Amygdala Mediated Connectivity in Perceptual Decision-Making of Emotional Facial Expressions

Recognizing emotional facial expressions is a part of perceptual decision-making processes in the brain. Arriving at a decision for the brain becomes more difficult when available sensory information is limited or ambiguous. We used clear and noisy pictures with happy and angry emotional expressions and asked 32 participants to categorize these pictures based on emotions. There were significant differences in behavioral accuracy and reaction time between the decisions of clear and noisy images. The functional magnetic resonance imaging activations showed that the inferior occipital gyrus (IOG), fusiform gyrus (FG), amygdala (AMG) and ventrolateral prefrontal cortex (VPFC) along with other regions were active during the perceptual decision-making process. Using dynamic causal modeling analysis, we obtained three important results. First, from Bayesian model selection (BMS) approach, we found that the feed-forward network activity was enhanced during the processing of clear and noisy happy faces more than during the processing of clear angry faces. The AMG mediated this feed-forward connectivity in processing of clear and noisy happy faces, whereas the AMG mediation was absent in case of clear angry faces. However, this network activity was enhanced in case of noisy angry faces. Second, connectivity parameters obtained from Bayesian model averaging (BMA) suggested that the forward connectivity dominated over the backward connectivity during such processes. Third, based on the BMA parameters, we found that the easier tasks modulated effective connectivity from IOG to FG, AMG, and VPFC more than the difficult tasks did. These findings suggest that both parallel and hierarchical brain processes are at work during perceptual decision-making of negative, positive, unambiguous and ambiguous emotional expressions, but the AMG-mediated feed-forward network plays a dominant role in such decisions.

[1]  Stephan Eliez,et al.  Amygdalar activation associated with positive and negative facial expressions , 2002, Neuroreport.

[2]  Sophie K. Scott,et al.  Impaired auditory recognition of fear and anger following bilateral amygdala lesions , 1997, Nature.

[3]  J. Haxby,et al.  Human neural systems for face recognition and social communication , 2002, Biological Psychiatry.

[4]  Katherine Vytal,et al.  Neuroimaging Support for Discrete Neural Correlates of Basic Emotions: A Voxel-based Meta-analysis , 2010, Journal of Cognitive Neuroscience.

[5]  Y Yonekura,et al.  An fMRI study of the functional neuroanatomy of picture encoding in younger and older adults. , 2001, Brain research. Cognitive brain research.

[6]  R. Dolan,et al.  Common effects of emotional valence, arousal and attention on neural activation during visual processing of pictures , 1999, Neuropsychologia.

[7]  E. G. Jones,et al.  A projection from the medial pulvinar to the amygdala in primates , 1976, Brain Research.

[8]  J. O'Doherty,et al.  Neural Responses during Anticipation of a Primary Taste Reward , 2002, Neuron.

[9]  K. Luan Phan,et al.  Functional Neuroimaging Studies of Human Emotions , 2004, CNS Spectrums.

[10]  H. Critchley,et al.  Explicit and implicit neural mechanisms for processing of social information from facial expressions: A functional magnetic resonance imaging study , 2000, Human brain mapping.

[11]  T. Johnstone,et al.  Human amygdala responses during presentation of happy and neutral faces: correlations with state anxiety , 2004, Biological Psychiatry.

[12]  P. Whalen,et al.  The Structural Integrity of an Amygdala–Prefrontal Pathway Predicts Trait Anxiety , 2009, The Journal of Neuroscience.

[13]  S. Hamann,et al.  Positive and negative emotional verbal stimuli elicit activity in the left amygdala , 2002, Neuroreport.

[14]  L. Swanson,et al.  What is the amygdala? , 1998, Trends in Neurosciences.

[15]  Karine Sergerie,et al.  The role of the amygdala in emotional processing: A quantitative meta-analysis of functional neuroimaging studies , 2008, Neuroscience & Biobehavioral Reviews.

[16]  Karl J. Friston,et al.  A neuromodulatory role for the human amygdala in processing emotional facial expressions. , 1998, Brain : a journal of neurology.

[17]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[18]  R. Dolan,et al.  A subcortical pathway to the right amygdala mediating "unseen" fear. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[19]  Carl Senior,et al.  Dynamic Facial Expressions Evoke Distinct Activation in the Face Perception Network: A Connectivity Analysis Study , 2012, Journal of Cognitive Neuroscience.

[20]  Karl J. Friston,et al.  Ten simple rules for dynamic causal modeling , 2010, NeuroImage.

[21]  P. Whalen Fear, Vigilance, and Ambiguity , 1998 .

[22]  R. Dolan,et al.  Emotion, Cognition, and Behavior , 2002, Science.

[23]  Luiz Pessoa,et al.  Target visibility and visual awareness modulate amygdala responses to fearful faces. , 2006, Cerebral cortex.

[24]  Dana M Small,et al.  Toward an Understanding of the Brain Substrates of Reward in Humans , 2002, Neuron.

[25]  Wasserman,et al.  Bayesian Model Selection and Model Averaging. , 2000, Journal of mathematical psychology.

[26]  A. Ohman,et al.  Automaticity and the Amygdala: Nonconscious Responses to Emotional Faces , 2002 .

[27]  Karl J. Friston,et al.  Comparing dynamic causal models , 2004, NeuroImage.

[28]  Karl J. Friston,et al.  Comparing Families of Dynamic Causal Models , 2010, PLoS Comput. Biol..

[29]  R. Desimone,et al.  Selective attention gates visual processing in the extrastriate cortex. , 1985, Science.

[30]  N. Kanwisher,et al.  The fusiform face area: a cortical region specialized for the perception of faces , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[31]  U. Noppeney,et al.  Perceptual Decisions Formed by Accumulation of Audiovisual Evidence in Prefrontal Cortex , 2010, The Journal of Neuroscience.

[32]  S. Rauch,et al.  A functional magnetic resonance imaging study of amygdala and medial prefrontal cortex responses to overtly presented fearful faces in posttraumatic stress disorder. , 2005, Archives of general psychiatry.

[33]  Adam P. Morris,et al.  Amygdala Responses to Fearful and Happy Facial Expressions under Conditions of Binocular Suppression , 2004, The Journal of Neuroscience.

[34]  A. Anderson,et al.  Neural Correlates of the Automatic Processing of Threat Facial Signals , 2022 .

[35]  J. Grafman,et al.  The Human Amygdala: An Evolved System for Relevance Detection , 2003, Reviews in the neurosciences.

[36]  Mortimer Mishkin,et al.  Evidence for the sequential participation of inferior temporal cortex and amygdala in the acquisition of stimulus-reward associations , 1981, Behavioural Brain Research.

[37]  Robert T. Schultz,et al.  Bidirectional communication between amygdala and fusiform gyrus during facial recognition , 2011, NeuroImage.

[38]  R. Desimone,et al.  High-Frequency, Long-Range Coupling Between Prefrontal and Visual Cortex During Attention , 2009, Science.

[39]  Ewald Moser,et al.  Amygdala activation and facial expressions: Explicit emotion discrimination versus implicit emotion processing , 2007, Neuropsychologia.

[40]  N. Cohen,et al.  Prefrontal regions play a predominant role in imposing an attentional 'set': evidence from fMRI. , 2000, Brain research. Cognitive brain research.

[41]  G. McCarthy,et al.  Dynamic perception of facial affect and identity in the human brain. , 2003, Cerebral Cortex.

[42]  Håkan Fischer,et al.  Enhanced amygdala responses to emotional versus neutral schematic facial expressions , 2002, Neuroreport.

[43]  I. J. Myung,et al.  When a good fit can be bad , 2002, Trends in Cognitive Sciences.

[44]  Jie Tian,et al.  Effective connectivities of cortical regions for top-down face processing: A Dynamic Causal Modeling study , 2010, Brain Research.

[45]  M. Posner The Brain and Emotion , 1999, Nature Medicine.

[46]  Jennifer A. Mangels,et al.  Predictive Codes for Forthcoming Perception in the Frontal Cortex , 2006, Science.

[47]  P. Vuilleumier,et al.  How brains beware: neural mechanisms of emotional attention , 2005, Trends in Cognitive Sciences.

[48]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[49]  Michael Davis,et al.  The amygdala: vigilance and emotion , 2001, Molecular Psychiatry.

[50]  Cheuk Y. Tang,et al.  Differential amygdala activation during emotional decision and recognition memory tasks using unpleasant words: an fMRI study , 2001, Neuropsychologia.

[51]  R. Adolphs Neural systems for recognizing emotion , 2002, Current Opinion in Neurobiology.

[52]  E. Rolls The Brain and Emotion , 2000 .

[53]  J. Driver,et al.  Modulation of visual processing by attention and emotion: windows on causal interactions between human brain regions , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[54]  Karl J. Friston Dynamic causal modeling and Granger causality Comments on: The identification of interacting networks in the brain using fMRI: Model selection, causality and deconvolution , 2011, NeuroImage.

[55]  J. Haxby,et al.  The distributed human neural system for face perception , 2000, Trends in Cognitive Sciences.

[56]  S. Rauch,et al.  Response and Habituation of the Human Amygdala during Visual Processing of Facial Expression , 1996, Neuron.

[57]  Leslie G. Ungerleider,et al.  A general mechanism for perceptual decision-making in the human brain , 2004, Nature.

[58]  Norihiro Sadato,et al.  Functional association of the amygdala and ventral prefrontal cortex during cognitive evaluation of facial expressions primed by masked angry faces: an event-related fMRI study , 2004, NeuroImage.

[59]  P. McGuire,et al.  Laterality effect on emotional faces processing: ALE meta-analysis of evidence , 2009, Neuroscience Letters.

[60]  R. Dolan,et al.  Distant influences of amygdala lesion on visual cortical activation during emotional face processing , 2004, Nature Neuroscience.

[61]  David C. Alsop,et al.  Brain Activation during Facial Emotion Processing , 2002, NeuroImage.

[62]  M. Thase,et al.  Can’t shake that feeling: event-related fMRI assessment of sustained amygdala activity in response to emotional information in depressed individuals , 2002, Biological Psychiatry.

[63]  Arne Öhman,et al.  Automaticity and the Amygdala: Nonconscious Responses to Emotional Faces , 2002 .

[64]  Karl J. Friston,et al.  Behavioral/systems/cognitive Effective Connectivity during Processing of Facial Affect: Evidence for Multiple Parallel Pathways , 2022 .

[65]  Karl J. Friston Causal Modelling and Brain Connectivity in Functional Magnetic Resonance Imaging , 2009, PLoS biology.

[66]  A. Frick,et al.  Disruption of Reconsolidation Erases a Fear Memory Trace in the Human Amygdala , 2012, Science.

[67]  S. Paradiso The Emotional Brain: The Mysterious Underpinnings of Emotional Life , 1998 .

[68]  P. Whalen,et al.  The structural and functional connectivity of the amygdala: From normal emotion to pathological anxiety , 2011, Behavioural Brain Research.

[69]  R. Adolphs,et al.  Fear and the human amygdala , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[70]  Jennifer C. Britton,et al.  Neural correlates of social and nonsocial emotions: An fMRI study , 2006, NeuroImage.

[71]  Michael Davis,et al.  The amygdala , 2000, Current Biology.

[72]  J. Haxby,et al.  Distinct representations of eye gaze and identity in the distributed human neural system for face perception , 2000, Nature Neuroscience.

[73]  C. Büchel,et al.  Modulation of connectivity in visual pathways by attention: cortical interactions evaluated with structural equation modelling and fMRI. , 1997, Cerebral cortex.

[74]  K. Luan Phan,et al.  Functional Neuroanatomy of Emotion: A Meta-Analysis of Emotion Activation Studies in PET and fMRI , 2002, NeuroImage.

[75]  J. Russell,et al.  A Role for the Human Amygdala in Recognizing Emotional Arousal From Unpleasant Stimuli , 1999 .

[76]  N. Kanwisher,et al.  Brain Imaging , 2003, Encyclopedia of Behavioral Medicine.

[77]  Qingyang Li,et al.  Emotional perception: Meta-analyses of face and natural scene processing , 2011, NeuroImage.

[78]  A. Ishai,et al.  Effective connectivity within the distributed cortical network for face perception. , 2007, Cerebral cortex.

[79]  Jason B. Mattingley,et al.  Differential amygdala responses to happy and fearful facial expressions depend on selective attention , 2005, NeuroImage.

[80]  L. Pessoa,et al.  Emotion processing and the amygdala: from a 'low road' to 'many roads' of evaluating biological significance , 2010, Nature Reviews Neuroscience.

[81]  Leslie G. Ungerleider,et al.  The neural systems that mediate human perceptual decision making , 2008, Nature Reviews Neuroscience.

[82]  Conny F. Schmidt,et al.  Face perception is mediated by a distributed cortical network , 2005, Brain Research Bulletin.

[83]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[84]  Leslie G. Ungerleider,et al.  Neural processing of emotional faces requires attention , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[85]  Karl J. Friston,et al.  Bayesian model selection for group studies , 2009, NeuroImage.