Temporal pole activity during understanding other persons' mental states correlates with neuroticism trait

Comprehension of other persons' mental states is one of the representative cognitive functions involved in social situations. It has been suggested that this function sometimes recruits emotional processes. The present fMRI study examined the neural mechanisms associated with understanding others' mental states, and the conditions that determine the recruitment of the emotional processes. The false belief paradigm, a traditional behavioral paradigm to investigate comprehension of others, was applied to an event-related fMRI analysis, allowing for the extraction of brain activity time-locked to successful understanding of others' mental states. Prominent brain activity was observed in multiple cortical regions including the medial prefrontal cortex, temporo-parietal junction, precuneus, and temporal pole. Then, correlational analyses were performed between the activations and individuals' scores of neuroticism, a personality trait that reflects emotional instability in daily life. It was revealed that the neuroticism scores were positively correlated with the activity in the temporal pole region, but not in the other regions. These results suggest that the emotional processes implemented in the temporal pole are recruited during successful understanding of other persons' mental states, and that the recruitment may be modulated by an emotional personality trait of individual subjects.

[1]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited—Again , 1995, NeuroImage.

[2]  D. Stuss,et al.  The frontal lobes are necessary for 'theory of mind'. , 2001, Brain : a journal of neurology.

[3]  Toshio Iijima,et al.  Time-dependent neural activations related to recognition of people's names in emotional and neutral face-name associative learning: an fMRI study , 2003, NeuroImage.

[4]  B. L. Miller,et al.  The influence of right frontotemporal dysfunction on social behavior in frontotemporal dementia , 2001, Neurology.

[5]  Raymond J. Dolan,et al.  Fear Recognition Ability Predicts Differences in Social Cognitive and Neural Functioning in Men , 2006, Journal of Cognitive Neuroscience.

[6]  D. Premack,et al.  Does the chimpanzee have a theory of mind? , 1978, Behavioral and Brain Sciences.

[7]  Walter Mischel,et al.  Toward an integrative science of the person. , 2004, Annual review of psychology.

[8]  C. Frith,et al.  Interacting minds--a biological basis. , 1999, Science.

[9]  U. Frith Emanuel Miller lecture: confusions and controversies about Asperger syndrome. , 2004, Journal of child psychology and psychiatry, and allied disciplines.

[10]  A. Bandura Social cognitive theory: an agentic perspective. , 1999, Annual review of psychology.

[11]  B R Karney,et al.  The longitudinal course of marital quality and stability: a review of theory, method, and research. , 1995, Psychological bulletin.

[12]  K. Kendler,et al.  Low extraversion and high neuroticism as indices of genetic and environmental risk for social phobia, agoraphobia, and animal phobia. , 2007, The American journal of psychiatry.

[13]  R. Hobson The autistic child's appraisal of expressions of emotion. , 1986, Journal of child psychology and psychiatry, and allied disciplines.

[14]  F. Happé An advanced test of theory of mind: Understanding of story characters' thoughts and feelings by able autistic, mentally handicapped, and normal children and adults , 1994, Journal of autism and developmental disorders.

[15]  Robin I. M. Dunbar,et al.  Theory of mind deficits in bipolar affective disorder. , 2003, Journal of affective disorders.

[16]  T. Rogers,et al.  Where do you know what you know? The representation of semantic knowledge in the human brain , 2007, Nature Reviews Neuroscience.

[17]  W. K. Simmons,et al.  The anterior temporal lobes and the functional architecture of semantic memory , 2009, Journal of the International Neuropsychological Society.

[18]  N. Bolger,et al.  Personality and the problems of everyday life: the role of neuroticism in exposure and reactivity to daily stressors. , 1991, Journal of personality.

[19]  K. Zilles,et al.  Mind Reading: Neural Mechanisms of Theory of Mind and Self-Perspective , 2001, NeuroImage.

[20]  I. Wilkinson,et al.  Investigating the functional anatomy of empathy and forgiveness , 2001, Neuroreport.

[21]  D. Perrett,et al.  Dissociable neural responses to facial expressions of sadness and anger. , 1999, Brain : a journal of neurology.

[22]  I. Olson,et al.  The Enigmatic temporal pole: a review of findings on social and emotional processing. , 2007, Brain : a journal of neurology.

[23]  Y. Miyashita,et al.  Temporal pole activity during perception of sad faces, but not happy faces, correlates with neuroticism trait , 2009, Neuroscience Letters.

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

[25]  M Mary Konstantareas,et al.  Affect Regulation and Temperament in Children with Autism Spectrum Disorder , 2006, Journal of autism and developmental disorders.

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

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

[28]  U. Frith,et al.  Prospects for a cognitive neuropsychology of autism: Hobson's choice. , 1990, Psychological review.

[29]  R. Buckner,et al.  Self-projection and the brain , 2007, Trends in Cognitive Sciences.

[30]  G. Rizzolatti,et al.  The mirror-neuron system. , 2004, Annual review of neuroscience.

[31]  Richard S. J. Frackowiak,et al.  Other minds in the brain: a functional imaging study of “theory of mind” in story comprehension , 1995, Cognition.

[32]  Yasuyuki Gondo,et al.  日本版NEO-PI-Rの作成とその因子的妥当性の検討 , 1998 .

[33]  Uta Frith,et al.  Theory of mind , 2001, Current Biology.

[34]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

[35]  J. Dunn,et al.  Understanding mind and emotion: longitudinal associations with mental-state talk between young friends. , 1998, Developmental psychology.

[36]  Hanneke E. M. den Ouden,et al.  Thinking about intentions , 2005, NeuroImage.

[37]  F. Happé The role of age and verbal ability in the theory of mind task performance of subjects with autism. , 1995, Child development.

[38]  A. David,et al.  A prospective study of the effects of anterior temporal lobectomy on emotion recognition and theory of mind , 2007, Neuropsychologia.

[39]  R. Buckner,et al.  Transient Activation during Block Transition , 2001, NeuroImage.

[40]  Hiroshi Matsuda,et al.  Impaired self-awareness and theory of mind: An fMRI study of mentalizing in alexithymia , 2006, NeuroImage.

[41]  S. Baron-Cohen,et al.  The ‘Reading the Mind in the Voice’ Test-Revised: A Study of Complex Emotion Recognition in Adults with and Without Autism Spectrum Conditions , 2007, Journal of autism and developmental disorders.

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

[43]  C. Polkey,et al.  "Theory of mind" impairments and their relationship to executive functioning following frontal lobe excisions. , 2001, Brain : a journal of neurology.

[44]  S. Baron-Cohen,et al.  Does the autistic child have a “theory of mind” ? , 1985, Cognition.

[45]  R. Gordon Folk Psychology as Simulation , 1986 .

[46]  S. Carey,et al.  Understanding other minds: linking developmental psychology and functional neuroimaging. , 2004, Annual review of psychology.

[47]  C. Frith,et al.  How we predict what other people are going to do , 2006, Brain Research.

[48]  A. Dale,et al.  Functional-Anatomic Correlates of Object Priming in Humans Revealed by Rapid Presentation Event-Related fMRI , 1998, Neuron.

[49]  Jill A Jacobson,et al.  Mental state decoding abilities in clinical depression. , 2005, Journal of affective disorders.

[50]  R. Knight,et al.  Frontal Lobe Contributions to Theory of Mind , 1998, Journal of Cognitive Neuroscience.

[51]  Luke Clark,et al.  The relationship between affective decision-making and theory of mind in the frontal variant of fronto-temporal dementia , 2007, Neuropsychologia.

[52]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[53]  V. Ramachandran,et al.  The simulating social mind: the role of the mirror neuron system and simulation in the social and communicative deficits of autism spectrum disorders. , 2007, Psychological bulletin.

[54]  H. Wimmer,et al.  Beliefs about beliefs: Representation and constraining function of wrong beliefs in young children's understanding of deception , 1983, Cognition.

[55]  Gregory J. Meyer,et al.  Structural convergence of mood and personality: Evidence for old and new directions. , 1989 .

[56]  Jason P. Mitchell,et al.  Dissociable Medial Prefrontal Contributions to Judgments of Similar and Dissimilar Others , 2006, Neuron.

[57]  P. Costa,et al.  Influence of extraversion and neuroticism on subjective well-being: happy and unhappy people. , 1980, Journal of personality and social psychology.

[58]  Ian A. Apperly,et al.  Intact first- and second-order false belief reasoning in a patient with severely impaired grammar , 2006, Social neuroscience.

[59]  T. Singer The neuronal basis and ontogeny of empathy and mind reading: Review of literature and implications for future research , 2006, Neuroscience & Biobehavioral Reviews.

[60]  H. Eysenck Dimensions of Personality , 1947 .

[61]  M. Hallett,et al.  Modeling other minds , 1995, Neuroreport.

[62]  C. Frith,et al.  Movement and Mind: A Functional Imaging Study of Perception and Interpretation of Complex Intentional Movement Patterns , 2000, NeuroImage.

[63]  S. Kanba,et al.  Deficit in theory of mind is a risk for relapse of major depression. , 2006, Journal of affective disorders.

[64]  Daniel Cervone,et al.  The Coherence of Personality: Social-Cognitive Bases of Consistency, Variability, and Organization , 1999 .

[65]  Suk-Ho Shin Confusions and Controversies about Asperger Syndrome , 2008 .

[66]  M. Brass,et al.  Imitation: is cognitive neuroscience solving the correspondence problem? , 2005, Trends in Cognitive Sciences.

[67]  R. McCrae,et al.  An introduction to the five-factor model and its applications. , 1992, Journal of personality.

[68]  J. Decety,et al.  Effect of subjective perspective taking during simulation of action: a PET investigation of agency , 2001, Nature Neuroscience.

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

[70]  J. Decety,et al.  A PET Investigation of the Attribution of Intentions with a Nonverbal Task , 2000, NeuroImage.

[71]  C. Frith,et al.  Reading the mind in cartoons and stories: an fMRI study of ‘theory of mind’ in verbal and nonverbal tasks , 2000, Neuropsychologia.

[72]  V. Cervin Individual behavior in social situations: its relation to anxiety, neuroticism, and group solidarity. , 1956, Journal of experimental psychology.

[73]  Kevin N. Ochsner,et al.  The neural correlates of direct and reflected self-knowledge , 2005, NeuroImage.

[74]  G. Fink,et al.  Cerebral Representation of One’s Own Past: Neural Networks Involved in Autobiographical Memory , 1996, The Journal of Neuroscience.

[75]  Maria Luisa Gorno-Tempini,et al.  Structural anatomy of empathy in neurodegenerative disease. , 2006, Brain : a journal of neurology.