Homogenization of word relationships in schizophrenia: Topological analysis of cortical semantic representations

Author:

Hayashi Ryusuke1ORCID,Kaji Shizuo2ORCID,Matsumoto Yukiko345ORCID,Nishida Satoshi678ORCID,Nishimoto Shinji67ORCID,Takahashi Hidehiko349ORCID

Affiliation:

1. Human Informatics and Interaction Research Institute National Institute of Advanced Industrial Science and Technology (AIST) Tsukuba Japan

2. Institute of Mathematics for Industry Kyushu University Fukuoka Japan

3. Department of Psychiatry and Behavioral Sciences, Graduate School of Medical and Dental Sciences Tokyo Medical and Dental University Tokyo Japan

4. Department of Psychiatry Graduate School of Medicine, Kyoto University Kyoto Japan

5. Department of Neuropsychiatry Nippon Medical School Tokyo Japan

6. Center for Information and Neural Networks (CiNet) National Institute of Information and Communications Technology (NICT) Osaka Japan

7. Graduate School of Frontier Biosciences Osaka University Osaka Japan

8. Center for Human Nature, Artificial Intelligence, and Neuroscience Hokkaido University Sapporo Japan

9. Center for Brain Integration Research Tokyo Medical and Dental University Tokyo Japan

Abstract

AimPatients with schizophrenia typically exhibit symptoms of disorganized thought and display concreteness and over‐inclusion in verbal reports, depending on the level of abstraction. While concreteness and over‐inclusion may appear contradictory, the underlying psychopathology that explains these symptoms remains unclear. In the current study, we used functional magnetic resonance imaging with an encoding modeling approach to examine how concepts of various words, represented as brain activity, are anomalously connected at different levels of abstraction in patients with schizophrenia.MethodsFourteen individuals diagnosed with schizophrenia and 17 healthy controls underwent functional magnetic resonance imaging to measure brain activity representing concepts of various words. We used a persistent homology (PH) method to analyze the topological structures of word representations in schizophrenia patients, healthy controls, and random data, across different levels of abstraction by varying dissimilarity scales in the representation space.ResultsThe results revealed that patients with schizophrenia exhibited more homogeneous word relationships across different levels of abstraction compared with healthy controls. Additionally, topological structures exhibited a shift toward a random network structure in patients with schizophrenia compared with controls. The PH method successfully distinguished semantic representations of patients with schizophrenia from those of controls.ConclusionsThe current results provide an explanation for the mechanisms underlying the deficits in abstraction ability observed in schizophrenia. The isotopic connection of individual concepts reflects both the reduction of contextual connections at a semantically fine‐grained scale and the absence of clear boundaries between related concepts at a coarse scale, which lead to concreteness and over‐inclusion, respectively.

Funder

Japan Agency for Medical Research and Development

Japan Society for the Promotion of Science

National Institute of Information and Communications Technology

Moonshot Research and Development Program

Publisher

Wiley

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