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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...
Autores principales: | , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Oxford University Press
2019
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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. |
format | Online Article Text |
id | pubmed-6906591 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
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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