Shared and nonshared neural networks of cognitive and affective theory‐of‐mind: A neuroimaging study using cartoon picture stories

Theory of mind (ToM) refers to the ability to represent one's own and others' cognitive and affective mental states. Recent imaging studies have aimed to disentangle the neural networks involved in cognitive as opposed to affective ToM, based on clinical observations that the two can functionally dissociate. Due to large differences in stimulus material and task complexity findings are, however, inconclusive. Here, we investigated the neural correlates of cognitive and affective ToM in psychologically healthy male participants (n = 39) using functional brain imaging, whereby the same set of stimuli was presented for all conditions (affective, cognitive and control), but associated with different questions prompting either a cognitive or affective ToM inference. Direct contrasts of cognitive versus affective ToM showed that cognitive ToM recruited the precuneus and cuneus, as well as regions in the temporal lobes bilaterally. Affective ToM, in contrast, involved a neural network comprising prefrontal cortical structures, as well as smaller regions in the posterior cingulate cortex and the basal ganglia. Notably, these results were complemented by a multivariate pattern analysis (leave one study subject out), yielding a classifier with an accuracy rate of more than 85% in distinguishing between the two ToM‐conditions. The regions contributing most to successful classification corresponded to those found in the univariate analyses. The study contributes to the differentiation of neural patterns involved in the representation of cognitive and affective mental states of others. Hum Brain Mapp, 36:29–39, 2015. © 2014 Wiley Periodicals, Inc.

[1]  Scott T. Grafton,et al.  Differential role of the orbital frontal lobe in emotional versus cognitive perspective-taking , 2006, Neuropsychologia.

[2]  Volkmar Nicolas,et al.  An fMRI study of theory of mind in schizophrenic patients with “passivity” symptoms , 2008, Neuropsychologia.

[3]  P. Fonagy,et al.  A developmental, mentalization-based approach to the understanding and treatment of borderline personality disorder , 2009, Development and Psychopathology.

[4]  G. Glover,et al.  Reflecting upon Feelings: An fMRI Study of Neural Systems Supporting the Attribution of Emotion to Self and Other , 2004, Journal of Cognitive Neuroscience.

[5]  M. Iacoboni,et al.  The mirror neuron system and the consequences of its dysfunction , 2006, Nature Reviews Neuroscience.

[6]  G. Juckel,et al.  Cooperation and Deception Recruit Different Subsets of the Theory-of-Mind Network , 2008, PloS one.

[7]  M. Adenzato,et al.  Cognitive and affective Theory of Mind in neurodegenerative diseases: Neuropsychological, neuroanatomical and neurochemical levels , 2012, Neuroscience & Biobehavioral Reviews.

[8]  Bryan T. Denny,et al.  Medial prefrontal activity differentiates self from close others. , 2006, Social cognitive and affective neuroscience.

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

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

[11]  Nora C. Vetter,et al.  Ongoing neural development of affective theory of mind in adolescence. , 2014, Social cognitive and affective neuroscience.

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

[13]  Henrik Walter,et al.  Functional relations of empathy and mentalizing: An fMRI study on the neural basis of cognitive empathy , 2011, NeuroImage.

[14]  M. Brüne,et al.  Theory of mind—evolution, ontogeny, brain mechanisms and psychopathology , 2006, Neuroscience & Biobehavioral Reviews.

[15]  M. Brüne,et al.  “Theory of mind” is impaired in Huntington's disease , 2011, Movement disorders : official journal of the Movement Disorder Society.

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

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

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

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

[20]  Simone G. Shamay-Tsoory,et al.  Double dissociation between cognitive and affective empathy in borderline personality disorder , 2010, Psychiatry Research.

[21]  Essi Viding,et al.  Neural responses to affective and cognitive theory of mind in children with conduct problems and varying levels of callous-unemotional traits. , 2012, Archives of general psychiatry.

[22]  Patrik Vuilleumier,et al.  Cognitive and affective theory of mind share the same local patterns of activity in posterior temporal but not medial prefrontal cortex. , 2014, Social cognitive and affective neuroscience.

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

[24]  Mark H. Davis Interpersonal Reactivity Index , 2011 .

[25]  M. Siegal,et al.  Neural systems involved in 'theory of mind' , 2002, Nature Reviews Neuroscience.

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

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

[28]  G. Fink,et al.  Being with virtual others: Neural correlates of social interaction , 2006, Neuropsychologia.

[29]  Glyn W. Humphreys,et al.  Frontal and Temporo-Parietal Lobe Contributions to Theory of Mind: Neuropsychological Evidence from a False-Belief Task with Reduced Language and Executive Demands , 2004, Journal of Cognitive Neuroscience.

[30]  W. Oertel,et al.  Affective and cognitive Theory of Mind in patients with parkinson's disease. , 2010, Parkinsonism & related disorders.

[31]  Martin Tegenthoff,et al.  An fMRI study of “theory of mind” in at-risk states of psychosis: Comparison with manifest schizophrenia and healthy controls , 2011, NeuroImage.

[32]  J. Artieda,et al.  Changes in subthalamic activity during movement observation in Parkinson’s disease: Is the mirror system mirrored in the basal ganglia? , 2010, Clinical Neurophysiology.

[33]  A. Abu-Akel A neurobiological mapping of theory of mind , 2003, Brain Research Reviews.

[34]  Sarah-Jayne Blakemore,et al.  Neural processing associated with cognitive and affective Theory of Mind in adolescents and adults. , 2012, Social cognitive and affective neuroscience.

[35]  Christoph G. Paulus DER SAARBRÜCKER PERSÖNLICHKEITSFRAGEBOGEN SPF(IRI) ZUR MESSUNG VON EMPATHIE: Psychometrische Evaluation der deutschen Version des Interpersonal Reactivity Index , 2009 .

[36]  G. Juckel,et al.  Mentalizing in preclinical Huntington’s disease: an fMRI study using cartoon picture stories , 2012, Brain Imaging and Behavior.

[37]  Beate Sodian,et al.  Neural correlates of true and false belief reasoning , 2007, NeuroImage.

[38]  A. Leslie Pretense and representation: The origins of "theory of mind." , 1987 .

[39]  J. Heverhagen,et al.  Comparing the neural correlates of affective and cognitive theory of mind using fMRI: Involvement of the basal ganglia in affective theory of mind , 2013, Advances in cognitive psychology.

[40]  C. Frith,et al.  Modulation of the mirror system by social relevance. , 2006, Social cognitive and affective neuroscience.

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

[42]  J. Perner,et al.  Neuroscience and Biobehavioral Reviews Fractionating Theory of Mind: a Meta-analysis of Functional Brain Imaging Studies , 2022 .

[43]  J. Aharon-Peretz,et al.  The neuroanatomical basis of affective mentalizing in schizophrenia: Comparison of patients with schizophrenia and patients with localized prefrontal lesions , 2007, Schizophrenia Research.