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Evolutionary modifications in human brain connectivity associated with schizophrenia

The genetic basis and human-specific character of schizophrenia has led to the hypothesis that human brain evolution may have played a role in the development of the disorder. We examined schizophrenia-related changes in brain connectivity in the context of evolutionary changes in human brain wiring...

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Autores principales: van den Heuvel, Martijn P, Scholtens, Lianne H, de Lange, Siemon C, Pijnenburg, Rory, Cahn, Wiepke, van Haren, Neeltje E M, Sommer, Iris E, Bozzali, Marco, Koch, Kathrin, Boks, Marco P, Repple, Jonathan, Pievani, Michela, Li, Longchuan, Preuss, Todd M, Rilling, James K
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6906591/
https://www.ncbi.nlm.nih.gov/pubmed/31724729
http://dx.doi.org/10.1093/brain/awz330
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author van den Heuvel, Martijn P
Scholtens, Lianne H
de Lange, Siemon C
Pijnenburg, Rory
Cahn, Wiepke
van Haren, Neeltje E M
Sommer, Iris E
Bozzali, Marco
Koch, Kathrin
Boks, Marco P
Repple, Jonathan
Pievani, Michela
Li, Longchuan
Preuss, Todd M
Rilling, James K
author_facet van den Heuvel, Martijn P
Scholtens, Lianne H
de Lange, Siemon C
Pijnenburg, Rory
Cahn, Wiepke
van Haren, Neeltje E M
Sommer, Iris E
Bozzali, Marco
Koch, Kathrin
Boks, Marco P
Repple, Jonathan
Pievani, Michela
Li, Longchuan
Preuss, Todd M
Rilling, James K
author_sort van den Heuvel, Martijn P
collection PubMed
description The genetic basis and human-specific character of schizophrenia has led to the hypothesis that human brain evolution may have played a role in the development of the disorder. We examined schizophrenia-related changes in brain connectivity in the context of evolutionary changes in human brain wiring by comparing in vivo neuroimaging data from humans and chimpanzees, one of our closest living evolutionary relatives and a species with which we share a very recent common ancestor. We contrasted the connectome layout between the chimpanzee and human brain and compared differences with the pattern of schizophrenia-related changes in brain connectivity as observed in patients. We show evidence of evolutionary modifications of human brain connectivity to significantly overlap with the cortical pattern of schizophrenia-related dysconnectivity (P < 0.001, permutation testing). We validated these effects in three additional, independent schizophrenia datasets. We further assessed the specificity of effects by examining brain dysconnectivity patterns in seven other psychiatric and neurological brain disorders (including, among others, major depressive disorder and obsessive-compulsive disorder, arguably characterized by behavioural symptoms that are less specific to humans), which showed no such associations with modifications of human brain connectivity. Comparisons of brain connectivity across humans, chimpanzee and macaques further suggest that features of connectivity that evolved in the human lineage showed the strongest association to the disorder, that is, brain circuits potentially related to human evolutionary specializations. Taken together, our findings suggest that human-specific features of connectome organization may be enriched for changes in brain connectivity related to schizophrenia. Modifications in human brain connectivity in service of higher order brain functions may have potentially also rendered the brain vulnerable to brain dysfunction.
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spelling pubmed-69065912019-12-16 Evolutionary modifications in human brain connectivity associated with schizophrenia van den Heuvel, Martijn P Scholtens, Lianne H de Lange, Siemon C Pijnenburg, Rory Cahn, Wiepke van Haren, Neeltje E M Sommer, Iris E Bozzali, Marco Koch, Kathrin Boks, Marco P Repple, Jonathan Pievani, Michela Li, Longchuan Preuss, Todd M Rilling, James K Brain Original Articles The genetic basis and human-specific character of schizophrenia has led to the hypothesis that human brain evolution may have played a role in the development of the disorder. We examined schizophrenia-related changes in brain connectivity in the context of evolutionary changes in human brain wiring by comparing in vivo neuroimaging data from humans and chimpanzees, one of our closest living evolutionary relatives and a species with which we share a very recent common ancestor. We contrasted the connectome layout between the chimpanzee and human brain and compared differences with the pattern of schizophrenia-related changes in brain connectivity as observed in patients. We show evidence of evolutionary modifications of human brain connectivity to significantly overlap with the cortical pattern of schizophrenia-related dysconnectivity (P < 0.001, permutation testing). We validated these effects in three additional, independent schizophrenia datasets. We further assessed the specificity of effects by examining brain dysconnectivity patterns in seven other psychiatric and neurological brain disorders (including, among others, major depressive disorder and obsessive-compulsive disorder, arguably characterized by behavioural symptoms that are less specific to humans), which showed no such associations with modifications of human brain connectivity. Comparisons of brain connectivity across humans, chimpanzee and macaques further suggest that features of connectivity that evolved in the human lineage showed the strongest association to the disorder, that is, brain circuits potentially related to human evolutionary specializations. Taken together, our findings suggest that human-specific features of connectome organization may be enriched for changes in brain connectivity related to schizophrenia. Modifications in human brain connectivity in service of higher order brain functions may have potentially also rendered the brain vulnerable to brain dysfunction. Oxford University Press 2019-12 2019-11-14 /pmc/articles/PMC6906591/ /pubmed/31724729 http://dx.doi.org/10.1093/brain/awz330 Text en © The Author(s) (2019). Published by Oxford University Press on behalf of the Guarantors of Brain. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Original Articles
van den Heuvel, Martijn P
Scholtens, Lianne H
de Lange, Siemon C
Pijnenburg, Rory
Cahn, Wiepke
van Haren, Neeltje E M
Sommer, Iris E
Bozzali, Marco
Koch, Kathrin
Boks, Marco P
Repple, Jonathan
Pievani, Michela
Li, Longchuan
Preuss, Todd M
Rilling, James K
Evolutionary modifications in human brain connectivity associated with schizophrenia
title Evolutionary modifications in human brain connectivity associated with schizophrenia
title_full Evolutionary modifications in human brain connectivity associated with schizophrenia
title_fullStr Evolutionary modifications in human brain connectivity associated with schizophrenia
title_full_unstemmed Evolutionary modifications in human brain connectivity associated with schizophrenia
title_short Evolutionary modifications in human brain connectivity associated with schizophrenia
title_sort evolutionary modifications in human brain connectivity associated with schizophrenia
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6906591/
https://www.ncbi.nlm.nih.gov/pubmed/31724729
http://dx.doi.org/10.1093/brain/awz330
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