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Reorganization of the Social Brain in Individuals with Only One Intact Cerebral Hemisphere

Kliemann, Dorit and Adolphs, Ralph and Paul, Lynn K. and Tyszka, J. Michael and Tranel, Daniel (2021) Reorganization of the Social Brain in Individuals with Only One Intact Cerebral Hemisphere. Brain Sciences, 11 (8). Art. No. 965. ISSN 2076-3425. PMCID PMC8392565. doi:10.3390/brainsci11080965. https://resolver.caltech.edu/CaltechAUTHORS:20210817-224516597

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Abstract

Social cognition and emotion are ubiquitous human processes that recruit a reliable set of brain networks in healthy individuals. These brain networks typically comprise midline (e.g., medial prefrontal cortex) as well as lateral regions of the brain including homotopic regions in both hemispheres (e.g., left and right temporo-parietal junction). Yet the necessary roles of these networks, and the broader roles of the left and right cerebral hemispheres in socioemotional functioning, remains debated. Here, we investigated these questions in four rare adults whose right (three cases) or left (one case) cerebral hemisphere had been surgically removed (to a large extent) to treat epilepsy. We studied four closely matched healthy comparison participants, and also compared the patient findings to data from a previously published larger healthy comparison sample (n = 33). Participants completed standardized socioemotional and cognitive assessments to investigate social cognition. Functional magnetic resonance imaging (fMRI) data were obtained during passive viewing of a short, animated movie that distinctively recruits two social brain networks: one engaged when thinking about other agents’ internal mental states (e.g., beliefs, desires, emotions; so-called Theory of Mind or ToM network), and the second engaged when thinking about bodily states (e.g., pain, hunger; so-called PAIN network). Behavioral assessments demonstrated remarkably intact general cognitive functioning in all individuals with hemispherectomy. Social-emotional functioning was somewhat variable in the hemispherectomy participants, but strikingly, none of these individuals had consistently impaired social-emotional processing and none of the assessment scores were consistent with a psychiatric disorder. Using inter-region correlation analyses, we also found surprisingly typical ToM and PAIN networks, as well as typical differentiation of the two networks (in the intact hemisphere of patients with either right or left hemispherectomy), based on idiosyncratic reorganization of cortical activation. The findings argue that compensatory brain networks can process social and emotional information following hemispherectomy across different age levels (from 3 months to 20 years old), and suggest that social brain networks typically distributed across midline and lateral brain regions in this domain can be reorganized, to a substantial degree


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.3390/brainsci11080965DOIArticle
https://nda.nih.gov/edit_collection.html?id=2417Related ItemData
https://openneuro.org/datasets/ds000228Related ItemData
http://www.ncbi.nlm.nih.gov/pmc/articles/pmc8392565/PubMed CentralArticle
ORCID:
AuthorORCID
Adolphs, Ralph0000-0002-8053-9692
Paul, Lynn K.0000-0002-3128-8313
Tyszka, J. Michael0000-0001-9342-9014
Tranel, Daniel0000-0002-1338-1389
Additional Information:© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). Received: 1 June 2021; Accepted: 14 July 2021; Published: 22 July 2021. (This article belongs to the Special Issue Emotions and the Right Hemisphere) We thank Hilary Richardson for generously providing comparison data from Richardson et al., 2018, as well as earlier comments on the manuscript and analyses. We thank the laboratory of Warren Brown at Fuller Graduate School of Psychology for providing IQ data from participants with hemispherectomy. We thank the participants and their families for their important contribution to our ongoing work on this condition. We thank Monika Jones for great encouragement and organizational support. This project was funded in large part by the Brain Recovery Project. Additional support was provided by NSF grant BCS-1845958 (RA, LKP), NIH/NIMH grant 5 P50 MH094258 (JMT, RA, LKP), and the Kiwanis Neuroscience Research Foundation (DT). Author Contributions: Conceptualization, D.K., D.T., L.K.P., R.A.; Methodology, D.K., D.T., J.M.T., L.K.P., R.A.; Software, D.K., J.M.T.; Validation, D.K., J.M.T., L.K.P.; Formal Analysis, D.K., J.M.T., L.K.P.; Investigation, D.K., J.M.T., L.K.P.; Resources, J.M.T., L.K.P., R.A.; Data Curation, D.K., J.M.T., L.K.P.; Writing—Original Draft Preparation, D.K., D.T., L.K.P., R.A.; Writing—Review and Editing, D.K., D.T., J.M.T., L.K.P., R.A.; Visualization, D.K.; Supervision, D.K., D.T., L.K.P., R.A.; Project Administration, D.K., L.K.P., R.A.; Funding Acquisition, R.A., L.K.P. All authors have read and agreed to the published version of the manuscript. Institutional Review Board Statement: The study was conducted according to the guidelines of the Declaration of Helsinki, and approved by the Institutional Review Board of the California Institute of Technology (protocols 17-0398–1/12/2018, 19-0234 3/27/2019, 16-0692B 01/31/2017). Informed Consent Statement: Written informed consent was obtained from all subjects involved in the study. Data Availability Statement: The data presented in this study are in part openly available in [https://nda.nih.gov/edit_collection.html?id=2417, accessed on 15 July 2021, https://openneuro.org/datasets/ds000228, accessed on 15 July 2021,); data from hemispherectomy subjects are not publicly available due to privacy restrictions.
Group:Tianqiao and Chrissy Chen Institute for Neuroscience
Funders:
Funding AgencyGrant Number
Brain Recovery ProjectUNSPECIFIED
NSFBCS-1845958
NIH5 P50 MH094258
Kiwanis Neuroscience Research FoundationUNSPECIFIED
Subject Keywords:emotion; social cognition; hemispherectomy; theory of mind; fMRI; plasticity
Issue or Number:8
PubMed Central ID:PMC8392565
DOI:10.3390/brainsci11080965
Record Number:CaltechAUTHORS:20210817-224516597
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20210817-224516597
Official Citation:Kliemann, D.; Adolphs, R.; Paul, L.K.; Tyszka, J.M.; Tranel, D. Reorganization of the Social Brain in Individuals with Only One Intact Cerebral Hemisphere. Brain Sci. 2021, 11, 965. https://doi.org/10.3390/brainsci11080965
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:110301
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:18 Aug 2021 16:24
Last Modified:30 Aug 2021 16:47

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