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      Single-neuronal predictions of others’ beliefs in humans

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          Abstract

          Human social behavior crucially depends on our ability to reason about others. This capacity for ‘theory of mind’ plays a vital role in social cognition because it allows us not only to form a detailed understanding of the hidden thoughts and beliefs of other individuals but to also understand that they may differ from our own 13 . Although a number of areas in the human brain have been linked to social reasoning 4, 5 and its disruption across a variety of psychosocial disorders 68 , the basic cellular mechanisms that underlie human theory of mind remain undefined. Using a rare opportunity to acutely record from single cells in the human dorsomedial prefrontal cortex, we discover neurons that reliably encode information about others’ beliefs across richly varying scenarios and that distinguish self- from other-belief related representations. By further following their encoding dynamics, we show how these cells represent the contents of the other’s beliefs and accurately predict whether they are true or false. We also show how they track inferred beliefs from another’s specific perspective and how their activities relate to behavioral performance. Together, these findings reveal a detailed cellular process in the human dorsomedial prefrontal cortex for representing another’s beliefs and identify candidate neurons that could support theory of mind.

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          Most cited references62

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          People thinking about thinking people. The role of the temporo-parietal junction in "theory of mind".

          Humans powerfully and flexibly interpret the behaviour of other people based on an understanding of their minds: that is, we use a "theory of mind." In this study we distinguish theory of mind, which represents another person's mental states, from a representation of the simple presence of another person per se. The studies reported here establish for the first time that a region in the human temporo-parietal junction (here called the TPJ-M) is involved specifically in reasoning about the contents of another person's mind. First, the TPJ-M was doubly dissociated from the nearby extrastriate body area (EBA; Downing et al., 2001). Second, the TPJ-M does not respond to false representations in non-social control stories. Third, the BOLD response in the TPJ-M bilaterally was higher when subjects read stories about a character's mental states, compared with stories that described people in physical detail, which did not differ from stories about nonhuman objects. Thus, the role of the TPJ-M in understanding other people appears to be specific to reasoning about the content of mental states.
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            People thinking about thinking peopleThe role of the temporo-parietal junction in “theory of mind”

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              Single-neuron responses in humans during execution and observation of actions.

              Direct recordings in monkeys have demonstrated that neurons in frontal and parietal areas discharge during execution and perception of actions [1-8]. Because these discharges "reflect" the perceptual aspects of actions of others onto the motor repertoire of the perceiver, these cells have been called mirror neurons. Their overlapping sensory-motor representations have been implicated in observational learning and imitation, two important forms of learning [9]. In humans, indirect measures of neural activity support the existence of sensory-motor mirroring mechanisms in homolog frontal and parietal areas [10, 11], other motor regions [12-15], and also the existence of multisensory mirroring mechanisms in nonmotor regions [16-19]. We recorded extracellular activity from 1177 cells in human medial frontal and temporal cortices while patients executed or observed hand grasping actions and facial emotional expressions. A significant proportion of neurons in supplementary motor area, and hippocampus and environs, responded to both observation and execution of these actions. A subset of these neurons demonstrated excitation during action-execution and inhibition during action-observation. These findings suggest that multiple systems in humans may be endowed with neural mechanisms of mirroring for both the integration and differentiation of perceptual and motor aspects of actions performed by self and others. Copyright © 2010 Elsevier Ltd. All rights reserved.
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                Author and article information

                Journal
                0410462
                6011
                Nature
                Nature
                Nature
                0028-0836
                1476-4687
                18 December 2020
                27 January 2021
                March 2021
                27 July 2021
                : 591
                : 7851
                : 610-614
                Affiliations
                [1 ]Department of Neurosurgery, Massachusetts General Hospital, Harvard Medical School, Boston MA
                [2 ]Brain and Cognitive Sciences, Massachusetts Institute of Technology, Boston MA
                [3 ]Harvard-MIT Division of Health Sciences and Technology, Boston MA
                [4 ]Program in Neuroscience, Harvard Medical School, Boston MA
                Author notes

                Contributions: M.J performed the analysis, M.J, B.G. and R.B.-M performed the experiments, E.F. and R.S. provided feedback and Z.M.W conceived and designed the study, performed the experiments, obtained the recordings and oversaw the project.

                [* ]corresponding author, zwilliams@ 123456mgh.harvard.edu
                Article
                NIHMS1654341
                10.1038/s41586-021-03184-0
                7990696
                33505022
                e3f1e53c-694f-4b8e-bdb5-fb17d89274bc

                Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use: http://www.nature.com/authors/editorial_policies/license.html#terms

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