Boys do it the right way: Sex-dependent amygdala lateralization during face processing in adolescents

Previous studies have observed a sex-dependent lateralization of amygdala activation related to emotional memory. Specifically, it was shown that the activity of the right amygdala correlates significantly stronger with memory for images judged as arousing in men than in women, and that there is a significantly stronger relationship in women than in men between activity of the left amygdala and memory for arousing images. Using a large sample of 235 male adolescents and 235 females matched for age and handedness, we investigated the sex-specific lateralization of amygdala activation during an emotional face perception fMRI task. Performing a formal sex by hemisphere analysis, we observed in males a significantly stronger right amygdala activation as compared to females. Our results indicate that adolescents display a sex-dependent lateralization of amygdala activation that is also present in basic processes of emotional perception. This finding suggests a sex-dependent development of human emotion processing and may further implicate possible etiological pathways for mental disorders most frequent in adolescent males (i.e., conduct disorder).

[1]  J. Kim,et al.  Amygdalar lateralization in fear conditioning: evidence for greater involvement of the right amygdala. , 2004, Behavioral neuroscience.

[2]  P. McGuire,et al.  Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. , 2009, Journal of psychiatry & neuroscience : JPN.

[3]  Philipp Sterzer,et al.  Abnormal neural responses to emotional visual stimuli in adolescents with conduct disorder , 2005, Biological Psychiatry.

[4]  Michael Angstadt,et al.  Beyond threat: Amygdala reactivity across multiple expressions of facial affect , 2006, NeuroImage.

[5]  T. Allison,et al.  Social perception from visual cues: role of the STS region , 2000, Trends in Cognitive Sciences.

[6]  Michael G. Hardin,et al.  Triadic model of the neurobiology of motivated behavior in adolescence , 2005, Psychological Medicine.

[7]  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.

[8]  John A Updegraff,et al.  Biobehavioral responses to stress in females: tend-and-befriend, not fight-or-flight. , 2000, Psychological review.

[9]  Alessandra M Passarotti,et al.  Neural correlates of incidental and directed facial emotion processing in adolescents and adults. , 2009, Social cognitive and affective neuroscience.

[10]  T. Paus,et al.  Brain networks involved in viewing angry hands or faces. , 2006, Cerebral cortex.

[11]  Larry Cahill,et al.  Sex-related hemispheric lateralization of electrical potentials evoked by arousing negative stimuli , 2007, Brain Research.

[12]  Hans Steiner,et al.  Prevalence of and gender differences in psychiatric disorders among juvenile delinquents incarcerated for nine months. , 2009, Psychiatric services.

[13]  G. J. Vries,et al.  Minireview: Sex differences in adult and developing brains: compensation, compensation, compensation. , 2004 .

[14]  R. Kahn,et al.  Lateralization of amygdala activation: a systematic review of functional neuroimaging studies , 2004, Brain Research Reviews.

[15]  R. Davidson Anterior cerebral asymmetry and the nature of emotion , 1992, Brain and Cognition.

[16]  S. Stokes,et al.  Factors that influence vocabulary development in two-year-old children. , 2009, Journal of child psychology and psychiatry, and allied disciplines.

[17]  J. Armony,et al.  Own-sex effects in emotional memory for faces , 2007, Neuroscience Letters.

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

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

[20]  Timo D. Vloet,et al.  Entwicklungsfaktoren dissozialer Störungen – die Bedeutung des autonomen Stresssystems , 2010 .

[21]  J. Haxby,et al.  fMRI Responses to Video and Point-Light Displays of Moving Humans and Manipulable Objects , 2003, Journal of Cognitive Neuroscience.

[22]  James L McGaugh,et al.  Memory enhancement induced by post-training intrabasolateral amygdala infusions of beta-adrenergic or muscarinic agonists requires activation of dopamine receptors: Involvement of right, but not left, basolateral amygdala. , 2005, Learning & memory.

[23]  Gereon R Fink,et al.  Emotional processing in male adolescents with childhood-onset conduct disorder. , 2008, Journal of child psychology and psychiatry, and allied disciplines.

[24]  R. Sullivan,et al.  Lateralized sex differences in stress-induced dopamine release in the rat , 2009, Neuroreport.

[25]  Wim van den Brink,et al.  Psychiatric Disorders in Detained Male Adolescents: A Systematic Literature Review , 2010, Canadian journal of psychiatry. Revue canadienne de psychiatrie.

[26]  Alice Mado Proverbio,et al.  Sex differences in the brain response to affective scenes with or without humans , 2009, Neuropsychologia.

[27]  R. E. Gur,et al.  Effects of Emotional Discrimination Tasks on Cerebral Blood Flow: Regional Activation and Its Relation to Performance , 1994, Brain and Cognition.

[28]  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.

[29]  Donna M. Palmer,et al.  Explicit identification and implicit recognition of facial emotions: I. Age effects in males and females across 10 decades , 2009, Journal of clinical and experimental neuropsychology.

[30]  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.

[31]  James L. McGaugh,et al.  Enhancement of extinction memory consolidation: The role of the noradrenergic and GABAergic systems within the basolateral amygdala , 2006, Neurobiology of Learning and Memory.

[32]  R. Blair,et al.  The development of antisocial behavior: What can we learn from functional neuroimaging studies? , 2008, Development and Psychopathology.

[33]  Margot J. Taylor,et al.  The development of emotional face processing during childhood. , 2006, Developmental science.

[34]  M. Keshavan,et al.  Sex differences in brain maturation during childhood and adolescence. , 2001, Cerebral cortex.

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

[36]  Ivanka Savic,et al.  PET and MRI show differences in cerebral asymmetry and functional connectivity between homo- and heterosexual subjects , 2008, Proceedings of the National Academy of Sciences.

[37]  Daniella J. Furman,et al.  Menstrual cycle phase modulates reward-related neural function in women , 2007, Proceedings of the National Academy of Sciences.

[38]  R. Adolphs,et al.  Annals of the New York Academy of Sciences What Does the Amygdala Contribute to Social Cognition? , 2022 .

[39]  D. Thomson,et al.  Development of face recognition. , 1995, British journal of psychology.

[40]  Ellen Leibenluft,et al.  A Developmental Examination of Amygdala Response to Facial Expressions , 2008, Journal of Cognitive Neuroscience.

[41]  Matthew K Nock,et al.  Prevalence, subtypes, and correlates of DSM-IV conduct disorder in the National Comorbidity Survey Replication , 2006, Psychological Medicine.

[42]  C Baldock,et al.  Test liquids for quantitative MRI measurements of self‐diffusion coefficient in vivo , 2000, Magnetic resonance in medicine.

[43]  F. Pacitti,et al.  Sex-related lateralized effect of emotional content on declarative memory: An event related potential study , 2006, Behavioural Brain Research.

[44]  E. Gordon,et al.  BOLD, sweat and fears: fMRI and skin conductance distinguish facial fear signals , 2005, Neuroreport.

[45]  Monique Ernst,et al.  A developmental examination of gender differences in brain engagement during evaluation of threat , 2004, Biological Psychiatry.

[46]  Turhan Canli,et al.  Individual differences in emotion processing , 2004, Current Opinion in Neurobiology.

[47]  Issidoros C. Sarinopoulos,et al.  The effect of anticipation and the specificity of sex differences for amygdala and hippocampus function in emotional memory , 2006, Proceedings of the National Academy of Sciences.

[48]  Ellen Leibenluft,et al.  Adolescent immaturity in attention-related brain engagement to emotional facial expressions , 2003, NeuroImage.

[49]  Richard Rowe,et al.  Conduct disorder and oppositional defiant disorder in a national sample: developmental epidemiology. , 2004, Journal of child psychology and psychiatry, and allied disciplines.

[50]  K. Luan Phan,et al.  Valence, gender, and lateralization of functional brain anatomy in emotion: a meta-analysis of findings from neuroimaging , 2003, NeuroImage.

[51]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[52]  William D S Killgore,et al.  Sex-specific developmental changes in amygdala responses to affective faces , 2001, Neuroreport.

[53]  R. Adamec,et al.  Evidence that long-lasting potentiation of amygdala efferents in the right hemisphere underlies pharmacological stressor (FG-7142) induced lasting increases in anxiety-like behaviour: role of GABA tone in initiation of brain and behavioural changes , 2000, Journal of psychopharmacology.

[54]  D. Pine,et al.  Emotional Reactivity and Risk for Psychopathology Among Adolescents , 2001, CNS Spectrums.

[55]  Benjamin B. Lahey,et al.  Atypical empathic responses in adolescents with aggressive conduct disorder: A functional MRI investigation , 2009, Biological Psychology.

[56]  David H. Zald,et al.  Sex-related differences in amygdala functional connectivity during resting conditions , 2006, NeuroImage.

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

[58]  Jessica Turner,et al.  Sex-related hemispheric lateralization of amygdala function in emotionally influenced memory: an FMRI investigation. , 2004, Learning & memory.

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

[60]  G. Glover,et al.  Biological Substrates of Emotional Reactivity and Regulation in Adolescence During an Emotional Go-Nogo Task , 2008, Biological Psychiatry.

[61]  Susan D. Voyer,et al.  Magnitude of sex differences in spatial abilities: a meta-analysis and consideration of critical variables. , 1995, Psychological bulletin.

[62]  A. Addington,et al.  Longitudinally mapping the influence of sex and androgen signaling on the dynamics of human cortical maturation in adolescence , 2010, Proceedings of the National Academy of Sciences.

[63]  Steven G. Potkin,et al.  Sex-Related Difference in Amygdala Activity during Emotionally Influenced Memory Storage , 2001, Neurobiology of Learning and Memory.