Cognitive and Affective Perspective-Taking: Evidence for Shared and Dissociable Anatomical Substrates

Perspective-taking refers to the ability to recognize another person's point of view. Crucial to the development of interpersonal relationships and prosocial behavior, perspective-taking is closely linked to human empathy, and like empathy, perspective-taking is commonly subdivided into cognitive and affective components. While the two components of empathy have been frequently compared, the differences between cognitive and affective perspective-taking have been under-investigated in the cognitive neuroscience literature to date. Here, we define cognitive perspective-taking as the ability to infer an agent's thoughts or beliefs, and affective perspective-taking as the ability to infer an agent's feelings or emotions. In this paper, we review data from functional imaging studies in healthy adults as well as behavioral and structural imaging studies in patients with behavioral variant frontotemporal dementia in order to determine if there are distinct neural correlates for cognitive and affective perspective-taking. Data suggest that there are both shared and non-shared cognitive and anatomic substrates. For example, while both types of perspective-taking engage regions such as the temporoparietal junction, precuneus, and temporal poles, only affective perspective-taking engages regions within the limbic system and basal ganglia. Differences are also observed in prefrontal cortex: while affective perspective-taking engages ventromedial prefrontal cortex, cognitive perspective-taking engages dorsomedial prefrontal cortex and dorsolateral prefrontal cortex (DLPFC). To corroborate these findings, we also examine if cognitive and affective perspective-taking share the same relationship with executive functions. While it is clear that affective perspective-taking requires emotional substrates that are less prominent in cognitive perspective-taking, it remains unknown to what extent executive functions (including working memory, mental set switching, and inhibitory control) may contribute to each process. Overall results indicate that cognitive perspective-taking is dependent on executive functioning (particularly mental set switching), while affective perspective-taking is less so. We conclude with a critique of the current literature, with a focus on the different outcome measures used across studies and misconceptions due to imprecise terminology, as well as recommendations for future research.

[1]  J. Aharon-Peretz,et al.  Two systems for empathy: a double dissociation between emotional and cognitive empathy in inferior frontal gyrus versus ventromedial prefrontal lesions. , 2009, Brain : a journal of neurology.

[2]  J. Decety,et al.  The functional architecture of human empathy. , 2004, Behavioral and cognitive neuroscience reviews.

[3]  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.

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

[5]  Riitta Parkkola,et al.  Is emotional contagion special? An fMRI study on neural systems for affective and cognitive empathy , 2008, NeuroImage.

[6]  J. Hodges,et al.  Uncovering the Neural Bases of Cognitive and Affective Empathy Deficits in Alzheimer's Disease and the Behavioral-Variant of Frontotemporal Dementia. , 2016, Journal of Alzheimer's disease : JAD.

[7]  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.

[8]  M. Weiner,et al.  Neural substrates of socioemotional self-awareness in neurodegenerative disease , 2014, Brain and behavior.

[9]  J. Cacioppo,et al.  Differential Impairment of Cognitive and Affective Mentalizing Abilities in Neurodegenerative Dementias: Evidence from Behavioral Variant of Frontotemporal Dementia, Alzheimer's Disease, and Mild Cognitive Impairment. , 2016, Journal of Alzheimer's disease : JAD.

[10]  M. Diehl,et al.  Empathy across the adult lifespan: Longitudinal and experience-sampling findings. , 2008, Emotion.

[11]  Howard J. Rosen,et al.  Distinctive Neuropsychological Patterns in Frontotemporal Dementia, Semantic Dementia, And Alzheimer Disease , 2003, Cognitive and behavioral neurology : official journal of the Society for Behavioral and Cognitive Neurology.

[12]  Oscar Alcantar,et al.  Standardised measurement of self-awareness deficits in FTD and AD , 2009, Journal of Neurology, Neurosurgery & Psychiatry.

[13]  James Stiller,et al.  Perspective-taking and memory capacity predict social network size , 2007, Soc. Networks.

[14]  Brian Avants,et al.  Neuroanatomy of Apathy and Disinhibition in Frontotemporal Lobar Degeneration , 2009, Dementia and Geriatric Cognitive Disorders.

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

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

[17]  S. Cappa,et al.  Neural correlates of empathic impairment in the behavioral variant of frontotemporal dementia , 2014, Alzheimer's & Dementia.

[18]  F. Manes,et al.  Differential Cognitive and Affective Theory of Mind Abilities at Mild and Moderate Stages of Behavioral Variant Frontotemporal Dementia , 2015, Cognitive and behavioral neurology : official journal of the Society for Behavioral and Cognitive Neurology.

[19]  S Antani,et al.  Metacognitive deficits in frontotemporal dementia , 2005, Journal of Neurology, Neurosurgery & Psychiatry.

[20]  Peter Kirsch,et al.  The involvement of emotion recognition in affective theory of mind. , 2010, Psychophysiology.

[21]  Penelope A. Lewis,et al.  Ventromedial prefrontal volume predicts understanding of others and social network size , 2011, NeuroImage.

[22]  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.

[23]  B L Miller,et al.  Self awareness and personality change in dementia , 2005, Journal of Neurology, Neurosurgery & Psychiatry.

[24]  Nick C Fox,et al.  Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia. , 2011, Brain : a journal of neurology.

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

[26]  M. Grossman,et al.  Self-appraisal in behavioural variant frontotemporal degeneration , 2012, Journal of Neurology, Neurosurgery & Psychiatry.

[27]  K. Ochsner,et al.  The neuroscience of empathy: progress, pitfalls and promise , 2012, Nature Neuroscience.

[28]  P. Eslinger,et al.  Social cognition, executive functioning, and neuroimaging correlates of empathic deficits in frontotemporal dementia. , 2011, The Journal of neuropsychiatry and clinical neurosciences.

[29]  J. Grafman,et al.  Theory of mind impairment in patients with behavioural variant fronto-temporal dementia (bv-FTD) increases caregiver burden. , 2015, Age and ageing.

[30]  J. Decety,et al.  Primary empathy deficits in frontotemporal dementia , 2014, Front. Aging Neurosci..

[31]  Mark H. Davis Measuring individual differences in empathy: Evidence for a multidimensional approach. , 1983 .

[32]  S. Shamay-Tsoory,et al.  Neuroanatomical and neurochemical bases of theory of mind , 2011, Neuropsychologia.

[33]  K. Rankin,et al.  Parsing cognitive and emotional empathy deficits for negative and positive stimuli in frontotemporal dementia , 2015, Neuropsychologia.

[34]  Lara Schlaffke,et al.  Shared and nonshared neural networks of cognitive and affective theory‐of‐mind: A neuroimaging study using cartoon picture stories , 2015, Human brain mapping.

[35]  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.

[36]  A. Hillis Inability to empathize: brain lesions that disrupt sharing and understanding another's emotions. , 2014, Brain : a journal of neurology.

[37]  F. Pasquier,et al.  My belief or yours? Differential theory of mind deficits in frontotemporal dementia and Alzheimer's disease. , 2012, Brain : a journal of neurology.

[38]  Katy A. Cross,et al.  Patterns of neuropsychological impairment in frontotemporal dementia , 2007, Neurology.

[39]  Jodie A. Baird,et al.  False-belief understanding in frontotemporal dementia and Alzheimer's disease , 2009, Journal of clinical and experimental neuropsychology.

[40]  L. Phillips,et al.  The overlapping relationship between emotion perception and theory of mind , 2015, Neuropsychologia.

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

[42]  A. Böckler,et al.  Decoding the Charitable Brain: Empathy, Perspective Taking, and Attention Shifts Differentially Predict Altruistic Giving , 2016, The Journal of Neuroscience.

[43]  M. Grossman,et al.  Getting on the same page: The neural basis for social coordination deficits in behavioral variant frontotemporal degeneration , 2015, Neuropsychologia.

[44]  Eveline A. Crone,et al.  Sharing and giving across adolescence: an experimental study examining the development of prosocial behavior , 2014, Front. Psychol..

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

[46]  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.

[47]  M. J. Emerson,et al.  The Unity and Diversity of Executive Functions and Their Contributions to Complex “Frontal Lobe” Tasks: A Latent Variable Analysis , 2000, Cognitive Psychology.

[48]  S. Shamay-Tsoory The Neural Bases for Empathy , 2011, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[49]  John R. Hodges,et al.  Social reasoning, emotion and empathy in frontotemporal dementia , 2006, Neuropsychologia.

[50]  Jodie A. Baird,et al.  Please Scroll down for Article Journal of Clinical and Experimental Neuropsychology Empathy in Frontotemporal Dementia and Alzheimer's Disease , 2022 .

[51]  S. Cappa,et al.  Affective mentalizing and brain activity at rest in the behavioral variant of frontotemporal dementia , 2015, NeuroImage: Clinical.