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Breakdown of category-specific word representations in a brain-constrained neurocomputational model of semantic dementia
The neurobiological nature of semantic knowledge, i.e., the encoding and storage of conceptual information in the human brain, remains a poorly understood and hotly debated subject. Clinical data on semantic deficits and neuroimaging evidence from healthy individuals have suggested multiple cortical...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Nature Publishing Group UK
2023
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Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10638411/ https://www.ncbi.nlm.nih.gov/pubmed/37949997 http://dx.doi.org/10.1038/s41598-023-41922-8 |
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author | Shtyrov, Yury Efremov, Aleksei Kuptsova, Anastasia Wennekers, Thomas Gutkin, Boris Garagnani, Max |
author_facet | Shtyrov, Yury Efremov, Aleksei Kuptsova, Anastasia Wennekers, Thomas Gutkin, Boris Garagnani, Max |
author_sort | Shtyrov, Yury |
collection | PubMed |
description | The neurobiological nature of semantic knowledge, i.e., the encoding and storage of conceptual information in the human brain, remains a poorly understood and hotly debated subject. Clinical data on semantic deficits and neuroimaging evidence from healthy individuals have suggested multiple cortical regions to be involved in the processing of meaning. These include semantic hubs (most notably, anterior temporal lobe, ATL) that take part in semantic processing in general as well as sensorimotor areas that process specific aspects/categories according to their modality. Biologically inspired neurocomputational models can help elucidate the exact roles of these regions in the functioning of the semantic system and, importantly, in its breakdown in neurological deficits. We used a neuroanatomically constrained computational model of frontotemporal cortices implicated in word acquisition and processing, and adapted it to simulate and explain the effects of semantic dementia (SD) on word processing abilities. SD is a devastating, yet insufficiently understood progressive neurodegenerative disease, characterised by semantic knowledge deterioration that is hypothesised to be specifically related to neural damage in the ATL. The behaviour of our brain-based model is in full accordance with clinical data—namely, word comprehension performance decreases as SD lesions in ATL progress, whereas word repetition abilities remain less affected. Furthermore, our model makes predictions about lesion- and category-specific effects of SD: our simulation results indicate that word processing should be more impaired for object- than for action-related words, and that degradation of white matter should produce more severe consequences than the same proportion of grey matter decay. In sum, the present results provide a neuromechanistic explanatory account of cortical-level language impairments observed during the onset and progress of semantic dementia. |
format | Online Article Text |
id | pubmed-10638411 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
spelling | pubmed-106384112023-11-11 Breakdown of category-specific word representations in a brain-constrained neurocomputational model of semantic dementia Shtyrov, Yury Efremov, Aleksei Kuptsova, Anastasia Wennekers, Thomas Gutkin, Boris Garagnani, Max Sci Rep Article The neurobiological nature of semantic knowledge, i.e., the encoding and storage of conceptual information in the human brain, remains a poorly understood and hotly debated subject. Clinical data on semantic deficits and neuroimaging evidence from healthy individuals have suggested multiple cortical regions to be involved in the processing of meaning. These include semantic hubs (most notably, anterior temporal lobe, ATL) that take part in semantic processing in general as well as sensorimotor areas that process specific aspects/categories according to their modality. Biologically inspired neurocomputational models can help elucidate the exact roles of these regions in the functioning of the semantic system and, importantly, in its breakdown in neurological deficits. We used a neuroanatomically constrained computational model of frontotemporal cortices implicated in word acquisition and processing, and adapted it to simulate and explain the effects of semantic dementia (SD) on word processing abilities. SD is a devastating, yet insufficiently understood progressive neurodegenerative disease, characterised by semantic knowledge deterioration that is hypothesised to be specifically related to neural damage in the ATL. The behaviour of our brain-based model is in full accordance with clinical data—namely, word comprehension performance decreases as SD lesions in ATL progress, whereas word repetition abilities remain less affected. Furthermore, our model makes predictions about lesion- and category-specific effects of SD: our simulation results indicate that word processing should be more impaired for object- than for action-related words, and that degradation of white matter should produce more severe consequences than the same proportion of grey matter decay. In sum, the present results provide a neuromechanistic explanatory account of cortical-level language impairments observed during the onset and progress of semantic dementia. Nature Publishing Group UK 2023-11-10 /pmc/articles/PMC10638411/ /pubmed/37949997 http://dx.doi.org/10.1038/s41598-023-41922-8 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Article Shtyrov, Yury Efremov, Aleksei Kuptsova, Anastasia Wennekers, Thomas Gutkin, Boris Garagnani, Max Breakdown of category-specific word representations in a brain-constrained neurocomputational model of semantic dementia |
title | Breakdown of category-specific word representations in a brain-constrained neurocomputational model of semantic dementia |
title_full | Breakdown of category-specific word representations in a brain-constrained neurocomputational model of semantic dementia |
title_fullStr | Breakdown of category-specific word representations in a brain-constrained neurocomputational model of semantic dementia |
title_full_unstemmed | Breakdown of category-specific word representations in a brain-constrained neurocomputational model of semantic dementia |
title_short | Breakdown of category-specific word representations in a brain-constrained neurocomputational model of semantic dementia |
title_sort | breakdown of category-specific word representations in a brain-constrained neurocomputational model of semantic dementia |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10638411/ https://www.ncbi.nlm.nih.gov/pubmed/37949997 http://dx.doi.org/10.1038/s41598-023-41922-8 |
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