Neural processing associated with cognitive and affective Theory of Mind in adolescents and adults.

Theory of Mind (ToM) is the ability to attribute thoughts, intentions and beliefs to others. This involves component processes, including cognitive perspective taking (cognitive ToM) and understanding emotions (affective ToM). This study assessed the distinction and overlap of neural processes involved in these respective components, and also investigated their development between adolescence and adulthood. While data suggest that ToM develops between adolescence and adulthood, these populations have not been compared on cognitive and affective ToM domains. Using fMRI with 15 adolescent (aged 11-16 years) and 15 adult (aged 24-40 years) males, we assessed neural responses during cartoon vignettes requiring cognitive ToM, affective ToM or physical causality comprehension (control). An additional aim was to explore relationships between fMRI data and self-reported empathy. Both cognitive and affective ToM conditions were associated with neural responses in the classic ToM network across both groups, although only affective ToM recruited medial/ventromedial PFC (mPFC/vmPFC). Adolescents additionally activated vmPFC more than did adults during affective ToM. The specificity of the mPFC/vmPFC response during affective ToM supports evidence from lesion studies suggesting that vmPFC may integrate affective information during ToM. Furthermore, the differential neural response in vmPFC between adult and adolescent groups indicates developmental changes in affective ToM processing.

[1]  Hanna Damasio,et al.  Impairment of social and moral behavior related to early damage in human prefrontal cortex , 1999, Nature Neuroscience.

[2]  D. Farrington,et al.  Development and validation of the Basic Empathy Scale. , 2006, Journal of adolescence.

[3]  Jean Decety,et al.  Neurodevelopmental changes in the circuits underlying empathy and sympathy from childhood to adulthood. , 2010, Developmental science.

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

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

[6]  H. Wimmer,et al.  “John thinks that Mary thinks that…” attribution of second-order beliefs by 5- to 10-year-old children ☆ , 1985 .

[7]  G. Coricelli Two-levels of mental states attribution: from automaticity to voluntariness , 2005, Neuropsychologia.

[8]  R. Saxe Uniquely human social cognition , 2006, Current Opinion in Neurobiology.

[9]  M. Tomasello,et al.  Does the chimpanzee have a theory of mind? 30 years later , 2008, Trends in Cognitive Sciences.

[10]  Ulrike M. Krämer,et al.  Emotional and cognitive aspects of empathy and their relation to social cognition—an fMRI-study , 2010, Brain Research.

[11]  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.

[12]  J Aharon-Peretz,et al.  Impaired “Affective Theory of Mind” Is Associated with Right Ventromedial Prefrontal Damage , 2005, Cognitive and behavioral neurology : official journal of the Society for Behavioral and Cognitive Neurology.

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

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

[15]  K. Blair,et al.  The Psychopath: Emotion and the Brain , 2005 .

[16]  Simone G. Shamay-Tsoory,et al.  The role of the orbitofrontal cortex in affective theory of mind deficits in criminal offenders with psychopathic tendencies , 2010, Cortex.

[17]  C. Frith,et al.  Social Cognition in Humans , 2007, Current Biology.

[18]  Jean Decety,et al.  The Neurodevelopment of Empathy in Humans , 2010, Developmental Neuroscience.

[19]  C. Frith,et al.  Functional imaging of ‘theory of mind’ , 2003, Trends in Cognitive Sciences.

[20]  Rebecca Elliott,et al.  Neuronal correlates of theory of mind and empathy: A functional magnetic resonance imaging study in a nonverbal task , 2006, NeuroImage.

[21]  Iroise Dumontheil,et al.  Online usage of theory of mind continues to develop in late adolescence. , 2010, Developmental science.

[22]  Simone G. Shamay-Tsoory,et al.  The ventromedial prefrontal cortex is involved in understanding affective but not cognitive theory of mind stories , 2006, Social neuroscience.

[23]  Simone G. Shamay-Tsoory,et al.  Dissociable prefrontal networks for cognitive and affective theory of mind: A lesion study , 2007, Neuropsychologia.

[24]  Dennis A. Nowak,et al.  Dissociating cognitive from affective theory of mind: A TMS study , 2010, Cortex.

[25]  R. Jones,et al.  Recognition of Faux Pas by Normally Developing Children and Children with Asperger Syndrome or High-Functioning Autism , 1999, Journal of autism and developmental disorders.

[26]  H. Critchley,et al.  A common role of insula in feelings, empathy and uncertainty , 2009, Trends in Cognitive Sciences.

[27]  Geoffrey Bird,et al.  Development during Adolescence of the Neural Processing of Social Emotion , 2009, Journal of Cognitive Neuroscience.

[28]  G. Baird,et al.  Prevalence of disorders of the autism spectrum in a population cohort of children in South Thames: the Special Needs and Autism Project (SNAP) , 2006, The Lancet.

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

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

[31]  John O. Willis,et al.  Wechsler Abbreviated Scale of Intelligence , 2014 .

[32]  T. Singer,et al.  The empathic brain: how, when and why? , 2006, Trends in Cognitive Sciences.

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