Gender differences in the cortical electrophysiological processing of visual emotional stimuli

The processing of visual emotional stimuli has been investigated previously; however, gender differences in the processing of emotional stimuli remain to be clarified. The aim of the current study was to use steady-state probe topography (SSPT) to examine steady-state visually evoked potentials (SSVEPs) during the processing of pleasant and unpleasant images relative to neutral images, and to determine whether this processing differs between males and females. Thirty participants (15 males and 15 females) viewed 75 images low on the arousal dimension (categorised as pleasant, neutral or unpleasant) selected from the International Affective Picture System (IAPS), whilst a 13-Hz sinusoidal white visual flicker was superimposed over the visual field and brain electrical activity was recorded from 64 electrode sites. Results suggest that pleasant and unpleasant images relative to neutral images are associated with reductions in frontal latency and occipital amplitude. In addition, electrophysiological gender differences were observed despite there being no differences found between males and females on subjective mood or behavioural ratings of presented images (valence and arousal dimensions). The main gender difference reported in the current study related to the processing of unpleasant images (relative to neutral images) which is associated with widespread frontal latency reductions (predominantly right sided) in females but not in males. Our results suggest that gender differences do exist in the processing of visual emotional stimuli, and illustrate the importance of taking these differences into account during investigations of emotional processing. Finally, these gender differences may have implications for the pathophysiology of mood disorders such as depression.

[1]  Joseph Ciorciari,et al.  Steady-State Visually Evoked Potential topography associated with a visual vigilance task , 2005, Brain Topography.

[2]  E. Gordon,et al.  Arousal Dissociates Amygdala and Hippocampal Fear Responses: Evidence from Simultaneous fMRI and Skin Conductance Recording , 2001, NeuroImage.

[3]  M. Bradley,et al.  Affective picture processing: the late positive potential is modulated by motivational relevance. , 2000, Psychophysiology.

[4]  R. Kötter,et al.  Functional dissociation between medial and lateral prefrontal cortical spatiotemporal activation in negative and positive emotions: a combined fMRI/MEG study. , 2000, Cerebral cortex.

[5]  R. Dolan,et al.  The interaction between mood and cognitive function studied with PET , 1997, Psychological Medicine.

[6]  Julian Meltzoff,et al.  Research in Psychotherapy , 1970 .

[7]  Richard J. Davidson,et al.  Parsing the subcomponents of emotion and disorders of emotion: Perspectives from affective neuroscience. , 2003 .

[8]  F. L. D. Silva,et al.  Event-related EEG/MEG synchronization and desynchronization: basic principles , 1999, Clinical Neurophysiology.

[9]  Chetwyn C. H. Chan,et al.  Gender differences in neural correlates of recognition of happy and sad faces in humans assessed by functional magnetic resonance imaging , 2002, Neuroscience Letters.

[10]  Eric Vermetten,et al.  Regional brain metabolic correlates of alpha-methylparatyrosine-induced depressive symptoms: implications for the neural circuitry of depression. , 2003, JAMA.

[11]  R. Post,et al.  Gender differences in regional cerebral blood flow during transient self-induced sadness or happiness , 1996, Biological Psychiatry.

[12]  J. Mcglone.  The Neuropsychology of Sex Differences in Human Brain Organization , 1986 .

[13]  The functional neuroanatomy of emotional disorders , 2001 .

[14]  R. Davidson,et al.  The functional neuroanatomy of emotion and affective style , 1999, Trends in Cognitive Sciences.

[15]  L. Abramson,et al.  Development of gender differences in depression: an elaborated cognitive vulnerability-transactional stress theory. , 2001, Psychological bulletin.

[16]  M. Bradley,et al.  Emotion and motivation II: sex differences in picture processing. , 2001, Emotion.

[17]  E. Stein,et al.  Right hemispheric dominance of inhibitory control: an event-related functional MRI study. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Jerre Levy,et al.  Perceptual asymmetry for chimeric faces across the life span , 1986, Brain and Cognition.

[19]  L. F. Barrett,et al.  Handbook of Emotions , 1993 .

[20]  W. Heller.  Neuropsychological mechanisms of individual differences in emotion, personality, and arousal. , 1993 .

[21]  R. Davidson.  Anxiety and affective style: role of prefrontal cortex and amygdala , 2002, Biological Psychiatry.

[22]  G. D. de Courten-Myers,et al.  Gender Differences in the Human Cerebral Cortex: More Neurons in Males; More Processes in Females , 1999, Journal of child neurology.

[23]  P. Lang.  Cognition in emotion: Concept and action. , 1985 .

[24]  A. H Kemp,et al.  Cortical neurophysiology of anticipatory anxiety: an investigation utilizing steady state probe topography (SSPT) , 2003, NeuroImage.

[25]  Charles D. Smith,et al.  Neural substrates of facial emotion processing using fMRI. , 2001, Brain research. Cognitive brain research.

[26]  M. Bradley,et al.  Fleeting images: a new look at early emotion discrimination. , 2001, Psychophysiology.

[27]  R. Davidson.  Emotion and Affective Style: Hemispheric Substrates , 1992 .

[28]  M Diksic,et al.  Differences between males and females in rates of serotonin synthesis in human brain. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[29]  Hans-Jochen Heinze,et al.  GABA-ergic Modulation of Prefrontal Spatio-temporal Activation Pattern during Emotional Processing: A Combined fMRI/MEG Study with Placebo and Lorazepam , 2002, Journal of Cognitive Neuroscience.

[30]  M. Bradley,et al.  Neuroanatomical correlates of pleasant and unpleasant emotion , 1997, Neuropsychologia.

[31]  Barry D. Smith,et al.  Hemispheric asymmetry and emotion: Effects of nonverbal affective stimuli , 1986, Biological Psychology.

[32]  M. Mesulam,et al.  Dominant language functions of the right hemisphere? Prosody and emotional gesturing. , 1979, Archives of neurology.

[33]  H. Sackeim,et al.  Emotions are expressed more intensely on the left side of the face. , 1978, Science.

[34]  森田 恵史.  Effects of facial affect recognition on the auditory P300 in healthy subjects , 2002 .

[35]  R. Silberstein,et al.  Steady-state visually evoked potential topography during the continuous performance task in normal controls and schizophrenia , 2000, Clinical Neurophysiology.

[36]  R. B. Silberstein,et al.  Steady-State Visually Evoked Potential Topography during Processing of Emotional Valence in Healthy Subjects , 2002, NeuroImage.

[37]  J. Desmond,et al.  Hemispheric asymmetry for emotional stimuli detected with fMRI , 1998, Neuroreport.

[38]  W. Ray,et al.  EEG alpha activity reflects attentional demands, and beta activity reflects emotional and cognitive processes. , 1985, Science.

[39]  M. Fava,et al.  Predictors of Mood Response to Acute Tryptophan Depletion: A Reanalysis , 2002, Neuropsychopharmacology.

[40]  S. Taylor,et al.  The Effect of Emotional Content on Visual Recognition Memory: A PET Activation Study , 1998, NeuroImage.

[41]  P. Ekman.  Expression and the Nature of Emotion , 1984 .

[42]  H L Miller,et al.  Positron emission tomography measurement of cerebral metabolic correlates of tryptophan depletion-induced depressive relapse. , 1997, Archives of general psychiatry.

[43]  C D Tesche,et al.  Characterizing the local oscillatory content of spontaneous cortical activity during mental imagery. , 1995, Brain research. Cognitive brain research.

[44]  Hanna Damasio,et al.  Single-neuron responses to emotional visual stimuli recorded in human ventral prefrontal cortex , 2001, Nature Neuroscience.

[45]  John J. Foxe,et al.  The Spatiotemporal Dynamics of Illusory Contour Processing: Combined High-Density Electrical Mapping, Source Analysis, and Functional Magnetic Resonance Imaging , 2002, The Journal of Neuroscience.

[46]  S. M. Breedlove,et al.  Sexual Differentiation of the Vertebrate Brain: Principles and Mechanisms , 1998, Frontiers in Neuroendocrinology.

[47]  P. Lang,et al.  International Affective Picture System (IAPS): Instruction Manual and Affective Ratings (Tech. Rep. No. A-4) , 1999 .

[48]  G. Goldstein,et al.  Advances in Clinical Neuropsychology , 1986, Advances in Clinical Neuropsychology.

[49]  M. Erb,et al.  Dynamic Brain Activation during Processing of Emotional Intonation: Influence of Acoustic Parameters, Emotional Valence, and Sex , 2002, NeuroImage.

[50]  A. Angrilli,et al.  Emotional Information Processing and Visual Evoked Brain Potentials , 1996, Perceptual and motor skills.

[51]  P. Cowen,et al.  Effect of Tryptophan Depletion on Mood in Male and Female Volunteers: A Pilot Study , 1997 .

[52]  A. Kemp,et al.  Acute augmentation of serotonin suppresses cardiovascular responses to emotional valence. , 2004, The international journal of neuropsychopharmacology.

[53]  A. Angrilli,et al.  Visual evoked potentials, heart rate responses and memory to emotional pictorial stimuli. , 1997, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[54]  M. Raichle,et al.  Neural correlates of self-induced dysphoria. , 1993, The American journal of psychiatry.

[55]  M. Bradley,et al.  Emotional arousal and activation of the visual cortex: an fMRI analysis. , 1998, Psychophysiology.

[56]  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.

[57]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[58]  S. G. Cox,et al.  Functional MRI study of the cognitive generation of affect. , 1999, The American journal of psychiatry.

[59]  B. Horwitz,et al.  Brain activity during transient sadness and happiness in healthy women. , 1995, The American journal of psychiatry.

[60]  R. Hu.  Diagnostic and Statistical Manual of Mental Disorders (DSM-IV) , 2003 .

[61]  S. Nolen-Hoeksema.  Responses to depression and their effects on the duration of depressive episodes. , 1991, Journal of abnormal psychology.

[62]  L. Aftanas,et al.  Time-dependent cortical asymmetries induced by emotional arousal: EEG analysis of event-related synchronization and desynchronization in individually defined frequency bands. , 2002, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[63]  D. Lindsley,et al.  Chapter 1 – The Electroencephalogram: Autonomous Electrical Activity in Man and Animals , 1974 .

[64]  M. Lorr,et al.  Manual for the Profile of Mood States , 1971 .

[65]  J. Russell,et al.  Science Current Directions in Psychological the Structure of Current Affect : Controversies and Emerging Consensus on Behalf Of: Association for Psychological Science , 2022 .

[66]  Peggy Dean,et al.  Mood Response to Acute Tryptophan Depletion in Healthy Volunteers: Sex Differences and Temporal Stability , 1996, Neuropsychopharmacology.

[67]  R. Davidson.  Affective Style and Affective Disorders: Perspectives from Affective Neuroscience , 1998 .

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

[69]  D. Guthrie,et al.  Significance testing of difference potentials. , 1991, Psychophysiology.

[70]  S. Paradiso,et al.  Cerebral blood flow changes associated with attribution of emotional valence to pleasant, unpleasant, and neutral visual stimuli in a PET study of normal subjects. , 1999, The American journal of psychiatry.

[71]  Judith A. Hall,et al.  Gender and emotion , 2008 .

[72]  P. Ekman,et al.  Approaches To Emotion , 1985 .

[73]  Harald T. Schupp,et al.  Emotional Facilitation of Sensory Processing in the Visual Cortex , 2003, Psychological science.

[74]  G. Fink,et al.  Neural activation during selective attention to subjective emotional responses , 1997, Neuroreport.

[75]  R. Silberstein,et al.  Steady-state visually evoked potential topography during the Wisconsin card sorting test. , 1995, Electroencephalography and clinical neurophysiology.

[76]  L. Aftanas,et al.  Affective picture processing: event-related synchronization within individually defined human theta band is modulated by valence dimension. , 2001, Neuroscience Letters.

[77]  Ronald C Kessler,et al.  Epidemiology of women and depression. , 2003, Journal of affective disorders.

[78]  Kewei Chen,et al.  Sex differences in the human brain's response to hunger and satiation. , 2002, The American journal of clinical nutrition.

[79]  P. Fox,et al.  Differential limbic–cortical correlates of sadness and anxiety in healthy subjects: implications for affective disorders , 2000, Biological Psychiatry.

[80]  H. Flor,et al.  Gender differences in the processing of standardized emotional visual stimuli in humans: a functional magnetic resonance imaging study , 2003, Neuroscience Letters.

[81]  Leslie R. Brody.  Gender, Emotion, and the Family , 1999 .

[82]  A. Alavi,et al.  Sex differences in regional cerebral glucose metabolism during a resting state , 1995, Science.

[83]  J. Iaccino,et al.  Left Brain - Right Brain Differences: Inquiries, Evidence, and New Approaches , 1993 .

[84]  William D S Killgore,et al.  Sex differences in amygdala activation during the perception of facial affect , 2001, Neuroreport.

[85]  Wendy Heller,et al.  The Neuropsychology of Emotion: Developmental Patterns and Implications for Psychopathology , 1990 .

[86]  W. Heller,et al.  Gender Differences in Human Neuropsychological Function , 1992 .

[87]  K. Scherer,et al.  Handbook of affective sciences. , 2003 .

[88]  Jordan Grafman,et al.  Handbook of Neuropsychology , 1991 .

[89]  P. Nunez,et al.  A theoretical and experimental study of high resolution EEG based on surface Laplacians and cortical imaging. , 1994, Electroencephalography and clinical neurophysiology.

[90]  Joan C. Borod,et al.  Cerebral mechanisms underlying facial, prosodic, and lexical emotional expression: A review of neuropsychological studies and methodological issues. , 1993 .

[91]  Peter J. Lang,et al.  Fear reduction and fear behavior: Problems in treating a construct. , 1968 .

[92]  U. Habel,et al.  Gender differences in regional cerebral activity during sadness , 2000, Human brain mapping.

[93]  Barry D. Smith,et al.  The lateralized processing of affect in emotionally labile extraverts and introverts: central and autonomic effects , 1995, Biological Psychology.

[94]  Nancy L. Stein,et al.  Psychological and Biological Approaches To Emotion , 1990 .

[95]  F C Jarman,et al.  Functional brain electrical activity mapping in boys with attention-deficit/hyperactivity disorder. , 1998, Archives of general psychiatry.

[96]  P. Gartside,et al.  Structure of the Cerebral Cortex in Men and Women , 2002, Journal of neuropathology and experimental neurology.

[97]  L. Aftanas,et al.  Event-Related Synchronization and Desynchronization During Affective Processing: Emergence of Valence-Related Time-Dependent Hemispheric Asymmetries in Theta and Upper Alpha Band , 2001, The International journal of neuroscience.