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Abstract
SummaryAn 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.
Highlights
In humans and other animals, ‘‘cognitive maps’’ (Craik, 1943; Tolman, 1948)—rich internal models of the world that account for the relationships between objects and events—are supported by neural representations within hippocampal-entorhinal cortex (HEC) (Behrens et al, 2018; Bellmund et al, 2018; O’Keefe and Nadel, 1978)
We show that patients exhibit abnormalities in the temporal dynamics of spontaneous memory reactivations, and associated high-frequency oscillations, during post-learning rest, mirroring those seen in animal models (Altimus et al, 2015; Suh et al, 2013; Zaremba et al, 2017)
In the post-learning rest period, we found evidence for forward sequenceness associated with a peak transition lag of 40–50 ms in the combined sample of patients and controls, replicating previous findings (Liu et al, 2019) (maximal effect at 40 ms lag: b = 0.89 ± 0.27, PFWE = 0.005, peak-level significance threshold derived from a non-parametric permutation test, family-wise error (FWE) corrected across lags, n = 54; Figure 4B)
Summary
In humans and other animals, ‘‘cognitive maps’’ (Craik, 1943; Tolman, 1948)—rich internal models of the world that account for the relationships between objects and events—are supported by neural representations within hippocampal-entorhinal cortex (HEC) (Behrens et al, 2018; Bellmund et al, 2018; O’Keefe and Nadel, 1978) This has been described best in rodents during active navigation, where subpopulations of HEC pyramidal neurons exhibit spatially localized firing fields (e.g., place and grid cells; Fyhn et al, 2004; Hafting et al, 2005; O’Keefe and Dostrovsky, 1971; Wilson and McNaughton, 1993).
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