Discrete Neural Signatures of Basic Emotions Saarimäki, Heini; Gotsopoulos, Athanasios; Jääskeläinen, Iiro P ...
Cerebral cortex (New York, N.Y. 1991),
06/2016, Volume:
26, Issue:
6
Journal Article
Peer reviewed
Open access
Categorical models of emotions posit neurally and physiologically distinct human basic emotions. We tested this assumption by using multivariate pattern analysis (MVPA) to classify brain activity ...patterns of 6 basic emotions (disgust, fear, happiness, sadness, anger, and surprise) in 3 experiments. Emotions were induced with short movies or mental imagery during functional magnetic resonance imaging. MVPA accurately classified emotions induced by both methods, and the classification generalized from one induction condition to another and across individuals. Brain regions contributing most to the classification accuracy included medial and inferior lateral prefrontal cortices, frontal pole, precentral and postcentral gyri, precuneus, and posterior cingulate cortex. Thus, specific neural signatures across these regions hold representations of different emotional states in multimodal fashion, independently of how the emotions are induced. Similarity of subjective experiences between emotions was associated with similarity of neural patterns for the same emotions, suggesting a direct link between activity in these brain regions and the subjective emotional experience.
Rapid interruption of ongoing motor actions is crucial to respond to unexpected and potentially threatening situations. Yet, it remains unclear how motor inhibition interacts with emotional ...processes. Here we used a modified stop-signal task including an emotional component (fearful faces) to investigate whether neural circuits engaged by action suppression are modulated by task-irrelevant threat-related signals. Behavioral performance showed that reaction times were prolonged in the presence of incidental threat information, and this emotional slowing was enhanced when incorrect responses were made following stop signals. However, the speed and efficacy of voluntary inhibition was unaffected by emotion. Brain imaging data revealed that emotional cues during stop trials interacted with activity in limbic regions encompassing the basal amygdala and sublenticular extended amygdala region, as well as with the supplementary motor area (SMA). In addition, successful motor inhibition to threat signals selectively recruited a region in lateral orbitofrontal cortex, distinct from areas in inferior frontal gyrus typically associated with voluntary inhibition. Activity in primary motor cortex was lower when incorrect responses were made on stop signal trials accompanied by a fearful face, relative to neutral, in parallel with the slower response times observed behaviorally. Taken together, our findings suggest that the amygdala may not only promote protective motor reactions in emotionally-significant contexts (such as freezing or defensive behavior) but also influence the execution of ongoing actions by modulating brain circuits involved in motor control, so as to afford quick and adaptive changes in current behavior.
► Emotions may entail changes or suppression of ongoing actions ► Interactions between fear and motor control were tested in a stop-signal task ► Fear modulated motor responses via amygdala, lateral orbitofrontal cortex, and SMA ► 3An interaction between threat and stop signals arose in the sublenticular amygdala
Basic emotional states (such as anger, fear, and joy) can be similarly conveyed by the face, the body, and the voice. Are there human brain regions that represent these emotional mental states ...regardless of the sensory cues from which they are perceived? To address this question, in the present study participants evaluated the intensity of emotions perceived from face movements, body movements, or vocal intonations, while their brain activity was measured with functional magnetic resonance imaging (fMRI). Using multivoxel pattern analysis, we compared the similarity of response patterns across modalities to test for brain regions in which emotion-specific patterns in one modality (e.g., faces) could predict emotion-specific patterns in another modality (e.g., bodies). A whole-brain searchlight analysis revealed modality-independent but emotion category-specific activity patterns in medial prefrontal cortex (MPFC) and left superior temporal sulcus (STS). Multivoxel patterns in these regions contained information about the category of the perceived emotions (anger, disgust, fear, happiness, sadness) across all modality comparisons (face-body, face-voice, body-voice), and independently of the perceived intensity of the emotions. No systematic emotion-related differences were observed in the overall amplitude of activation in MPFC or STS. These results reveal supramodal representations of emotions in high-level brain areas previously implicated in affective processing, mental state attribution, and theory-of-mind. We suggest that MPFC and STS represent perceived emotions at an abstract, modality-independent level, and thus play a key role in the understanding and categorization of others' emotional mental states.
Motor inhibition in hysterical conversion paralysis Cojan, Yann; Waber, Lakshmi; Carruzzo, Alain ...
NeuroImage (Orlando, Fla.),
September 2009, 2009-Sep, 2009-09-00, 20090901, Volume:
47, Issue:
3
Journal Article
Peer reviewed
Brain mechanisms underlying hysterical conversion symptoms are still poorly known. Recent hypotheses suggested that activation of motor pathways might be suppressed by inhibitory signals based on ...particular emotional situations. To assess motor and inhibitory brain circuits during conversion paralysis, we designed a go–nogo task while a patient underwent functional magnetic resonance imaging (fMRI). Preparatory activation arose in right motor cortex despite left paralysis, indicating preserved motor intentions, but with concomitant increases in vmPFC regions that normally mediate motivational and affective processing. Failure to execute movement on go trials with the affected left hand was associated with activations in precuneus and ventrolateral frontal gyrus. However, right frontal areas normally subserving inhibition were activated by nogo trials for the right (normal) hand, but not during go trials for the left hand (affected by conversion paralysis). By contrast, a group of healthy controls who were asked to feign paralysis showed similar activation on nogo trials and left-go trials with simulated weakness, suggesting that distinct inhibitory mechanisms are implicated in simulation and conversion paralysis. In the patient, right motor cortex also showed enhanced functional connectivity with the posterior cingulate cortex, precuneus, and vmPFC. These results suggest that conversion symptoms do not act through cognitive inhibitory circuits, but involve selective activations in midline brain regions associated with self-related representations and emotion regulation.
Abstract
Alterations in activity and connectivity of brain circuits implicated in emotion processing and emotion regulation have been observed during resting-state for different clinical phases of ...bipolar disorders (BD), but longitudinal investigations across different mood states in the same patients are still rare. Furthermore, measuring dynamics of functional connectivity patterns offers a powerful method to explore changes in the brain’s intrinsic functional organization across mood states. We used a novel co-activation pattern (CAP) analysis to explore the dynamics of amygdala connectivity at rest in a cohort of 20 BD patients prospectively followed-up and scanned across distinct mood states: euthymia (20 patients; 39 sessions), depression (12 patients; 18 sessions), or mania/hypomania (14 patients; 18 sessions). We compared them to 41 healthy controls scanned once or twice (55 sessions). We characterized temporal aspects of dynamic fluctuations in amygdala connectivity over the whole brain as a function of current mood. We identified six distinct networks describing amygdala connectivity, among which an interoceptive-sensorimotor CAP exhibited more frequent occurrences during hypomania compared to other mood states, and predicted more severe symptoms of irritability and motor agitation. In contrast, a default-mode CAP exhibited more frequent occurrences during depression compared to other mood states and compared to controls, with a positive association with depression severity. Our results reveal distinctive interactions between amygdala and distributed brain networks in different mood states, and foster research on interoception and default-mode systems especially during the manic and depressive phase, respectively. Our study also demonstrates the benefits of assessing brain dynamics in BD.
Functional connectivity (FC) as measured by correlation between fMRI BOLD time courses of distinct brain regions has revealed meaningful organization of spontaneous fluctuations in the resting brain. ...However, an increasing amount of evidence points to non-stationarity of FC; i.e., FC dynamically changes over time reflecting additional and rich information about brain organization, but representing new challenges for analysis and interpretation. Here, we propose a data-driven approach based on principal component analysis (PCA) to reveal hidden patterns of coherent FC dynamics across multiple subjects. We demonstrate the feasibility and relevance of this new approach by examining the differences in dynamic FC between 13 healthy control subjects and 15 minimally disabled relapse-remitting multiple sclerosis patients. We estimated whole-brain dynamic FC of regionally-averaged BOLD activity using sliding time windows. We then used PCA to identify FC patterns, termed “eigenconnectivities”, that reflect meaningful patterns in FC fluctuations. We then assessed the contributions of these patterns to the dynamic FC at any given time point and identified a network of connections centered on the default-mode network with altered contribution in patients. Our results complement traditional stationary analyses, and reveal novel insights into brain connectivity dynamics and their modulation in a neurodegenerative disease.
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•Data-driven approach to characterize whole-brain dynamic functional connectivity•Principal component analysis reveals connections with coherent dynamics during rest•Connectivity patterns form orthogonal building blocks of dynamic connectivity•Altered contribution of connectivity patterns in patients with multiple sclerosis
Guilt is a central moral emotion due to its inherent link to norm violations, thereby affecting both individuals and society. Furthermore, the nature and specificity of guilt is still debated in ...psychology and philosophy, particularly with regard to the differential involvement of self-referential representations in guilt relative to shame. Here, using functional magnetic resonance imaging (fMRI) in healthy volunteers, we identified specific brain regions associated with guilt by comparison with the 2 most closely related emotions, shame and sadness. To induce high emotional intensity, we used an autobiographical memory paradigm where participants relived during fMRI scanning situations from their own past that were associated with strong feelings of guilt, shame, or sadness. Compared with the control emotions, guilt episodes specifically recruited a region of right orbitofrontal cortex, which was also highly correlated with individual propensity to experience guilt (Trait Guilt). Guilt-specific activity was also observed in the paracingulate dorsomedial prefrontal cortex, a critical "Theory of Mind" region, which overlapped with brain areas of self-referential processing identified in an independent task. These results provide new insights on the unique nature of guilt as a "self-conscious" moral emotion and the neural bases of antisocial disorders characterized by impaired guilt processing.
•Selective attention is driven by several factors such as the salience of objects or expectations based on past experience.•We examined the neural substrates of the interaction between current ...attention goal and past reward learning.•We identified a key region, the frontal-eye-field, that may integrate different sources of information that ultimately guide our attention focus.
Attentional selection and the decision of where to make an eye-movement are driven by various factors such as the representation of salience, task goal, and stimulus relevance, as well as expectations or predictions based on past experience. Brain systems implicated in these processes recruit cortico-subcortical areas including the Frontal Eye-Field (FEF), parietal cortex, or superior colliculus. How these areas interact to govern attention remains elusive. Priority maps of space have been observed in several brain regions, but the neural substrates where different sources of information are combined and integrated to guide attentional selection has not been elucidated. We investigated here the neural mechanisms subserving how reward cues influence the voluntary deployment of attention, in conditions where stimulus-driven capture and task-related goals compete for attention selection. Using fMRI in a visual search task in n = 23 participants, we found a selective modulation of FEF by the reward value of distractors during attentional shifts, particularly after high-predictive cueing to invalid locations. Reward information also modulated FEF connectivity to superior colliculus, striatum, and visual cortex. We conclude that FEF may occupy a central position within brain circuits integrating different sources of top-down biases for the generation of spatial saliency maps and guidance of selective attention.
Human gaze is a critical social cue that can reveal intentions and dispositions of others. The right posterior superior temporal sulcus (pSTS) is thought to be critically involved in processing eye ...gaze information. We combined diffusion tensor imaging (DTI) and functional magnetic resonance imaging (fMRI) to identify direct neural connections of right pSTS and to determine how these connections are modulated by the social significance of perceived gaze shifts. Participants saw faces with direct or averted gaze during event-related fMRI. Half of these faces remained static, and half displayed a dynamic gaze shift either towards or away from the subject. Social attention (dynamic gaze shifts towards the observer) not only increased activity in right pSTS, but also its functional connectivity with the right anterior insula (aIns) and right fusiform gyrus (FG). However, direct fiber connections from pSTS were demonstrated by DTI for the right aIns, but not the right FG. Moreover, the right FG responded to eye motion irrespective of direction and social significance; whereas the right aIns was selectively sensitive to social significance (i.e. gaze shifts towards the observer), but not generally to eye motion. We conclude that the social aspects of mutual gaze contact are processed by direct fiber pathways between right pSTS and right aIns; whereas increased connectivity with FG could reflect an enhanced perceptual analysis of changing facial features in dynamic gaze conditions and involves indirect fiber pathways with pSTS, perhaps via motion-selective regions in middle temporal (MT) gyrus that exhibited strong white-matter connections with both pSTS and FG and could thus provide inputs to these two areas.
► First neuroimaging study examining fiber connections of the gaze processing network. ► Examination of both structural and effective connectivity of gaze processing areas. ► Social gaze is processed by direct pathways between right pSTS and right aIns.
▸ Differential impact of reappraisal and expressive suppression on brain activity. ▸ Distinct effects of emotion regulation as a function of valence and scene content. ▸ Fusiform and insula activity ...decreased during reappraisal and suppression. ▸ PFC and cingulate activity to social content decreased only during reappraisal. ▸ Lateralization effect in amygdala: reappraisal on the left, suppression on the right.
Emotion Regulation (ER) includes different mechanisms aiming at volitionally modulating emotional responses, including cognitive re-evaluation (re-appraisal; REAP) or inhibition of emotion expression and behavior (expressive suppression; ESUP). However, despite the importance of these ER strategies, previous functional magnetic resonance imaging (fMRI) studies have not sufficiently disentangled the specific neural impact of REAP versus ESUP on brain responses to different kinds of emotion-eliciting events. Moreover, although different effects have been reported for stimulus valence (positive vs. negative), no study has systematically investigated how ER may change emotional processing as a function of particular stimulus content variables (i.e., social vs. nonsocial). Our fMRI study directly compared brain activation to visual scenes during the use of different ER strategies, relative to a “natural” viewing condition, but also examined the effects of ER as a function of the social versus nonsocial content of scenes, in addition to their negative versus positive valence (by manipulating these factors orthogonally in a 2×2 factorial design). Our data revealed that several prefrontal cortical areas were differentially recruited during either REAP or ESUP, independent of the valence and content of images. In addition, selective modulations by either REAP or ESUP were found depending on the negative valence of scenes (medial fusiform gyrus, anterior insula, dmPFC), and on their nonsocial (middle insula) or social (bilateral amygdala, mPFC, posterior cingulate) significance. Furthermore, we observed a significant lateralization in the amygdala for the effect of the two different ER strategies, with a predominant modulation by REAP on the left side but by ESUP on the right side. Taken together, these results do not only highlight the distributed nature of neural changes induced by ER, but also reveal the specific impact of different strategies (REAP or ESUP), and the specific sites implicated by different dimensions of emotional information (social or negative).