cortex (ventral portion) (BA 10: −4, 66, −4; Z = 3.78, p<0.05, small-volume-FDR-corrected; red cluster in Figure 3A) was active for attention as covariate and the percentage BOLD signal change correlated positively with the subjects' subjective attention strength reports (r(32) = 0.54, p = 0.0013, Figure 3B.1) but not for subjects' subjective somatosensory experience reports (r(32) = −0.1, p = 0.563, Figure 3B.4).

Figure 3. Subjective-Sensation analysis: Significant activations and correlations for the covariates from the Phenomenology Questionnaire.
A) Attention as a covariate revealed left ventral frontopolar prefrontal cortex (BA10 in red); Subjective somatosensory experience mean as a covariate revealed (in green) left dorsal frontopolar prefrontal cortex (BA10 in green), right primary somatosensory cortex (BA2), right premotor cortex (BA 6), precuneus (BA 7), left temporopolar cortex (BA 38), right inferior parietal lober (BA 39), right hippocampus, right insula and right amygdala, and. B) Spearman's rank correlations of subjective sensation scores with % BOLD signal change of peak voxels for 1) Subjective Attention score vs. ventral BA10 L, 2) Subjective Somatosensory Experiences vs. ventral BA 10 L, 3) Subjective Attention score vs. dorsal BA10 L, 4) Subjective Somatosensory Experiences vs. dorsal BA 10 L, 5) Subjective Somatosensory Experiences vs. BA 2 R, 6) Subjective Somatosensory Experiences vs. BA 6 L, 7) Subjective Somatosensory Experiences vs.BA 7 R, 8) 6) Subjective Somatosensory Experiences vs. BA 38 L, 9) Subjective Somatosensory Experiences vs. BA 39 R, 10) Subjective Somatosensory Experiences vs. Hippocampus R, 11) Subjective Somatosensory Experiences vs. Insula R, 12) Subjective Somatosensory Experiences vs. Amygdala R. Coordinates shown are X, Y, Z in mm for the MNI152 template. Activations have a significance threshold of Z>2.3, with a cluster significance threshold of p<0.05 (corrected for multiple comparisons) except for *BA10 = small-volume-FDR-correction with p<0.05. All correlations were assessed with the Pearson product-moment correlation and assessed for outliers using Spearman's rank-order correlation. Dashed lines indicate 95% confidence intervals. doi:10.1371/journal.pone.0104721.g003

Subjective Somatosensory Experiences.

Activity in several regions covaried with subjective somatosensory experiences (Figure 3A, green clusters, all clusters corrected p<0.05). These regions include the left frontopolar prefrontal cortex (dorsal portion) (BA10: −20, 72, 8), right primary somatosensory cortex (BA 2: 28, −42), right premotor cortex (BA 6: 50, 0, 28), right precuneus (BA 7: 8, −64, 52), left temporopolar cortex (BA 38: −32, 2, −18), right inferior parietal lobe (BA 39: 46, −70, 32), right hippocampus (30, −26, −14), right insula (38, −8, 4), and right amygdala (26, −8, −18). Additionally, the percentage BOLD signal change correlated positively with the subjects' subjective somatosensory experience reports (i.e. BA10: r(32) = 0.46, p = 0.007, Figure 3B.2; BA 2: r(32) = 0.36, p = 0.039, Figure 3B.5; BA 6: r(32) = 0.38, p = 0.029, Figure 3B.6; Precuneus: r(32) = 0.37, p = 0.034, Figure 3B.7; BA 38: r(32) = 0.33, p = 0.57, ρ = 0.4, p = 0.21, Figure 3B.8; BA 39: r(32) = 0.4, p = 0.02, Figure 3B.9; Hippocampus: r(32) = 0.51, p = 0.002, Figure 3B.10; Insula: r(32) = 0.38, p = 0.028, Figure 3B.11; Amygdala: r(32) = 0.36, p = 0.039, Figure 3B.12). Additionally, ventral BA 10 (−20, 72, 8) did not correlate with subjects' subjective attention strength reports (r = −0.07, p = 0.719, Figure 3B.3). To check for outliers we ran a non-parametric correlation test for all the brain areas, i.e. Spearman's rank-order correlation, which only showed a significant change for BA 38 (see above and Figure 3B.8).

Discussion

After verifying in 34 healthy volunteers that sustained attention directed to the spontaneous sensations of either thumb in the absence of any external stimuli effectively activates brain somatosensory areas, the present results show that corresponding subjective somatosensory experiences correlate with left dorsal frontopolar prefrontal cortex, right primary somatosensory cortex, left temporopolar cortex, right inferior parietal lobe, right hippocampus, right insula and right amygdala activations. Therefore, the main hypothesis of this work was largely corroborated with the additional finding that the left frontopolar prefrontal cortex (BA 10) and the temporopolar cortex (BA 38), in conjunction with primary somatosensory (BA 2), cortex, premotor cortex (BA 6), precuneus (BA 7), inferior parietal lobe (BA 39), hippocampus, insula and amygdala are involved in general spontaneous subjective somatosensory experiences.

The results show that the frontopolar prefrontal cortex has functional subdivisions, updating previous theories [11]. In particular, we show that the dorsal part of the frontopolar prefrontal cortex is involved during subjective sensory experiences known as qualia [6]–[8] and that it is coupled with other brain areas during this process. Hence, contributing to narrow down the individual brain structures involved [9], [10], [40]. In particular, our results agree with Feinstein et al. [6] in terms that the magnitude and time course of activation within the frontopolar prefrontal cortex, medial prefrontal cortex, and the anterior cingulate predict whether information is consciously perceived or slips away unnoticed. Other studies also report signal increases in frontopolar prefrontal cortex during different self-referential processing tasks [11]–[13]. It has also been shown that synchronic frontal gamma patterns (around 40 Hz) emerge with the recognition of a 3D object from an auto-stereogram and this pattern occurred only when subjects were readily expecting the arrival of the concealed visual object (26).

We also found that the left temporopolar cortex (BA38), together with the frontopolar cortex, becomes active during both attention mechanisms and subjective experience. Since the temporopolar cortex is a convergence zone where information from sensory, association, and limbic systems is integrated [41], [42]; this activation may relate to the awareness and conscious processing of the affective component of somatosensory experiences. In agreement with this interpretation, Ramsøy et al. [14] found that object encoding evokes bilateral activations of temporopolar, perirhinal, parahippocampal cortices, hippocampus and amygdala, while D'Argembeau et al. [43] found that the temporopolar cortex along with dorsomedial prefrontal cortex, left anterior middle temporal gyrus, and right cerebellum is implicated in reflective tasks pertaining to self, another person, and social issues.

Besides frontopolar and temporopolar activation, in the present study other areas appeared to be involved in the retrieval and processing of somatosensory experiences, i.e., primary somatosensory cortex, premotor cortex, precuneus, inferior parietal lobe, hippocampus, insula and amygdala. The combined activity of these areas probably supports conscious perceptual and phenomenological awareness [44], [45]. Consequently, pimary somatosensory cortex activation suggests its causal involvement due to the nature of the attended somatosensory experiences [21], [45]. Parietal and premotor cortices have been implicated in multisensory integration, embodiment, localization and self-attribution of body parts [46]–[49] and insula activation has been implicated in the integration of interoceptive and exteroceptive signals to construct the mental self [49], [50] and amygdala activation has been found coupled to frontal brain regions when subjects involve in self-related processing [43] and is probably a key node involved in self-referential emotion processing [51]–[53]. Finally, autobiographical memory and past experiences relate to consciousness of one self, which requires hippocampal processing [54]–[57]. Even though the instructions in our study focus on actual somatosensory experiences, the activations detected in these brain areas suggests an underlying neurocognitive requirement of body-ownership and self-consciousness. Finally, the noteworthy finding that primary somatosensory cortex is activated in the absence of external stimulation by the focusing of attention on spontaneous sensory qualia verifies that selective attention controlled by top-down cognitive processes enhance bottom-up qualitative processes of somatosensory/external and proprioceptive/internal nature that normally do not elicit primary somatosensory cortex activity in absence of stimuli [17]–[20]. This spontaneously-elicited somatosensory activity is accompanied by phenomenological somatosensory qualitative experiences or qualia, some of the most characteristic and enigmatic subjective phenomena [58], but suitable to be correlated with objective measures of brain activity [59].

Within a broader perspective, the study of sensory qualia intending to match third-person fMRI brain imaging with standardized first-person somatosensory reports constitutes a particular neurophenomenological endeavor to study the neural correlates of qualitative subjective experience. In the light of the present results, the precise mechanism for the production or correspondence of subjective sensory experiences in the detected neural networks remains a challenging, but perhaps a more delimited research question.

Supporting Information

Data_S1.docx

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Data S1.

doi:10.1371/journal.pone.0104721.s001

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Acknowledgments

We are grateful to Dr. Luis Concha for his relevant comments and to Dr. G. Andrew James for his thorough and insightful review of the paper and wonderful suggestions to improve it. Also to M.Sc. Leopoldo González-Santos, M.Sc. Juan J. Ortiz, Dr. Sarael Alcauter, and Dr. Erick Pasaye for technical support.

Author Contributions

Conceived and designed the experiments: CCCB FAB JLD. Performed the experiments: CCCB FAB. Analyzed the data: CCCB FAB. Contributed reagents/materials/analysis tools: FAB. Contributed to the writing of the manuscript: CCCB FAB JLD.

References are available at the PLoS ONE site.

Rick Hanson - The Mechanisms of Upset and Emotional Hijacking

Here are two cool posts from Dr. Rick Hanson (Buddhist neuroscientist) on "The Machinery of Upset" and "Emotional Hijacking." Both of these posts deal with the survival mode of the brain, essentially the limbic system and brain stem, the parts of the brain that take over when we are triggered by a traumatic memory/experience.

At the bottom, there is also a definition of the amygdala hijack, a term coined by Daniel Goleman.

When the amygdala takes over, we become our fear. Making that fear an object of awareness is one way to break that fear trance.

The Machinery of Upset

posted on: August 4th, 2014 

(Emotional) life is great when we feel enthusiastic, contented, peaceful, happy, interested, loving, etc. But when we’re upset, or aroused to go looking for trouble, life ain’t so great.

To address this problem, let’s turn to a strategy used widely in science (and Buddhism, interestingly): analyze things into their fundamental elements, such as the quarks and other subatomic particles that form an atom or the Five Aggregates in Buddhism of form, feeling (the “hedonic tone” of experience as pleasant-neutral-unpleasant), perception, volitional formations, and consciousness.

We’ll apply that strategy to the machinery of getting upset. Here is a summary of the eight major “gears” of that machine – somewhat based on how they unfold in time, though they actually often happen in circular or simultaneous ways, intertwining with and co-determining each other.

The point of this close analysis, this deconstruction, is not intellectual understanding or theory, but increasing your own mindfulness into your experience, and creating more points of intervention within it to reduce the suffering you cause for yourself – and other people.

This will be more real for you if you first imagine a recent upset or two, and replay it in your mind in slow motion.

Appraisals

• What do we focus on, what do we pick out of the larger mosaic?
• What meaning do we give the event? How do we frame it?
• How significant do we make it? (Is it a 2 on the Ugh scale . . . Or a 10?)
• What intentions do we attribute to others?
• What are the embedded beliefs about other people? The world? The past? The future?
• In sum, what views are we attached to? -> Mainly frontal lobe and language circuits of left temporal lobe.

Self-Referencing

• Upsets arise within the perspective of “I.”
• What is the sense of “I” that is running at the time? Strong? Weak? Mistreated?
• Are you taking things personally?
• How does the sense of self change over the course of the upset (often intensifying)? -> Circuits of “self” are distributed throughout the brain.

Vulnerabilities

• We all have vulnerabilities, which challenges penetrate through and/or get amplified by (moderated by inner and outer resources).
• Physiological: Pain, fatigue, hunger, lack of sleep, biochemical imbalances, illness.
• Temperamental: Anxious, rigid, angry, melancholic, spirited/ADHD.
• Psychological: Personality, culture, effects of gender, race, sexual orientation, etc. -> Depending on its nature, a vulnerability can be embodied or represented in many ways.

Memory

• Stimuli are interpreted in terms of episodic memories of similar experiences.
• And in terms of implicit, emotional memories or other, unconscious associations. (Especially trauma)
• These shade, distort, and amplify stimuli, packaging them with “spin” and sending them off to the rest of the brain. -> Hippocampus, with other memory circuits.

Aversion

• The feeling tone of “unpleasant” is in full swing at this point, though present in the previous “gears” of survival reactivity.
• In primitive organisms – and thus the primitive circuits of our own brain – the unpleasant/ aversion circuit is more primary than the pleasant/approach circuit since aversion often calls for all the animal’s resources and approaching does not.
• Aversion can also be a temperamental tendency.
• The Buddha paid much attention to aversion – such as to ill will – in his teachings, because it is so fundamental, and such a source of suffering. -> Involves the limbic system, especially the amygdala.

Bodily Activation

• The body energizes to respond; getting upset activates the stress machinery just like getting chased by a lion.
• Sympathetic nervous system (fight-or-flight).
• Hypothalamus-pituitary-adrenal (HPA) axis.
• All this triggers blood to the large muscles (hit or run), dilates pupils (see better in darkness), cascades cortisol and adrenaline, increases heart rate, etc.
• These systems activate quickly, but their effects fade away slowly.
• There is much collateral damage in the body and mind from chronically “going to war.”

Negative Emotions

• Emotions are a fantastic evolutionary achievement for promoting grandchildren.
• Both the prosocial bonding emotions of caring, compassion, love, sympathetic joy . . .
• And the fight-or-flight emotions of fear, anger, sorrow, shame.
• Emotions organize, mobilize the whole brain.
• They also shade our perceptions and thoughts in self-reinforcing ways.

Loss of Executive Control

• The survival machine is designed to make you identify yourself with your body and your emotional reactions. That identification is highly motivating for keeping yourself alive!
• So, in an upset, there is typically a loss of “observing ego” detachment, and instead a kind of emotional hijacking – all facilitated by neural circuits in which amygdala-shaped information gets fast-tracked throughout the brain, ahead of slower frontal lobe interpretations.
• With maturation (sometimes into the mid-twenties) and with experience, the frontal (especially prefrontal) cortices can comment on and direct emotional reactions more effectively.

* * * * *

Emotional Hijacking

posted on: September 1st, 2014 

In light of the machinery of survival-based, emotional reactivity, let’s look more narrowly at what Daniel Goleman has called “emotional hijacking.”

The emotional circuits of your brain – which are relatively primitive from an evolutionary standpoint, originally developed when dinosaurs ruled the earth – exert great influence over the more modern layers of the brain in the cerebral cortex. They do this in large part by continually “packaging” incoming sensory information in two hugely influential ways:

• Labeling it with a subjective feeling tone: pleasant, unpleasant, or neutral. This is primarily accomplished by the amygdala, in close concert with the hippocampus; this circuit is probably the specific structure of the brain responsible for the feeling aggregate in Buddhism (and one of the Four Foundations of Mindfulness).

• Ordering a fundamental behavioral response: approach, avoid, or ignore. The amygdala-hippocampus duo keep answering the two questions an organism – you and I – continually faces in its environment: Is it OK or not? And what should I do?

Meanwhile, the frontal lobes have also been receiving and processing sensory information. But much of it went through the amygdala first, especially if it was emotionally charged, including linked to past memories of threat or pain or trauma. Studies have shown that differences in amygdala activation probably account for much of the variation, among people, in emotional temperaments and reactions to negative information.

The amygdala sends its interpretations of stimuli – with its own “spin” added – throughout the brain, including to the frontal lobes. In particular, it sends its signals directly to the brain stem without processing by the frontal lobes – to trigger autonomic (fight or flight) and behavioral responses. And those patterns of activation in turn ripple back up to the frontal lobes, also affecting its interpretations of events and its plans for what to do.

It’s like there is a poorly controlled, emotionally reactive, not very bright, paranoid, and trigger-happy lieutenant in the control room of a missile silo watching radar screens and judging what he sees. Headquarters is a hundred miles away, also seeing the same screens — but (A) it gets its information after the lieutenant does, (B) the lieutenant’s judgments affect what shows upon the screens at headquarters, and (C) his instructions to “launch” get to the missiles seconds before headquarters can signal “stand down!”

* * * * *

Here is a definition of the "amygdala hijack" that Daniel Goleman outlined in his seminal book, Emotional Intelligence.

Amygdala hijack

From Wikipedia, the free encyclopedia

Amygdala hijack - fear caused by optical stimulus

Amygdala hijack is a term coined by Daniel Goleman in his 1996 book Emotional Intelligence: Why It Can Matter More Than IQ.^[1] Drawing on the work of Joseph E. LeDoux, Goleman uses the term to describe emotional responses from people which are immediate and overwhelming, and out of measure with the actual stimulus because it has triggered a much more significant emotional threat.^[2]

Contents

• 1 Definition
• 2 Positive hijacks
• 3 Emotional relearning
• 5 References

Definition

From the thalamus, a part of the stimulus goes directly to the amygdala while another part is sent to the neocortex or "thinking brain". If the amygdala perceives a match to the stimulus, i.e., if the record of experiences in the hippocampus tells the amygdala that it is a fight, flight or freeze situation, then the amygdala triggers the HPA (hypothalmic-pituitary-adrenal) axis and hijacks the rational brain. This emotional brain activity processes information milliseconds earlier than the rational brain, so in case of a match, the amygdala acts before any possible direction from the neocortex can be received. If, however, the amygdala does not find any match to the stimulus received with its recorded threatening situations, then it acts according to the directions received from the neo-cortex. When the amygdala perceives a threat, it can lead that person to react irrationally and destructively.^[3]

Goleman states that "[e]motions make us pay attention right now — this is urgent - and gives us an immediate action plan without having to think twice. The emotional component evolved very early: Do I eat it, or does it eat me?" The emotional response "can take over the rest of the brain in a millisecond if threatened."^[4][5] An amygdala hijack exhibits three signs: strong emotional reaction, sudden onset, and post-episode realization if the reaction was inappropriate.^[4]

Goleman later emphasised that "self-control is crucial ...when facing someone who is in the throes of an amygdala hijack"^[6] so as to avoid a complementary hijacking - whether in work situations, or in private life. Thus for example 'one key marital competence is for partners to learn to soothe their own distressed feelings...nothing gets resolved positively when husband or wife is in the midst of an emotional hijacking.'^[7] The danger is that "when our partner becomes, in effect, our enemy, we are in the grip of an 'amygdala hijack' in which our emotional memory, lodged in the limbic center of our brain, rules our reactions without the benefit of logic or reason...which causes our bodies to go into a 'fight or flight' response."^[8]

Positive hijacks

Goleman points out that "'not all limbic hijackings are distressing. When a joke strikes someone as so uproarious that their laughter is almost explosive, that, too, is a limbic response. It is at work also in moments of intense joy."^[9]

He also cites the case of a man strolling by a canal when he saw a girl staring petrified at the water. "[B]efore he knew quite why, he had jumped into the water — in his coat and tie. Only once he was in the water did he realize that the girl was staring in shock at a toddler who had fallen in — whom he was able to rescue."^[10]

Emotional relearning

LeDoux was positive about the possibility of learning to control the amygdala's hair-trigger role in emotional outbursts. "Once your emotional system learns something, it seems you never let it go. What therapy does is teach you how to control it — it teaches your neocortex how to inhibit your amygdala. The propensity to act is suppressed, while your basic emotion about it remains in a subdued form."^[11]

References

1. Nadler, Relly. "What Was I Thinking? Handling the Hijack". Retrieved 2010-04-06.
2. "Conflict and Your Brain aka "The Amygdala Hijacking"". Retrieved 2010-04-06.
3. Freedman, Joshua. "Hijacking of the Amygdala". Retrieved 2010-04-06.^{[dead link]}
4. Horowitz, Shell. "Emotional Intelligence - Stop Amygdala Hijackings". Retrieved 2010-04-06.
5. Hughes, Dennis. "Interview with Daniel Goleman". Retrieved 2010-04-06.
6. Daniel Goleman, Working with Emotional Intelligence (1999) p. 87
7. Goleman, Emotional Intelligence p. 144
8. Rita DeMaria et al., Building Intimate Relationships (2003) p. 57
9. Goleman, Emotional Intelligence p. 14
10. Goleman, Emotional Intelligence p. 17
11. Goleman, Emotional Intelligence p. 213

Tom Ireland - What Does Mindfulness Meditation Do to Your Brain?

Via Scientific American, an article from Tom Ireland on the ways mindfulness meditation changes the brain, not least of which is shrinking the amygdala (fear and stress center) and thickening the prefrontal cortex (executive function).

What Does Mindfulness Meditation Do to Your Brain?

By Tom Ireland | June 12, 2014

The views expressed are those of the author and are not necessarily those of Scientific American.

As you read this, wiggle your toes. Feel the way they push against your shoes, and the weight of your feet on the floor. Really think about what your feet feel like right now – their heaviness.

If you’ve never heard of mindfulness meditation, congratulations, you’ve just done a few moments of it. More people than ever are doing some form of this stress-busting meditation, and researchers are discovering it has some quite extraordinary effects on the brains of those who do it regularly.

Originally an ancient Buddhist meditation technique, in recent years mindfulness has evolved into a range of secular therapies and courses, most of them focused on being aware of the present moment and simply noticing feelings and thoughts as they come and go.



Credit: Sebastien Wiertz via Flickr
It’s been accepted as a useful therapy for anxiety and depression for around a decade, and mindfulness websites like GetSomeHeadSpace.com are attracting millions of subscribers. It’s being explored by schools, pro sports teams and military units to enhance performance, and is showing promise as a way of helping sufferers of chronic pain, addiction and tinnitus, too. There is even some evidence that mindfulness can help with the symptoms of certain physical conditions, such as irritable bowel syndrome, cancer, and HIV.

Yet until recently little was known about how a few hours of quiet reflection each week could lead to such an intriguing range of mental and physical effects. Now, as the popularity of mindfulness grows, brain imaging techniques are revealing that this ancient practice can profoundly change the way different regions of the brain communicate with each other – and therefore how we think – permanently.



Mindfulness practice and expertise is associated with a decreased volume of grey matter in the amygdala (red), a key stress-responding region. (Image courtesy of Adrienne Taren)
No fear

MRI scans show that after an eight-week course of mindfulness practice, the brain’s “fight or flight” center, the amygdala, appears to shrink. This primal region of the brain, associated with fear and emotion, is involved in the initiation of the body’s response to stress.

As the amygdala shrinks, the pre-frontal cortex – associated with higher order brain functions such as awareness, concentration and decision-making – becomes thicker.

The “functional connectivity” between these regions – i.e. how often they are activated together – also changes. The connection between the amygdala and the rest of the brain gets weaker, while the connections between areas associated with attention and concentration get stronger.

The scale of these changes correlate with the number of hours of meditation practice a person has done, says Adrienne Taren, a researcher studying mindfulness at the University of Pittsburgh.

“The picture we have is that mindfulness practice increases one’s ability to recruit higher order, pre-frontal cortex regions in order to down-regulate lower-order brain activity,” she says.

In other words, our more primal responses to stress seem to be superseded by more thoughtful ones.

Lots of activities can boost the size of various parts of the pre-frontal cortex – video games, for example – but it’s the disconnection of our mind from its “stress center” that seems to give rise to a range of physical as well as mental health benefits, says Taren.

“I’m definitely not saying mindfulness can cure HIV or prevent heart disease. But we do see a reduction in biomarkers of stress and inflammation. Markers like C-reactive proteins, interleukin 6 and cortisol – all of which are associated with disease.”

Feel the pain

Things get even more interesting when researchers study mindfulness experts experiencing pain. Advanced meditators report feeling significantly less pain than non-meditators. Yet scans of their brains show slightly more activity in areas associated with pain than the non-meditators.

“It doesn’t fit any of the classic models of pain relief, including drugs, where we see less activity in these areas,” says Joshua Grant, a postdoc at the Max Plank Institute for Human Cognitive and Brain Sciences in Leipzig, Germany. The expert mindfulness meditators also showed “massive” reductions in activity in regions involved in appraising stimuli, emotion and memory, says Grant.

Again, two regions that are normally functionally connected, the anterior cingulate cortex (associated with the unpleasantness of pain) and parts of the prefrontal cortex, appear to become “uncoupled” in meditators.

“It seems Zen practitioners were able to remove or lessen the aversiveness of the stimulation – and thus the stressing nature of it – by altering the connectivity between two brain regions which are normally communicating with one another,” says Grant. “They certainly don’t seem to have blocked the experience. Rather, it seems they refrained from engaging in thought processes that make it painful.”



Credit: Balint Földesi via Flickr
Feeling Zen

It’s worth noting that although this study tested expert meditators, they were not in a meditative state – the pain-lessening effect is not something you have to work yourself up into a trance to achieve; instead, it seems to be a permanent change in their perception.

“We asked them specifically not to meditate,” says Grant. “There is just a huge difference in their brains. There is no question expert meditators’ baseline states are different.”

Other studies on expert meditators – that is, subjects with at least 40,000 hours of mindfulness practice under their belt – discovered that their resting brain looks similar, when scanned, to the way a normal person’s does when he or she is meditating.

At this level of expertise, the pre-frontal cortex is no longer bigger than expected. In fact, its size and activity start to decrease again, says Taren. “It’s as if that way of thinking has becomes the default, it is automatic – it doesn’t require any concentration.”

There’s still much to discover, especially in terms of what is happening when the brain comprehends the present moment, and what other effects mindfulness might have on people. Research on the technique is still in its infancy, and the imprecision of brain imaging means researchers have to make assumptions about what different regions of the brain are doing.

Both Grant and Taren, and others, are in the middle of large, unprecedented studies that aim to isolate the effects of mindfulness from other methods of stress-relief, and track exactly how the brain changes over a long period of meditation practice.

“I’m really excited about the effects of mindfulness,” says Taren. “It’s been great to see it move away from being a spiritual thing towards proper science and clinical evidence, as stress is a huge problem and has a huge impact on many people’s health. Being able to take time out and focus our mind is increasingly important.”

Perhaps it is the new age, quasi-spiritual connotations of meditation that have so far prevented mindfulness from being hailed as an antidote to our increasingly frantic world. Research is helping overcome this perception, and ten minutes of mindfulness could soon become an accepted, stress-busting part of our daily health regimen, just like going to the gym or brushing our teeth.



About the Author: Tom Ireland is managing editor at the Society of Biology and a freelance journalist covering mostly health, education and science. Follow on Twitter @Tom_J_Ireland.

The views expressed are those of the author and are not necessarily those of Scientific American.