Development during Adolescence of the Neural Processing of Social Emotion

In this fMRI study, we investigated the development between adolescence and adulthood of the neural processing of social emotions. Unlike basic emotions (such as disgust and fear), social emotions (such as guilt and embarrassment) require the representation of another's mental states. Nineteen adolescents (10–18 years) and 10 adults (22–32 years) were scanned while thinking about scenarios featuring either social or basic emotions. In both age groups, the anterior rostral medial prefrontal cortex (MPFC) was activated during social versus basic emotion. However, adolescents activated a lateral part of the MPFC for social versus basic emotions, whereas adults did not. Relative to adolescents, adults showed higher activity in the left temporal pole for social versus basic emotions. These results show that, although the MPFC is activated during social emotion in both adults and adolescents, adolescents recruit anterior (MPFC) regions more than do adults, and adults recruit posterior (temporal) regions more than do adolescents.

[1]  Bregtje Gunther Moor,et al.  Please Scroll down for Article Social Neuroscience Do You like Me? Neural Correlates of Social Evaluation and Developmental Trajectories Do You like Me? Neural Correlates of Social Evaluation and Developmental Trajectories Neural Correlates of Peer Evaluation , 2022 .

[2]  R. Saxe,et al.  Making sense of another mind: The role of the right temporo-parietal junction , 2005, Neuropsychologia.

[3]  S. Blakemore.  The social brain in adolescence , 2008, Nature Reviews Neuroscience.

[4]  Essi Viding,et al.  Feeling, caring, knowing: different types of empathy deficit in boys with psychopathic tendencies and autism spectrum disorder , 2010, Journal of child psychology and psychiatry, and allied disciplines.

[5]  D. Yurgelun-Todd,et al.  Fear-related activity in the prefrontal cortex increases with age during adolescence: A preliminary fMRI study , 2006, Neuroscience Letters.

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

[7]  Jordan Grafman,et al.  Social concepts are represented in the superior anterior temporal cortex , 2007, Proceedings of the National Academy of Sciences.

[8]  Iroise Dumontheil,et al.  Taking perspective into account in a communicative task , 2010, NeuroImage.

[10]  Mark Meerum Terwogt,et al.  Children's Knowledge of the Situations that Provoke Emotion , 1987 .

[11]  C. Frith.  The social brain? , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[12]  Sarah-Jayne Blakemore,et al.  Functional connectivity during a social emotion task in adolescents and in adults , 2009, The European journal of neuroscience.

[13]  N. Eisenberg.  Emotion, regulation, and moral development. , 2000, Annual review of psychology.

[14]  A. Toga,et al.  Localizing Age-Related Changes in Brain Structure between Childhood and Adolescence Using Statistical Parametric Mapping , 1999, NeuroImage.

[15]  Deborah A. Yurgelun-Todd,et al.  Sex-Related Developmental Differences in the Lateralized Activation of the Prefrontal Cortex and Amygdala during Perception of Facial Affect , 2004, Perceptual and motor skills.

[16]  Claude Nahmias,et al.  Sex differences in functional activation patterns revealed by increased emotion processing demands , 2004, Neuroreport.

[17]  Michael D. Berzonsky,et al.  Blackwell handbook of adolescence , 2005 .

[18]  Dana Samson,et al.  Left temporoparietal junction is necessary for representing someone else's belief , 2004, Nature Neuroscience.

[19]  D. Elkind.  Egocentrism in adolescence. , 1967, Child development.

[20]  Deborah A Yurgelun-Todd,et al.  Sex Differences in Cerebral Tissue Volume and Cognitive Performance during Adolescence , 2002, Psychological reports.

[21]  J. Decety,et al.  How Would You Feel versus How Do You Think She Would Feel? A Neuroimaging Study of Perspective-Taking with Social Emotions , 2004, Journal of Cognitive Neuroscience.

[22]  K. Ochsner,et al.  The role of social cognition in emotion , 2008, Trends in Cognitive Sciences.

[23]  M. Rosenberg,et al.  Disturbance in the self-image at adolescence. , 1973, American sociological review.

[24]  Alan C. Evans,et al.  Structural maturation of neural pathways in children and adolescents: in vivo study. , 1999, Science.

[25]  Sarah Durston,et al.  A shift from diffuse to focal cortical activity with development. , 2006, Developmental science.

[26]  C. Frith,et al.  Development and neurophysiology of mentalizing. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[27]  T. Ohnishi,et al.  Changes of brain activity in the neural substrates for theory of mind during childhood and adolescence , 2007, Psychiatry and clinical neurosciences.

[28]  Stephen Lawrie,et al.  Functional Specialization within Rostral Prefrontal Cortex (Area 10): A Meta-analysis , 2006, Journal of Cognitive Neuroscience.

[29]  David Elkind,et al.  Imaginary Audience Behavior in Children and Adolescents. , 1979 .

[30]  Tetsuya Matsuda,et al.  Brain activation associated with evaluative processes of guilt and embarrassment: an fMRI study , 2004, NeuroImage.

[31]  Paul M. Thompson,et al.  Sexual dimorphism of brain developmental trajectories during childhood and adolescence , 2007, NeuroImage.

[32]  N. Alpert,et al.  Activation of anterior paralimbic structures during guilt-related script-driven imagery , 2000, Biological Psychiatry.

[33]  Ivanei E. Bramati,et al.  The Moral Affiliations of Disgust: A Functional MRI Study , 2005, Cognitive and behavioral neurology : official journal of the Society for Behavioral and Cognitive Neurology.

[34]  Thomas F. Nugent,et al.  Dynamic mapping of human cortical development during childhood through early adulthood. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Xiaoqi Li,et al.  The relation of cognitive control to social outcome after paediatric TBI: Implications for intervention , 2009, Developmental Neurorehabilitation.

[36]  Vincent J Schmithorst,et al.  Developmental differences in white matter architecture between boys and girls , 2008, Human brain mapping.

[37]  R. Dolan,et al.  An fMRI study of intentional and unintentional (embarrassing) violations of social norms. , 2002, Brain : a journal of neurology.

[38]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[39]  J. Grafman,et al.  The neural basis of human moral cognition , 2005, Nature Reviews Neuroscience.

[40]  P. Costa,et al.  NEO inventories for the NEO Personality Inventory-3 (NEO-PI-3), NEO Five-Factor Inventory-3 (NEO-FFI-3), NEO Personality Inventory-Revised (NEO PI-R) : professional manual , 2010 .

[41]  Beate Sodian,et al.  Modulation of the cortical false belief network during development , 2010, Brain Research.

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

[43]  C. Frith,et al.  Adolescent development of the neural circuitry for thinking about intentions , 2007, Social cognitive and affective neuroscience.

[44]  U. Frith,et al.  The impact of extensive medial frontal lobe damage on 'Theory of Mind' and cognition. , 2004, Brain : a journal of neurology.

[45]  J. Zeman,et al.  Social-contextual influences on expectancies for managing anger and sadness: the transition from middle childhood to adolescence. , 1997, Developmental psychology.

[46]  M. Raichle,et al.  Searching for a baseline: Functional imaging and the resting human brain , 2001, Nature Reviews Neuroscience.

[47]  Sarah-Jayne Blakemore,et al.  Pubertal development of the understanding of social emotions: Implications for education , 2011, Learning and Individual Differences.

[48]  K. Konrad,et al.  Development of neural correlates of empathy from childhood to early adulthood: an fMRI study in boys and adult men , 2010, Journal of Neural Transmission.

[49]  Alan C. Evans,et al.  Brain development during childhood and adolescence: a longitudinal MRI study , 1999, Nature Neuroscience.

[50]  Ivanei E. Bramati,et al.  The Neural Correlates of Moral Sensitivity: A Functional Magnetic Resonance Imaging Investigation of Basic and Moral Emotions , 2002, The Journal of Neuroscience.

[51]  Philip J. Barnard,et al.  Emotional Complexity and the Neural Representation of Emotion in Motion , 2010, Social cognitive and affective neuroscience.

[52]  J. Haidt.  The emotional dog and its rational tail: a social intuitionist approach to moral judgment. , 2001, Psychological review.

[53]  L. Brody,et al.  Gender differences in emotional development: A review of theories and research , 1985 .

[54]  C. Frith,et al.  Meeting of minds: the medial frontal cortex and social cognition , 2006, Nature Reviews Neuroscience.

[55]  B. Levin,et al.  Developmental gene×environment interactions affecting systems regulating energy homeostasis and obesity , 2010, Frontiers in Neuroendocrinology.

[56]  Josef Perner,et al.  Do visual perspective tasks need theory of mind? , 2006, NeuroImage.

[57]  Sarah-Jayne Blakemore,et al.  Social brain development and the affective consequences of ostracism in adolescence , 2010, Brain and Cognition.

[58]  J. Zeman,et al.  Emotion Regulation in Children and Adolescents , 2006, Journal of developmental and behavioral pediatrics : JDBP.

[59]  Susan A. Sadek,et al.  Atypical neural self-representation in autism. , 2010, Brain : a journal of neurology.

[60]  R Saxe,et al.  People thinking about thinking people The role of the temporo-parietal junction in “theory of mind” , 2003, NeuroImage.

[61]  Sarah-Jayne Blakemore,et al.  The Developing Social Brain: Implications for Education , 2010, Neuron.

[62]  Paul Bloom,et al.  The intelligence of the moral intuitions: comment on Haidt (2001). , 2003, Psychological review.

[63]  Mirella Dapretto,et al.  Developmental changes in the neural basis of interpreting communicative intent. , 2006, Social cognitive and affective neuroscience.

[64]  Nicholas B. Allen,et al.  The emergence of depression in adolescence: Development of the prefrontal cortex and the representation of reward , 2008, Neuroscience & Biobehavioral Reviews.

[65]  Matthew D. Lieberman,et al.  I Know You Are But What Am I?!: Neural Bases of Self- and Social Knowledge Retrieval in Children and Adults , 2007, Journal of Cognitive Neuroscience.

[66]  Sarah-Jayne Blakemore,et al.  The Development of Adolescent Social Cognition , 2009, Annals of the New York Academy of Sciences.