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The role of inhibitory circuits in hippocampal memory processing

Nature Reviews Neuroscience volume 23, pages 476–492 (2022)Cite this article

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Abstract

GABAergic inhibitory circuits play an essential role in coordinating various hippocampal functions. Several decades of work dedicated to a thorough characterization of hippocampal inhibitory populations have highlighted how specific types of interneuron can contribute to network activity. Recent studies have used genetically targeted recordings and peturbations of activity during memory-related behaviours to determine how interneurons that inhibit distinct subcellular domains of principal cells or specialize in principal cell disinhibition may sculpt hippocampal memory. These studies highlight unique contributions of distinct interneuron types to the temporal binding of hippocampal ensembles, synaptic plasticity and the acquisition of spatial and contextual information. Here, we review the current state of knowledge around hippocampal inhibition and memory by discussing the multifaceted roles of populations of inhibitory cells at different stages of hippocampal mnemonic processing.

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Fig. 1: Major types of hippocampal CA1 inhibitory interneurons that express PV, SOM and VIP.
Fig. 2: Activity patterns of CA1 inhibitory interneurons during network oscillations.
Fig. 3: Activity-dependent synaptic plasticity in CA1 inhibitory interneurons.
Fig. 4: Role of hippocampal CA1 interneurons in encoding and consolidation of contextual fear memory.

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Acknowledgements

The authors’ work was supported by the Canadian Institutes of Health Research and the Natural Sciences and Engineering Research Council of Canada. The authors thank D. Topolnik for preparation of figures.

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Authors and Affiliations

  1. Department of Biochemistry, Microbiology and Bio-informatics, Laval University, Québec City, Québec, Canada

    Lisa Topolnik & Suhel Tamboli

  2. Neuroscience Axis, CRCHUQ, Laval University, Québec City, Québec, Canada

    Lisa Topolnik & Suhel Tamboli

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  1. Lisa Topolnik
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Both authors contributed equally to the preparation of the manuscript.

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Correspondence to Lisa Topolnik.

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Glossary

Declarative memory

The capacity to store facts about the world (semantic memory) and episodes of everyday life (episodic memory).

Spatial mapping

The acquisition of information in relation to spatial location and orientation.

Memory encoding

The acquisition of experience-associated information by changes in activity levels, synaptic strengths and connectivity patterns in the neuronal networks that make memory systems.

Context

The static features of an environment that define the place in which an experience occurred.

Memory retrieval

The process that allows recall of experience-related information stored in memory traces using a relevant cue.

Memory consolidation

The transformation of temporary experience-associated memory constructs into long-lasting memory traces.

Phase precession

Progressive advancement in the time of firing of action potentials by individual place cells in relation to the phase of the extracellular theta oscillation.

Spatial remapping

The acquisition of information in response to altered spatial location and orientation.

Spatial working memory

The ability of animals to retain spatial information over a long period of time.

Goal-oriented spatial learning

A behavioural paradigm in which spatial learning is reinforced by a reward or punishment.

Novel object recognition

A paradigm in which an animal is exposed to two identical objects and, after a certain delay, is re-exposed to one novel object and one previously explored (familiar) object. Object memory is evaluated from the animal’s capacity to spend more time exploring a novel object than a familiar one.

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Topolnik, L., Tamboli, S. The role of inhibitory circuits in hippocampal memory processing. Nat Rev Neurosci 23, 476–492 (2022). https://doi.org/10.1038/s41583-022-00599-0

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