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Trajectories through semantic spaces in schizophrenia and the relationship to ripple bursts

Nour, Matthew M; McNamee, Daniel C; Liu, Yunzhe; Dolan, Raymond J; (2023) Trajectories through semantic spaces in schizophrenia and the relationship to ripple bursts. Proceedings of the National Academy of Sciences (PNAS) , 120 (42) , Article e2305290120. 10.1073/pnas.2305290120. Green open access

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Abstract

Human cognition is underpinned by structured internal representations that encode relationships between entities in the world (cognitive maps). Clinical features of schizophrenia-from thought disorder to delusions-are proposed to reflect disorganization in such conceptual representations. Schizophrenia is also linked to abnormalities in neural processes that support cognitive map representations, including hippocampal replay and high-frequency ripple oscillations. Here, we report a computational assay of semantically guided conceptual sampling and exploit this to test a hypothesis that people with schizophrenia (PScz) exhibit abnormalities in semantically guided cognition that relate to hippocampal replay and ripples. Fifty-two participants [26 PScz (13 unmedicated) and 26 age-, gender-, and intelligence quotient (IQ)-matched nonclinical controls] completed a category- and letter-verbal fluency task, followed by a magnetoencephalography (MEG) scan involving a separate sequence-learning task. We used a pretrained word embedding model of semantic similarity, coupled to a computational model of word selection, to quantify the degree to which each participant's verbal behavior was guided by semantic similarity. Using MEG, we indexed neural replay and ripple power in a post-task rest session. Across all participants, word selection was strongly influenced by semantic similarity. The strength of this influence showed sensitivity to task demands (category > letter fluency) and predicted performance. In line with our hypothesis, the influence of semantic similarity on behavior was reduced in schizophrenia relative to controls, predicted negative psychotic symptoms, and correlated with an MEG signature of hippocampal ripple power (but not replay). The findings bridge a gap between phenomenological and neurocomputational accounts of schizophrenia.

Type: Article
Title: Trajectories through semantic spaces in schizophrenia and the relationship to ripple bursts
Location: United States
Open access status: An open access version is available from UCL Discovery
DOI: 10.1073/pnas.2305290120
Publisher version: https://doi.org/10.1073/pnas.2305290120
Language: English
Additional information: Copyright © 2023 the Author(s). Published by PNAS. This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY).
Keywords: cognitive map, hippocampal replay, natural language processing, psychosis, sharp wave ripple
UCL classification: UCL
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences > UCL Queen Square Institute of Neurology
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences > UCL Queen Square Institute of Neurology > Imaging Neuroscience
URI: https://discovery.ucl.ac.uk/id/eprint/10179062
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