Impaired neural replay of inferred relationships in schizophrenia

An ability to build structured mental maps of the world underpins our capacity to imagine relationships between objects that extend beyond experience. In rodents, such representations are supported by sequential place cell reactivations during rest, known as replay. Schizophrenia is proposed to refl...

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Bibliographic Details
Published in:Cell 2021-08, Vol.184 (16), p.4315-4328.e17
Main Authors: Nour, Matthew M., Liu, Yunzhe, Arumuham, Atheeshaan, Kurth-Nelson, Zeb, Dolan, Raymond J.
Format: Article
Language:English
Subjects:
Alpha Rhythm - physiology
Behavior
Brain Mapping
cognitive map
Female
Hippocampus - physiopathology
Humans
Learning
Magnetoencephalography
Male
mental simulation
model-based inference
Models, Biological
Neurons - pathology
psychosis
schema
Schizophrenia - pathology
Schizophrenia - physiopathology
Task Performance and Analysis
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Summary:An ability to build structured mental maps of the world underpins our capacity to imagine relationships between objects that extend beyond experience. In rodents, such representations are supported by sequential place cell reactivations during rest, known as replay. Schizophrenia is proposed to reflect a compromise in structured mental representations, with animal models reporting abnormalities in hippocampal replay and associated ripple activity during rest. Here, utilizing magnetoencephalography (MEG), we tasked patients with schizophrenia and control participants to infer unobserved relationships between objects by reorganizing visual experiences containing these objects. During a post-task rest session, controls exhibited fast spontaneous neural reactivation of presented objects that replayed inferred relationships. Replay was coincident with increased ripple power in hippocampus. Patients showed both reduced replay and augmented ripple power relative to controls, convergent with findings in animal models. These abnormalities are linked to impairments in behavioral acquisition and subsequent neural representation of task structure. [Display omitted] •Patients with schizophrenia show impairments in inferring sequential relationships•Patients show reduced neural replay, during rest, for inferred structure•Replay-associated ripple power is elevated in patients, as in animal models•Patients show blunted representations of task structure, related to ripple power In support of schizophrenia reflecting compromised cognitive maps of the environment, patients with schizophrenia display abnormalities in hippocampal replay relative to controls.
ISSN:0092-8674
1097-4172
DOI:10.1016/j.cell.2021.06.012