Breakdown of category-specific word representations in a brain-constrained neurocomputational model of semantic dementia

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Shtyrov, Y.; Efremov, A.; Kuptsova, A.; Wennekers, T.; Gutkin, B. and Garagnani, M.. 2023. Breakdown of category-specific word representations in a brain-constrained neurocomputational model of semantic dementia. Scientific Reports, 13, 19572. ISSN 2045-2322 [Article]

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Official URL: https://www.nature.com/articles/s41598-023-41922-8

Abstract or 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.

Item Type:

Article

Identification Number (DOI):

https://doi.org/10.1038/s41598-023-41922-8

Additional Information:

Tis research was supported by a grant by RF Ministry of Science and Higher Education (grant ID: 075-15- 2022-325) to HSE University. Also supported by Aarhus University, ENS—Paris, Goldsmiths—University of London, and University of Plymouth.

Data Access Statement:

Simulation software (including virtual machine and respective code) as well as the data generated and analysed in the present study are available at: https://tinyurl.com/SDneurosim. All software and data are provided as is, with no recourse to support; the authors take no responsibility for the use of these by any third parties. Note that no human data have been used in this study, and all data are a result of neurocomputational simulations.

Keywords:

language; word acquisition; cortex; embodied cognition; neurodegenerative disease; conceptual knowledge; simulated lesion; Hebbian learning; computational model; neural simulation; grey matter; white matter; fronto-temporal dementia (FTD); frontotemporal lobar degeneration (FTD); semantic dementia (SD); semantic variant primary progressive aphasia (svPPA)

Departments, Centres and Research Units:

Computing

Dates: