Amygdala Volume Predicts Inter-Individual Differences in Fearful Face Recognition

The present study investigates the relationship between inter-individual differences in fearful face recognition and amygdala volume. Thirty normal adults were recruited and each completed two identical facial expression recognition tests offline and two magnetic resonance imaging (MRI) scans. Linear regression indicated that the left amygdala volume negatively correlated with the accuracy of recognizing fearful facial expressions and positively correlated with the probability of misrecognizing fear as surprise. Further exploratory analyses revealed that this relationship did not exist for any other subcortical or cortical regions. Nor did such a relationship exist between the left amygdala volume and performance recognizing the other five facial expressions. These mind-brain associations highlight the importance of the amygdala in recognizing fearful faces and provide insights regarding inter-individual differences in sensitivity toward fear-relevant stimuli.

[1]  C. Michel,et al.  Evidence for rapid face recognition from human scalp and intracranial electrodes , 1997, Neuroreport.

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

[3]  A. Calder.  Facial Emotion Recognition after Bilateral Amygdala Damage: Differentially Severe Impairment of Fear , 1996 .

[4]  Adam K. Anderson,et al.  Expression Without Recognition: Contributions of the Human Amygdala to Emotional Communication , 2000, Psychological science.

[5]  S Z Rapcsak,et al.  Fear recognition deficits after focal brain damage: a cautionary note. , 2000, Neurology.

[6]  Kathleen M. Thomas,et al.  Amygdala response to facial expressions in children and adults , 2001, Biological Psychiatry.

[7]  Olaf Sporns,et al.  Can structure predict function in the human brain? , 2010, NeuroImage.

[8]  P. Gosselin,et al.  Children's knowledge of facial expressions of emotions : Distinguishing fear and surprise , 1999 .

[9]  E. Fox.  Processing emotional facial expressions: The role of anxiety and awareness , 2002, Cognitive, affective & behavioral neuroscience.

[10]  Justin S. Feinstein,et al.  The Human Amygdala and the Induction and Experience of Fear , 2011, Current Biology.

[11]  John P. Aggleton,et al.  The amygdala: Neurobiological aspects of emotion, memory, and mental dysfunction. , 1992 .

[12]  F. McGlone,et al.  Stimulus‐driven and strategic neural responses to fearful and happy facial expressions in humans , 2008, The European journal of neuroscience.

[13]  N. Ambady,et al.  Effects of Gaze on Amygdala Sensitivity to Anger and Fear Faces , 2003, Science.

[14]  Bruce Fischl,et al.  Thickness of ventromedial prefrontal cortex in humans is correlated with extinction memory. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Michael Davis,et al.  The role of the amygdala in fear and anxiety. , 1992, Annual review of neuroscience.

[16]  Osamu Abe,et al.  Smaller amygdala volume and reduced anterior cingulate gray matter density associated with history of post-traumatic stress disorder , 2009, Psychiatry Research: Neuroimaging.

[17]  Francesco Fera,et al.  The Amygdala Response to Emotional Stimuli: A Comparison of Faces and Scenes , 2002, NeuroImage.

[18]  Ralph Adolphs,et al.  Fear, faces, and the human amygdala , 2008, Current Opinion in Neurobiology.

[19]  L. Goldstein.  The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction , 1992, The Yale Journal of Biology and Medicine.

[20]  Anders M. Dale,et al.  A hybrid approach to the Skull Stripping problem in MRI , 2001, NeuroImage.

[21]  Yufeng Zang,et al.  Standardizing the intrinsic brain: Towards robust measurement of inter-individual variation in 1000 functional connectomes , 2013, NeuroImage.

[22]  A W Young,et al.  Knowing no fear , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

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

[24]  Bradford C. Dickerson,et al.  Amygdala Volume and Social Network Size in Humans , 2010, Nature Neuroscience.

[25]  R. Adolphs,et al.  Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala , 1994, Nature.

[26]  A. Kling,et al.  Uncus and Amiygdala Lesions: Effects on Social Behavior in the Free-Ranging Rhesus Monkey , 1969, Science.

[27]  Tom Manly,et al.  Facial expression recognition across the adult life span , 2003, Neuropsychologia.

[28]  R. Myers,et al.  Uncus and amygdala lesions: effects on social behavior in the free-ranging rhesus monkey. , 1968, Science.

[29]  Wen-Ming Luh,et al.  Amygdala lesions disrupt modulation of functional MRI activity evoked by facial expression in the monkey inferior temporal cortex , 2012, Proceedings of the National Academy of Sciences.

[30]  Naotsugu Tsuchiya,et al.  Intact rapid detection of fearful faces in the absence of the amygdala , 2009, Nature Neuroscience.

[31]  Reginald B. Adams,et al.  A 7 Tesla fMRI Study of Amygdala Responses to Fearful Faces , 2012, Brain Topography.

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

[33]  Shichuan Du,et al.  The resolution of facial expressions of emotion. , 2011, Journal of vision.

[34]  P. Broks,et al.  Face processing impairments after encephalitis: amygdala damage and recognition of fear , 2000 .

[35]  D. Perrett,et al.  A differential neural response in the human amygdala to fearful and happy facial expressions , 1996, Nature.

[36]  Daniel S Pine,et al.  Elevated fear conditioning to socially relevant unconditioned stimuli in social anxiety disorder. , 2008, The American journal of psychiatry.

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

[38]  A. Federspiel,et al.  Spider phobia is associated with decreased left amygdala volume: a cross-sectional study , 2013, BMC Psychiatry.

[39]  M. Ernst,et al.  Gray matter volume in adolescent anxiety: an impact of the brain-derived neurotrophic factor Val(66)Met polymorphism? , 2013, Journal of the American Academy of Child and Adolescent Psychiatry.

[40]  C. Darwin.  The Expression of the Emotions in Man and Animals , .

[41]  R. Adolphs.  Recognizing emotion from facial expressions: psychological and neurological mechanisms. , 2002, Behavioral and cognitive neuroscience reviews.

[42]  Rachael E. Jack,et al.  Cultural Confusions Show that Facial Expressions Are Not Universal , 2009, Current Biology.

[43]  Xiu-Xia Xing,et al.  PDE-based spatial smoothing: a practical demonstration of impacts on MRI brain extraction, tissue segmentation and registration. , 2011, Magnetic resonance imaging.

[44]  J. Tanaka,et al.  The NimStim set of facial expressions: Judgments from untrained research participants , 2009, Psychiatry Research.

[45]  H Fischer,et al.  Differential response in the human amygdala to racial outgroup vs ingroup face stimuli , 2000, Neuroreport.

[46]  A. David,et al.  Predictors of amygdala activation during the processing of emotional stimuli: A meta-analysis of 385 PET and fMRI studies , 2008, Brain Research Reviews.

[47]  S. Rauch,et al.  A functional MRI study of human amygdala responses to facial expressions of fear versus anger. , 2001, Emotion.

[48]  D. Hedges,et al.  Hippocampal and amygdala volumes in children and adults with childhood maltreatment‐related posttraumatic stress disorder: A meta‐analysis , 2008, Hippocampus.

[49]  Nikos Makris,et al.  Automatically parcellating the human cerebral cortex. , 2004, Cerebral cortex.

[50]  J. R. Landis,et al.  The measurement of observer agreement for categorical data. , 1977, Biometrics.

[51]  P. Ekman,et al.  Detecting deception from the body or face. , 1974 .

[52]  Leslie G. Ungerleider,et al.  Perception of emotional expressions is independent of face selectivity in monkey inferior temporal cortex , 2008, Proceedings of the National Academy of Sciences.

[53]  Steven C.R. Williams,et al.  Time courses of left and right amygdalar responses to fearful facial expressions , 2001, NeuroImage.

[54]  Bradford C. Dickerson,et al.  Intrinsic Amygdala–Cortical Functional Connectivity Predicts Social Network Size in Humans , 2012, The Journal of Neuroscience.

[55]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[56]  Xi-Nian Zuo,et al.  Effects of Non-Local Diffusion on Structural MRI Preprocessing and Default Network Mapping: Statistical Comparisons with Isotropic/Anisotropic Diffusion , 2011, PloS one.

[57]  P. Ekman,et al.  A new pan-cultural facial expression of emotion , 1986 .

[58]  Yufeng Zang,et al.  Toward reliable characterization of functional homogeneity in the human brain: Preprocessing, scan duration, imaging resolution and computational space , 2013, NeuroImage.

[59]  Robert T. Knight,et al.  The influence of personality on neural mechanisms of observational fear and reward learning , 2008, Neuropsychologia.

[60]  C. Goose,et al.  Glossary of Terms , 2004, Machine Learning.

[61]  P. Ekman.  An argument for basic emotions , 1992 .

[62]  C. Spielberger,et al.  Manual for the State-Trait Anxiety Inventory , 1970 .

[63]  Seung-Hwan Lee,et al.  Psychological characteristics of early remitters in patients with panic disorder , 2012, Psychiatry Research.

[64]  A. Aleman,et al.  Extraversion Is Linked to Volume of the Orbitofrontal Cortex and Amygdala , 2011, PloS one.

[65]  Nancy C. Andreasen,et al.  Problems with ratio and proportion measures of imaged cerebral structures , 1991, Psychiatry Research: Neuroimaging.

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

[67]  G. Rees,et al.  The structural basis of inter-individual differences in human behaviour and cognition , 2011, Nature Reviews Neuroscience.

[68]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[69]  David G. Amaral,et al.  The primate amygdala and the neurobiology of social behavior: implications for understanding social anxiety , 2002, Biological Psychiatry.

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