Failure to engage the temporoparietal junction/posterior superior temporal sulcus predicts impaired naturalistic social cognition in schizophrenia

Schizophrenia is associated with marked impairments in social cognition. However, the neural correlates of these deficits remain unclear. Here we use naturalistic stimuli to examine the role of the right temporoparietal junction/posterior superior temporal sulcus (TPJ-pSTS)—an integrative hub for th...

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Published in	Brain (London, England : 1878) Vol. 144; no. 6; pp. 1898 - 1910
Main Authors	Patel, Gaurav H, Arkin, Sophie C, Ruiz-Betancourt, Daniel R, Plaza, Fabiola I, Mirza, Safia A, Vieira, Daniel J, Strauss, Nicole E, Klim, Casimir C, Sanchez-Peña, Juan P, Bartel, Laura P, Grinband, Jack, Martinez, Antigona, Berman, Rebecca A, Ochsner, Kevin N, Leopold, David A, Javitt, Daniel C
Format	Journal Article
Language	English
Published	England Oxford University Press 28.07.2021
Subjects	Adult Female Humans Magnetic Resonance Imaging Male Original Parietal Lobe - physiopathology Schizophrenia - physiopathology Social Cognition Temporal Lobe - physiopathology functional MRI visual scanning attention biological motion hubs
Online Access	Get full text
ISSN	0006-8950 1460-2156 1460-2156
DOI	10.1093/brain/awab081

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Abstract	Schizophrenia is associated with marked impairments in social cognition. However, the neural correlates of these deficits remain unclear. Here we use naturalistic stimuli to examine the role of the right temporoparietal junction/posterior superior temporal sulcus (TPJ-pSTS)—an integrative hub for the cortical networks pertinent to the understanding complex social situations—in social inference, a key component of social cognition, in schizophrenia. Twenty-seven schizophrenia participants and 21 healthy control subjects watched a clip of the film The Good, the Bad and the Ugly while high resolution multiband functional MRI images were collected. We used inter-subject correlation to measure the evoked activity, which we then compared to social cognition as measured by The Awareness of Social Inference Test (TASIT). We also compared between groups the TPJ-pSTS blood oxygen level-dependent activity (i) relationship with the motion content in the film; (ii) synchronization with other cortical areas involved in the viewing of the movie; and (iii) relationship with the frequency of saccades made during the movie. Activation deficits were greatest in middle TPJ (TPJm) and correlated significantly with impaired TASIT performance across groups. Follow-up analyses of the TPJ-pSTS revealed decreased synchronization with other cortical areas, decreased correlation with the motion content of the movie, and decreased correlation with the saccades made during the movie. The functional impairment of the TPJm, a hub area in the middle of the TPJ-pSTS, predicts deficits in social inference in schizophrenia participants by disrupting the integration of visual motion processing into the TPJ. This disrupted integration then affects the use of the TPJ to guide saccades during the visual scanning of the movie clip. These findings suggest that the TPJ may be a treatment target for improving deficits in a key component of social cognition in schizophrenia participants.
AbstractList	Schizophrenia is associated with marked impairments in social cognition. However, the neural correlates of these deficits remain unclear. Here we use naturalistic stimuli to examine the role of the right temporoparietal junction/posterior superior temporal sulcus (TPJ-pSTS)-an integrative hub for the cortical networks pertinent to the understanding complex social situations-in social inference, a key component of social cognition, in schizophrenia. Twenty-seven schizophrenia participants and 21 healthy control subjects watched a clip of the film The Good, the Bad and the Ugly while high resolution multiband functional MRI images were collected. We used inter-subject correlation to measure the evoked activity, which we then compared to social cognition as measured by The Awareness of Social Inference Test (TASIT). We also compared between groups the TPJ-pSTS blood oxygen level-dependent activity (i) relationship with the motion content in the film; (ii) synchronization with other cortical areas involved in the viewing of the movie; and (iii) relationship with the frequency of saccades made during the movie. Activation deficits were greatest in middle TPJ (TPJm) and correlated significantly with impaired TASIT performance across groups. Follow-up analyses of the TPJ-pSTS revealed decreased synchronization with other cortical areas, decreased correlation with the motion content of the movie, and decreased correlation with the saccades made during the movie. The functional impairment of the TPJm, a hub area in the middle of the TPJ-pSTS, predicts deficits in social inference in schizophrenia participants by disrupting the integration of visual motion processing into the TPJ. This disrupted integration then affects the use of the TPJ to guide saccades during the visual scanning of the movie clip. These findings suggest that the TPJ may be a treatment target for improving deficits in a key component of social cognition in schizophrenia participants.Schizophrenia is associated with marked impairments in social cognition. However, the neural correlates of these deficits remain unclear. Here we use naturalistic stimuli to examine the role of the right temporoparietal junction/posterior superior temporal sulcus (TPJ-pSTS)-an integrative hub for the cortical networks pertinent to the understanding complex social situations-in social inference, a key component of social cognition, in schizophrenia. Twenty-seven schizophrenia participants and 21 healthy control subjects watched a clip of the film The Good, the Bad and the Ugly while high resolution multiband functional MRI images were collected. We used inter-subject correlation to measure the evoked activity, which we then compared to social cognition as measured by The Awareness of Social Inference Test (TASIT). We also compared between groups the TPJ-pSTS blood oxygen level-dependent activity (i) relationship with the motion content in the film; (ii) synchronization with other cortical areas involved in the viewing of the movie; and (iii) relationship with the frequency of saccades made during the movie. Activation deficits were greatest in middle TPJ (TPJm) and correlated significantly with impaired TASIT performance across groups. Follow-up analyses of the TPJ-pSTS revealed decreased synchronization with other cortical areas, decreased correlation with the motion content of the movie, and decreased correlation with the saccades made during the movie. The functional impairment of the TPJm, a hub area in the middle of the TPJ-pSTS, predicts deficits in social inference in schizophrenia participants by disrupting the integration of visual motion processing into the TPJ. This disrupted integration then affects the use of the TPJ to guide saccades during the visual scanning of the movie clip. These findings suggest that the TPJ may be a treatment target for improving deficits in a key component of social cognition in schizophrenia participants. Schizophrenia is associated with marked impairments in social cognition. However, the neural correlates of these deficits remain unclear. Here we use naturalistic stimuli to examine the role of the right temporoparietal junction/posterior superior temporal sulcus (TPJ-pSTS)-an integrative hub for the cortical networks pertinent to the understanding complex social situations-in social inference, a key component of social cognition, in schizophrenia. Twenty-seven schizophrenia participants and 21 healthy control subjects watched a clip of the film The Good, the Bad and the Ugly while high resolution multiband functional MRI images were collected. We used inter-subject correlation to measure the evoked activity, which we then compared to social cognition as measured by The Awareness of Social Inference Test (TASIT). We also compared between groups the TPJ-pSTS blood oxygen level-dependent activity (i) relationship with the motion content in the film; (ii) synchronization with other cortical areas involved in the viewing of the movie; and (iii) relationship with the frequency of saccades made during the movie. Activation deficits were greatest in middle TPJ (TPJm) and correlated significantly with impaired TASIT performance across groups. Follow-up analyses of the TPJ-pSTS revealed decreased synchronization with other cortical areas, decreased correlation with the motion content of the movie, and decreased correlation with the saccades made during the movie. The functional impairment of the TPJm, a hub area in the middle of the TPJ-pSTS, predicts deficits in social inference in schizophrenia participants by disrupting the integration of visual motion processing into the TPJ. This disrupted integration then affects the use of the TPJ to guide saccades during the visual scanning of the movie clip. These findings suggest that the TPJ may be a treatment target for improving deficits in a key component of social cognition in schizophrenia participants. Schizophrenia is associated with marked impairments in social cognition. However, the neural correlates of these deficits remain unclear. Here we use naturalistic stimuli to examine the role of the right temporoparietal junction/posterior superior temporal sulcus (TPJ-pSTS)—an integrative hub for the cortical networks pertinent to the understanding complex social situations—in social inference, a key component of social cognition, in schizophrenia. Twenty-seven schizophrenia participants and 21 healthy control subjects watched a clip of the film The Good, the Bad and the Ugly while high resolution multiband functional MRI images were collected. We used inter-subject correlation to measure the evoked activity, which we then compared to social cognition as measured by The Awareness of Social Inference Test (TASIT). We also compared between groups the TPJ-pSTS blood oxygen level-dependent activity (i) relationship with the motion content in the film; (ii) synchronization with other cortical areas involved in the viewing of the movie; and (iii) relationship with the frequency of saccades made during the movie. Activation deficits were greatest in middle TPJ (TPJm) and correlated significantly with impaired TASIT performance across groups. Follow-up analyses of the TPJ-pSTS revealed decreased synchronization with other cortical areas, decreased correlation with the motion content of the movie, and decreased correlation with the saccades made during the movie. The functional impairment of the TPJm, a hub area in the middle of the TPJ-pSTS, predicts deficits in social inference in schizophrenia participants by disrupting the integration of visual motion processing into the TPJ. This disrupted integration then affects the use of the TPJ to guide saccades during the visual scanning of the movie clip. These findings suggest that the TPJ may be a treatment target for improving deficits in a key component of social cognition in schizophrenia participants. Social functioning deficits are pervasive and disabling in schizophrenia, but their neural substrates remain poorly understood. Patel et al. reveal how deficits within a social cognition hub unique to human cortex impair the ability of individuals with schizophrenia to follow complex dynamic social situations.
Author	Leopold, David A Mirza, Safia A Ochsner, Kevin N Vieira, Daniel J Martinez, Antigona Javitt, Daniel C Grinband, Jack Arkin, Sophie C Ruiz-Betancourt, Daniel R Sanchez-Peña, Juan P Patel, Gaurav H Klim, Casimir C Bartel, Laura P Strauss, Nicole E Plaza, Fabiola I Berman, Rebecca A
AuthorAffiliation	3 Department of Psychology, University of California , Los Angeles, CA 90095, USA 1 Department of Psychiatry, Columbia University Medical Center , New York, NY 10032, USA 4 Palo Alto University , Palo Alto, CA 94304, USA 6 Schizophrenia Research Division, Nathan Kline Institute , Orangeburg, NY 10962, USA 8 Department of Psychology, Columbia University , New York, NY 10027, USA 2 Division of Experimental Therapeutics, New York State Psychiatric Institute , New York, NY 10032, USA 7 Section on Cognitive Neurophysiology and Imaging, National Institute of Mental Health , Bethesda, MD 20814, USA 5 University of Michigan Medical School , Ann Arbor, MI 48109, USA
AuthorAffiliation_xml	– name: 6 Schizophrenia Research Division, Nathan Kline Institute , Orangeburg, NY 10962, USA – name: 4 Palo Alto University , Palo Alto, CA 94304, USA – name: 2 Division of Experimental Therapeutics, New York State Psychiatric Institute , New York, NY 10032, USA – name: 3 Department of Psychology, University of California , Los Angeles, CA 90095, USA – name: 5 University of Michigan Medical School , Ann Arbor, MI 48109, USA – name: 7 Section on Cognitive Neurophysiology and Imaging, National Institute of Mental Health , Bethesda, MD 20814, USA – name: 1 Department of Psychiatry, Columbia University Medical Center , New York, NY 10032, USA – name: 8 Department of Psychology, Columbia University , New York, NY 10027, USA
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Snippet	Schizophrenia is associated with marked impairments in social cognition. However, the neural correlates of these deficits remain unclear. Here we use...
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SubjectTerms	Adult Female Humans Magnetic Resonance Imaging Male Original Parietal Lobe - physiopathology Schizophrenia - physiopathology Social Cognition Temporal Lobe - physiopathology
Title	Failure to engage the temporoparietal junction/posterior superior temporal sulcus predicts impaired naturalistic social cognition in schizophrenia
URI	https://www.ncbi.nlm.nih.gov/pubmed/33710282 https://www.proquest.com/docview/2501257311 https://pubmed.ncbi.nlm.nih.gov/PMC8320281 https://academic.oup.com/brain/article-pdf/144/6/1898/39427621/awab081.pdf
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