The shallow cognitive map hypothesis: A hippocampal framework for thought disorder in schizophrenia

Abstract

Memories are not formed in isolation. They are associated and organized into relational knowledge structures that allow coherent thought. Failure to express such coherent thought is a key hallmark of Schizophrenia. Here we explore the hypothesis that thought disorder arises from disorganized Hippocampal cognitive maps. In doing so, we combine insights from two key lines of investigation, one concerning the neural signatures of cognitive mapping, and another that seeks to understand lower-level cellular mechanisms of cognition within a dynamical systems framework. Specifically, we propose that multiple distinct pathological pathways converge on the shallowing of Hippocampal attractors, giving rise to disorganized Hippocampal cognitive maps and driving conceptual disorganization. We discuss the available evidence at the computational, behavioural, network, and cellular levels. We also outline testable predictions from this framework, including how it could unify major chemical and psychological theories of schizophrenia and how it can provide a rationale for understanding the aetiology and treatment of the disease.

Evidence for shallow cognitive maps in schizophrenia

“…These differences in the representations of task structure were coupled with a general increase in uniformity for the cognitive maps reported by patients. These findings are consistent with and provide novel evidence for the recent shallow cognitive map hypothesis of schizophrenia (Musa et al 2022). This theory posits that dysfunction of the hippocampus in patients results in a shallowing of ‘attractors’, stable states of activity that represent distinct components of memory representations.…”

“…This set of findings about cognitive impairments have led to the recently proposed "shallow cognitive map" hypothesis of schizophrenia. This hypothesis claims that these relational deficits stem from disorganization in hippocampal circuity, leading to disorganized thought (Musa et al 2022). If mechanisms such as those in the hippocampus underlying the formation of cognitive maps (O'Keefe & Nadel, 1978;Whittington et al, 2022) are disrupted in schizophrenia, then many deficits in schizophrenia -including goal-directed decision making -may be a consequence of poorly-built internal representations of the world.…”

Dynamic functional hippocampal markers of residual depressive symptoms in euthymic bipolar disorder

“…Alternatively, aberrant and inappropriately high salience assignment (i.e., attributing disproportionate significance to irrelevant stimuli) has been proposed (Musa et al., 2021) as a marker of high risk for psychosis, a BD symptom, which might be mediated, at least partly, by hippocampal dysfunction and hyperconnectivity with the SN. This may represent a different explanation of the higher dFC between the hippocampus and the SN in our BD patients’ sample.…”

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

“…Thus, in addition to our behavioral findings, we find a relationship between and an MEG measure of replay-associated ripple power, where the latter is measured during a rest session following a separate sequence learning task. We consider this intriguing given an established role for both HEC and hippocampal ripples in associative memory and reasoning across diverse task domains (e.g., spatial memory, non-spatial structure learning, semantic retrieval) ( 10 , 14 – 16 , 18 , 19 , 50 , 53 , 74 , 75 ). Although our cognitive and neural measures were derived from different task paradigms (semantic memory search and non-spatial sequence learning, respectively), under an HEC “cognitive map” hypothesis they are thought to engage similar neural circuits that support reasoning about the relationships between entities ( 14 , 15 ).…”

“…Core clinical features include conceptual disorganization, difficulties in abstract reasoning, and reduced language coherence (i.e., “formal thought disorder”) ( 4 , 5 ), which together predict poor social functioning ( 6 ). A longstanding notion is that these features reflect an abnormality in association-guided cognition ( 7 , 8 ), where associations reflect relationships between memories, concepts, or objects in the world (“relational knowledge”) ( 9 – 11 ).…”