Temporal context and latent state inference in the hippocampal splitter signal

The hippocampus is thought to enable the encoding and retrieval of ongoing experience, the organization of that experience into structured representations like contexts, maps, and schemas, and the use of these structures to plan for the future. A central goal is to understand what the core computati...

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Main Authors: Éléonore Duvelle, Roddy M Grieves, Matthijs AA van der Meer
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2023-01-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/82357
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author Éléonore Duvelle
Roddy M Grieves
Matthijs AA van der Meer
author_facet Éléonore Duvelle
Roddy M Grieves
Matthijs AA van der Meer
author_sort Éléonore Duvelle
collection DOAJ
description The hippocampus is thought to enable the encoding and retrieval of ongoing experience, the organization of that experience into structured representations like contexts, maps, and schemas, and the use of these structures to plan for the future. A central goal is to understand what the core computations supporting these functions are, and how these computations are realized in the collective action of single neurons. A potential access point into this issue is provided by ‘splitter cells’, hippocampal neurons that fire differentially on the overlapping segment of trajectories that differ in their past and/or future. However, the literature on splitter cells has been fragmented and confusing, owing to differences in terminology, behavioral tasks, and analysis methods across studies. In this review, we synthesize consistent findings from this literature, establish a common set of terms, and translate between single-cell and ensemble perspectives. Most importantly, we examine the combined findings through the lens of two major theoretical ideas about hippocampal function: representation of temporal context and latent state inference. We find that unique signature properties of each of these models are necessary to account for the data, but neither theory, by itself, explains all of its features. Specifically, the temporal gradedness of the splitter signal is strong support for temporal context, but is hard to explain using state models, while its flexibility and task-dependence is naturally accounted for using state inference, but poses a challenge otherwise. These theories suggest a number of avenues for future work, and we believe their application to splitter cells is a timely and informative domain for testing and refining theoretical ideas about hippocampal function.
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spelling doaj.art-07f9f630e77849468560f7aa9402f7582023-01-11T14:59:01ZengeLife Sciences Publications LtdeLife2050-084X2023-01-011210.7554/eLife.82357Temporal context and latent state inference in the hippocampal splitter signalÉléonore Duvelle0https://orcid.org/0000-0002-3514-8801Roddy M Grieves1https://orcid.org/0000-0002-6812-4056Matthijs AA van der Meer2https://orcid.org/0000-0002-2206-4473Department of Psychological and Brain Sciences, Dartmouth College, Hanover, United StatesDepartment of Psychological and Brain Sciences, Dartmouth College, Hanover, United StatesDepartment of Psychological and Brain Sciences, Dartmouth College, Hanover, United StatesThe hippocampus is thought to enable the encoding and retrieval of ongoing experience, the organization of that experience into structured representations like contexts, maps, and schemas, and the use of these structures to plan for the future. A central goal is to understand what the core computations supporting these functions are, and how these computations are realized in the collective action of single neurons. A potential access point into this issue is provided by ‘splitter cells’, hippocampal neurons that fire differentially on the overlapping segment of trajectories that differ in their past and/or future. However, the literature on splitter cells has been fragmented and confusing, owing to differences in terminology, behavioral tasks, and analysis methods across studies. In this review, we synthesize consistent findings from this literature, establish a common set of terms, and translate between single-cell and ensemble perspectives. Most importantly, we examine the combined findings through the lens of two major theoretical ideas about hippocampal function: representation of temporal context and latent state inference. We find that unique signature properties of each of these models are necessary to account for the data, but neither theory, by itself, explains all of its features. Specifically, the temporal gradedness of the splitter signal is strong support for temporal context, but is hard to explain using state models, while its flexibility and task-dependence is naturally accounted for using state inference, but poses a challenge otherwise. These theories suggest a number of avenues for future work, and we believe their application to splitter cells is a timely and informative domain for testing and refining theoretical ideas about hippocampal function.https://elifesciences.org/articles/82357place cellsstructure learninghippocampusstate spacesmemorytrajectory-dependent firing
spellingShingle Éléonore Duvelle
Roddy M Grieves
Matthijs AA van der Meer
Temporal context and latent state inference in the hippocampal splitter signal
eLife
place cells
structure learning
hippocampus
state spaces
memory
trajectory-dependent firing
title Temporal context and latent state inference in the hippocampal splitter signal
title_full Temporal context and latent state inference in the hippocampal splitter signal
title_fullStr Temporal context and latent state inference in the hippocampal splitter signal
title_full_unstemmed Temporal context and latent state inference in the hippocampal splitter signal
title_short Temporal context and latent state inference in the hippocampal splitter signal
title_sort temporal context and latent state inference in the hippocampal splitter signal
topic place cells
structure learning
hippocampus
state spaces
memory
trajectory-dependent firing
url https://elifesciences.org/articles/82357
work_keys_str_mv AT eleonoreduvelle temporalcontextandlatentstateinferenceinthehippocampalsplittersignal
AT roddymgrieves temporalcontextandlatentstateinferenceinthehippocampalsplittersignal
AT matthijsaavandermeer temporalcontextandlatentstateinferenceinthehippocampalsplittersignal