Neural responses to negative facial emotions: Sex differences in the correlates of individual anger and fear traits

Studies have examined sex differences in emotion processing in health and illness. However, it remains unclear how these neural processes may relate to individual differences in affective traits. We addressed this issue with a dataset of 970 subjects (508 women) curated from the Human Connectome Project. Participants were assessed with the NIH Toolbox Emotion Measures and fMRI while identifying negative facial emotion and neutral shape targets in alternating blocks. Imaging data were analyzed with published routines and the results were reported at a corrected threshold. Men scored similarly in Anger- but lower in Fear-Affect, as compared to women. Men as compared with women engaged the occipital-temporal visual cortex, retrosplenial cortex (RSC), and both anterior and posterior cingulate cortex to a greater extent during face versus shape identification. Women relative to men engaged higher activation of bilateral middle frontal cortex. In regional brain responses to face versus shape identification, men relative to women showed more significant modulations by both Anger- and Fear- Affect traits. The left RSC and right RSC/precuneus each demonstrated activities during face vs. shape identification in negative correlation with Anger- and Fear- Affect scores in men only. Anger affect was positively correlated with prolonged RT in identifying face vs. shape target in men but not women. In contrast, women relative to men showed higher Fear-Affect score and higher activation in the right middle frontal cortex, which was more strongly correlated with prolonged RT during face vs. shape identification. Together, men and women with higher Fear-Affect demonstrated lower accuracy in identifying negative facial emotion versus neutral shape target, a relationship mediated by activity of the RSC. These findings add to the literature of sex and trait individual differences in emotion processing and may help research of sex-shared and sex-specific behavioral and neural markers of emotional disorders.

[1]  G. Panayiotou,et al.  Psychophysiological and self-reported reactivity associated with social anxiety and public speaking fear symptoms: Effects of fear versus distress , 2017, Psychiatry Research.

[2]  John D E Gabrieli,et al.  Sex differences in the neural basis of emotional memories , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Bertram Walter,et al.  Hemodynamic brain correlates of disgust and fear ratings , 2007, NeuroImage.

[4]  D. Swick,et al.  Angry and Fearful Face Conflict Effects in Post-traumatic Stress Disorder , 2019, Front. Psychol..

[5]  Tatia M.C. Lee,et al.  Sex-related differences in neural activity during emotion regulation , 2009, Neuropsychologia.

[6]  M. Miller,et al.  Emotional Processing in PTSD: Heightened Negative Emotionality to Unpleasant Photographic Stimuli , 2009, The Journal of nervous and mental disease.

[7]  Sheng Zhang,et al.  Gender Differences in Cognitive Control: an Extended Investigation of the Stop Signal Task , 2009, Brain Imaging and Behavior.

[8]  M. Sams,et al.  Distributed affective space represents multiple emotion categories across the human brain , 2018, Social cognitive and affective neuroscience.

[9]  Mathieu Cassotti,et al.  Fear and anger have opposite effects on risk seeking in the gain frame , 2015, Front. Psychol..

[10]  Lisanne M. Jenkins,et al.  Considering sex differences clarifies the effects of depression on facial emotion processing during fMRI. , 2018, Journal of affective disorders.

[11]  Ralf Schulze,et al.  In Search of the Trauma Memory: A Meta-Analysis of Functional Neuroimaging Studies of Symptom Provocation in Posttraumatic Stress Disorder (PTSD) , 2013, PloS one.

[12]  M. Kret,et al.  A review on sex differences in processing emotional signals , 2012, Neuropsychologia.

[13]  G. E. Smith The Human Brain , 1924, Nature.

[14]  Jing Luo,et al.  Distinctive effects of fear and sadness induction on anger and aggressive behavior , 2015, Front. Psychol..

[15]  David I. Perrett,et al.  Sex differences in the perception of affective facial expressions: Do men really lack emotional sensitivity? , 2005, Cognitive Processing.

[16]  Travis P. Todd,et al.  Retrosplenial cortex and its role in cue-specific learning and memory , 2019, Neuroscience & Biobehavioral Reviews.

[17]  Lucy S. King,et al.  The association between early life stress and prefrontal cortex activation during implicit emotion regulation is moderated by sex in early adolescence , 2017, Development and Psychopathology.

[18]  Joseph H. Callicott,et al.  Sex differences in verbal working memory performance emerge at very high loads of common neuroimaging tasks , 2017, Brain and Cognition.

[19]  J. Pineda,et al.  Men and Women Exhibit a Differential Bias for Processing Movement versus Objects , 2012, PloS one.

[20]  D. H. Hay,et al.  Gender differences in anger and fear as a function of situational context , 1995 .

[21]  A. Szameitat,et al.  Sex Differences in Emotion Recognition and Working Memory Tasks , 2018, Front. Psychol..

[22]  L. Price,et al.  Sex differences in the use of coping strategies: predictors of anxiety and depressive symptoms , 2008, Depression and anxiety.

[23]  Gillian Tindall,et al.  Men and Women , 1968, Mental Health.

[24]  Brent L. Hughes,et al.  Prefrontal-Subcortical Pathways Mediating Successful Emotion Regulation , 2008, Neuron.

[25]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[26]  P. Albert,et al.  Why is depression more prevalent in women? , 2015, Journal of psychiatry & neuroscience : JPN.

[27]  Ruben C Gur,et al.  Sex differences in cognitive regulation of psychosocial achievement stress: Brain and behavior , 2015, Human brain mapping.

[28]  G. Goelman,et al.  Sex differences during emotion processing are dependent on the menstrual cycle phase , 2019, Psychoneuroendocrinology.

[29]  Sheng Zhang,et al.  Cerebral correlates of skin conductance responses in a cognitive task , 2012, NeuroImage.

[30]  Chen-Ying Huang,et al.  Gender differences in punishment and reward sensitivity in a sample of Taiwanese college students , 2007 .

[31]  Jing Luo,et al.  The Neural Basis of Fear Promotes Anger and Sadness Counteracts Anger , 2018, Neural plasticity.

[32]  S. Herpertz,et al.  Whole-brain functional connectivity during script-driven aggression in borderline personality disorder , 2019, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[33]  Jungmeen Kim-Spoon,et al.  Attention regulates anger and fear to predict changes in adolescent risk-taking behaviors. , 2015, Journal of child psychology and psychiatry, and allied disciplines.

[34]  N. Fox,et al.  Cognition assessment using the NIH Toolbox , 2013, Neurology.

[35]  R. Valentino,et al.  Sex differences in stress-related psychiatric disorders: Neurobiological perspectives , 2014, Frontiers in Neuroendocrinology.

[36]  R. Coppola,et al.  Functional Magnetic Resonance Imaging Brain Mapping in Psychiatry: Methodological Issues Illustrated in a Study of Working Memory in Schizophrenia , 1998, Neuropsychopharmacology.

[37]  J. Lerner,et al.  Fear, anger, and risk. , 2001, Journal of personality and social psychology.

[38]  Susan M Resnick,et al.  Sex differences in cognitive trajectories in clinically normal older adults. , 2016, Psychology and aging.

[39]  Valerie L. Kinner,et al.  Emotion regulation: exploring the impact of stress and sex , 2014, Front. Behav. Neurosci..

[40]  Thang M. Le,et al.  Alcohol Expectancy and Cerebral Responses to Cue-Elicited Craving in Adult Nondependent Drinkers. , 2019, Biological psychiatry. Cognitive neuroscience and neuroimaging.

[41]  Sophia Frangou,et al.  The effects of gender and COMT Val158Met polymorphism on fearful facial affect recognition: a fMRI study. , 2009, The international journal of neuropsychopharmacology.

[42]  B. Vogt The cingulate cortex in neurologic diseases: History, Structure, Overview. , 2019, Handbook of clinical neurology.

[43]  C. Neuper,et al.  Cognitively preserved MS patients demonstrate functional differences in processing neutral and emotional faces , 2011, Brain Imaging and Behavior.

[44]  Katja Hagen,et al.  Aging-related cortical reorganization of verbal fluency processing: a functional near-infrared spectroscopy study , 2013, Neurobiology of Aging.

[45]  Mark E Bastin,et al.  Sex Differences in the Adult Human Brain: Evidence from 5216 UK Biobank Participants , 2017, bioRxiv.

[46]  D. Halpern,et al.  The new science of cognitive sex differences , 2014, Trends in Cognitive Sciences.

[47]  S. Vandenberg,et al.  Mental Rotations, a Group Test of Three-Dimensional Spatial Visualization , 1978, Perceptual and motor skills.

[48]  C. Ávila,et al.  The Sensitivity to Punishment and Sensitivity to Reward Questionnaire (SPSRQ) as a measure of Gray's anxiety and impulsivity dimensions. , 2001 .

[49]  G. Frisoni,et al.  Abnormalities in functional connectivity in borderline personality disorder: Correlations with metacognition and emotion dysregulation , 2019, Psychiatry Research: Neuroimaging.

[50]  R. Seitz,et al.  Posterior and prefrontal contributions to the development posttraumatic stress disorder symptom severity: an fMRI study of symptom provocation in acute stress disorder , 2017, European Archives of Psychiatry and Clinical Neuroscience.

[51]  Renlai Zhou,et al.  Gender Differences in Emotional Response: Inconsistency between Experience and Expressivity , 2016, PloS one.

[52]  David Cella,et al.  Emotion assessment using the NIH Toolbox , 2013, Neurology.

[53]  Markus Heinrichs,et al.  The neural correlates of sex differences in emotional reactivity and emotion regulation , 2009, Human brain mapping.

[54]  Russell A. Poldrack,et al.  Guidelines for reporting an fMRI study , 2008, NeuroImage.

[55]  Emily W. Gower,et al.  Sex differences in cognition in healthy elderly individuals , 2012, Neuropsychology, development, and cognition. Section B, Aging, neuropsychology and cognition.

[56]  A. Yoshino,et al.  Relationships between temperament dimensions in personality and unconscious emotional responses , 2005, Biological Psychiatry.

[57]  A. Mühlberger,et al.  Men Scare Me More: Gender Differences in Social Fear Conditioning in Virtual Reality , 2019, Front. Psychol..

[58]  Xiaoqian J Chai,et al.  Sex differences in directional cue use in a virtual landscape. , 2009, Behavioral neuroscience.

[59]  R. Rogers,et al.  Gender differences in contributions of emotion to psychopathy and antisocial personality disorder. , 2008, Clinical Psychology Review.

[60]  Jack C. Rogers,et al.  Investigating Sex Differences in Emotion Recognition, Learning, and Regulation Among Youths With Conduct Disorder. , 2020, Journal of the American Academy of Child and Adolescent Psychiatry.

[61]  M. Yücel,et al.  Sex differences in the neural correlates of emotion: Evidence from neuroimaging , 2011, Biological Psychology.

[62]  Simon Zhornitsky,et al.  Cue-elicited craving, thalamic activity, and physiological arousal in adult non-dependent drinkers. , 2019, Journal of psychiatric research.

[63]  Thang M. Le,et al.  Reward sensitivity and electrodermal responses to actions and outcomes in a go/no-go task , 2019, PloS one.

[64]  G. J. Lewis,et al.  Sex Differences in Emotion Recognition: Evidence for a Small Overall Female Superiority on Facial Disgust , 2019, Emotion.

[65]  S. Sternberg High-Speed Scanning in Human Memory , 1966, Science.

[66]  Kenneth Hugdahl,et al.  Cognitive sex differences and hemispheric asymmetry: A critical review of 40 years of research , 2018, Laterality.

[67]  P. Vuilleumier,et al.  Distinct Brain Areas involved in Anger versus Punishment during Social Interactions , 2018, Scientific Reports.

[68]  D. Rubinow,et al.  Sex differences and the neurobiology of affective disorders , 2018, Neuropsychopharmacology.

[69]  Yue-jia Luo,et al.  Differentiating the influence of incidental anger and fear on risk decision-making , 2018, Physiology & Behavior.

[70]  Thang M. Le,et al.  Heart Rate Variability, Cue-Evoked Ventromedial Prefrontal Cortical Response, and Problem Alcohol Use in Adult Drinkers. , 2019, Biological psychiatry. Cognitive neuroscience and neuroimaging.

[71]  Rebecca Saxe,et al.  Attitudes towards the outgroup are predicted by activity in the precuneus in Arabs and Israelis , 2010, NeuroImage.

[72]  Thang M. Le,et al.  Posterior Cingulate Cortical Response to Active Avoidance Mediates the Relationship between Punishment Sensitivity and Problem Drinking , 2019, The Journal of Neuroscience.

[73]  Edward E. Smith,et al.  Temporal dynamics of brain activation during a working memory task , 1997, Nature.

[74]  Timo Mäntylä,et al.  Gender Differences in Multitasking Reflect Spatial Ability , 2013, Psychological science.

[75]  Zhenhong He,et al.  Gender Differences in Processing Fearful and Angry Body Expressions , 2018, Front. Behav. Neurosci..

[76]  B. Laeng,et al.  A Redrawn Vandenberg and Kuse Mental Rotations Test - Different Versions and Factors That Affect Performance , 1995, Brain and Cognition.

[77]  Natalia S. Lawrence,et al.  Sex Differences in Neural Responses to Disgusting Visual Stimuli: Implications for Disgust-Related Psychiatric Disorders , 2007, Biological Psychiatry.

[78]  J. Moyer,et al.  Modulation of intrinsic excitability as a function of learning within the fear conditioning circuit , 2019, Neurobiology of Learning and Memory.

[79]  Oliver T Wolf,et al.  Sex differences in stress effects on emotional learning , 2017, Journal of neuroscience research.

[80]  Matthew S. Fritz,et al.  Mediation analysis. , 2019, Annual review of psychology.

[81]  Rena Li,et al.  Sex differences in cognitive impairment and Alzheimer’s disease , 2014, Frontiers in Neuroendocrinology.

[82]  A S Gevins,et al.  Human neuroelectric patterns predict performance accuracy. , 1987, Science.

[83]  Christina M. Pawliczek,et al.  Sex differences in the neural correlates of aggression , 2018, Brain Structure and Function.

[84]  Reginald B. Adams,et al.  If it bleeds, it leads: separating threat from mere negativity. , 2015, Social cognitive and affective neuroscience.

[85]  A. Kring,et al.  Sex differences in emotion: expression, experience, and physiology. , 1998, Journal of personality and social psychology.

[86]  M. Manosevitz High-Speed Scanning in Human Memory , .

[87]  Mathieu Vandenbulcke,et al.  Affective scenes influence fear perception of individual body expressions , 2014, Human brain mapping.

[88]  R. M. Murray,et al.  Altered resting-state functional connectivity in emotion-processing brain regions in adults who were born very preterm , 2016, Psychological Medicine.

[89]  Abraham Z. Snyder,et al.  Function in the human connectome: Task-fMRI and individual differences in behavior , 2013, NeuroImage.

[90]  J. Neumann,et al.  Neural processing of negative emotional stimuli and the influence of age, sex and task-related characteristics , 2016, Neuroscience & Biobehavioral Reviews.

[91]  Zhuo Wang,et al.  Functional connectivity-based parcellation and connectome of cortical midline structures in the mouse: a perfusion autoradiography study , 2014, Front. Neuroinform..

[92]  E. Kreta,et al.  A review on sex differences in processing emotional signals , 2012 .