Familiarity modulates the functional relationship between theory of mind and autobiographical memory

Qualitative and quantitative reviews of the neuroimaging literature show that overlapping brain regions support theory of mind (ToM) and autobiographical memory (AM). This overlap has been taken to suggest that individuals draw on past personal experiences to infer others' mental states, but work with amnesic people shows that ToM does not always depend on AM. One variable that may determine the extent to which one relies on AM when inferring another's thoughts and feelings during ToM is whether that individual is personally known. To test this possibility, participants were scanned with fMRI as they remembered past experiences in response to personal photos ('AM' condition) and imagined others' experiences in response to photos of personally familiar ('pToM' condition) and unfamiliar ('ToM' condition) others. Spatiotemporal Partial Least Squares was used to identify the spatial and temporal characteristics of neural activation patterns associated with AM, pToM, and ToM. We found that the brain regions supporting pToM more closely resembled those supporting AM relative to ToM involving unfamiliar others, with the greatest degree of overlap within midline regions. A complementary finding was the observation of striking differences between pToM and ToM such that midline regions associated with AM predominated during pToM, whereas more lateral regions associated with social semantic memory predominated during ToM. Overall, this study demonstrates that ToM involves a dynamic interplay between AM and social semantic memory that is biased towards AM when a personally familiar other is the subject of the mental state inference.

[1]  D. Hassabis,et al.  Deconstructing episodic memory with construction , 2007, Trends in Cognitive Sciences.

[2]  Stephen C. Strother,et al.  An evaluation of methods for detecting brain activations from functional neuroimages , 2002, Artif. Intell. Medicine.

[3]  Pascale Piolino,et al.  Theory of mind impairments in patients with semantic dementia. , 2012, Brain : a journal of neurology.

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

[5]  Fenna M. Krienen,et al.  Clan Mentality: Evidence That the Medial Prefrontal Cortex Responds to Close Others , 2010, The Journal of Neuroscience.

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

[7]  Roberto Cabeza,et al.  Other Perspectives , 2015 .

[8]  J. Haxby,et al.  Neural systems for recognition of familiar faces , 2007, Neuropsychologia.

[9]  Lee Ryan,et al.  Impaired Category Fluency in Medial Temporal Lobe Amnesia: The Role of Episodic Memory , 2009, The Journal of Neuroscience.

[10]  Lila Davachi,et al.  The ensemble that plays together, stays together , 2004, Hippocampus.

[11]  Russell A. Epstein Parahippocampal and retrosplenial contributions to human spatial navigation , 2008, Trends in Cognitive Sciences.

[12]  D. Schacter,et al.  The cognitive neuroscience of constructive memory: remembering the past and imagining the future , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[13]  A. R. McIntosh,et al.  Spatiotemporal analysis of event-related fMRI data using partial least squares , 2004, NeuroImage.

[14]  D. Schacter,et al.  Constructive episodic simulation of the future and the past: Distinct subsystems of a core brain network mediate imagining and remembering , 2009, Neuropsychologia.

[15]  Morris Moscovitch,et al.  Recollective qualities modulate hippocampal activation during autobiographical memory retrieval , 2004, Hippocampus.

[16]  M. Moscovitch,et al.  Recollective performance advantages for implicit memory tasks , 2010, Memory.

[17]  Brian Levine,et al.  Theory of Mind Is Independent of Episodic Memory , 2007, Science.

[18]  E. Tulving Memory and consciousness. , 1985 .

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

[20]  Craig E. L. Stark,et al.  When zero is not zero: The problem of ambiguous baseline conditions in fMRI , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Robert Tibshirani,et al.  Bootstrap Methods for Standard Errors, Confidence Intervals, and Other Measures of Statistical Accuracy , 1986 .

[22]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[23]  John M. Gardiner,et al.  Experiences of Remembering, Knowing, and Guessing , 1998, Consciousness and Cognition.

[24]  G. Winocur,et al.  Aging and autobiographical memory: dissociating episodic from semantic retrieval. , 2002, Psychology and aging.

[25]  S. Baron-Cohen,et al.  Another advanced test of theory of mind: evidence from very high functioning adults with autism or asperger syndrome. , 1997, Journal of child psychology and psychiatry, and allied disciplines.

[26]  R. Corcoran Theory of mind and schizophrenia. , 2001 .

[27]  Richard S. J. Frackowiak,et al.  The Mind's Eye—Precuneus Activation in Memory-Related Imagery , 1995, NeuroImage.

[28]  Georg Northoff,et al.  Self-referential processing in our brain—A meta-analysis of imaging studies on the self , 2006, NeuroImage.

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

[30]  J. Fleiss,et al.  Intraclass correlations: uses in assessing rater reliability. , 1979, Psychological bulletin.

[31]  Donald T. Stuss,et al.  Common and Unique Neural Correlates of Autobiographical Memory and Theory of Mind , 2010, Journal of Cognitive Neuroscience.

[32]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[33]  S. Baron-Cohen,et al.  The "Reading the Mind in the Eyes" Test revised version: a study with normal adults, and adults with Asperger syndrome or high-functioning autism. , 2001, Journal of child psychology and psychiatry, and allied disciplines.

[34]  Arthur Aron,et al.  Confusions of Self With Close Others , 2003, Personality & social psychology bulletin.

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

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

[37]  Jean Decety,et al.  Love hurts: An fMRI study , 2010, NeuroImage.

[38]  R. Nathan Spreng,et al.  The Common Neural Basis of Autobiographical Memory, Prospection, Navigation, Theory of Mind, and the Default Mode: A Quantitative Meta-analysis , 2009, Journal of Cognitive Neuroscience.

[39]  B. Levine,et al.  The functional neuroanatomy of autobiographical memory: A meta-analysis , 2006, Neuropsychologia.

[40]  D. Hassabis,et al.  Using Imagination to Understand the Neural Basis of Episodic Memory , 2007, The Journal of Neuroscience.

[41]  Morris Moscovitch,et al.  New views on old memories: re-evaluating the role of the hippocampal complex , 2001, Behavioural Brain Research.

[42]  G. Winocur,et al.  Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory , 2005, Journal of anatomy.

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

[44]  Matthew D. Lieberman 5. Self-knowledge: from philosophy to neuroscience to psychology , 2012 .

[45]  G. Winocur,et al.  Memory formation and long-term retention in humans and animals: Convergence towards a transformation account of hippocampal–neocortical interactions , 2010, Neuropsychologia.

[46]  G. Winocur,et al.  Remembering our past: functional neuroanatomy of recollection of recent and very remote personal events. , 2004, Cerebral cortex.

[47]  G. Winocur,et al.  “I have often walked down this street before”: fMRI Studies on the hippocampus and other structures during mental navigation of an old environment , 2004, Hippocampus.

[48]  C. Neil Macrae,et al.  The Link between Social Cognition and Self-referential Thought in the Medial Prefrontal Cortex , 2005, Journal of Cognitive Neuroscience.

[49]  Joseph M. Andreano,et al.  Sex influences on the neurobiology of learning and memory. , 2009, Learning & memory.

[50]  H. Eichenbaum The hippocampus and declarative memory: cognitive mechanisms and neural codes , 2001, Behavioural Brain Research.

[51]  R. N. Spreng,et al.  I remember you: A role for memory in social cognition and the functional neuroanatomy of their interaction , 2012, Brain Research.

[52]  Talma Hendler,et al.  Projecting memories: The role of the hippocampus in emotional mentalizing , 2011, NeuroImage.

[53]  G. Winocur,et al.  The cognitive neuroscience of remote episodic, semantic and spatial memory , 2006, Current Opinion in Neurobiology.

[54]  R. Nathan Spreng,et al.  Patterns of Brain Activity Supporting Autobiographical Memory, Prospection, and Theory of Mind, and Their Relationship to the Default Mode Network , 2010, Journal of Cognitive Neuroscience.

[55]  Demis Hassabis,et al.  Cortical midline involvement in autobiographical memory , 2009, NeuroImage.

[56]  N. Cohen,et al.  Amnesia is a Deficit in Relational Memory , 2000, Psychological science.

[57]  G. Winocur,et al.  Amnesia as an impairment of detail generation and binding: Evidence from personal, fictional, and semantic narratives in K.C. , 2009, Neuropsychologia.

[58]  Alex Martin,et al.  Semantic memory and the brain: structure and processes , 2001, Current Opinion in Neurobiology.