Evaluating hippocampal replay without a ground truth

Abstract
Data availability
Article and author information
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Abstract

During rest and sleep, memory traces replay in the brain. The dialogue between brain regions during replay is thought to stabilize labile memory traces for long-term storage. However, because replay is an internally-driven, spontaneous phenomenon, it does not have a ground truth - an external reference that can validate whether a memory has truly been replayed. Instead, replay detection is based on the similarity between the sequential neural activity comprising the replay event and the corresponding template of neural activity generated during active locomotion. If the statistical likelihood of observing such a match by chance is sufficiently low, the candidate replay event is inferred to be replaying that specific memory. However, without the ability to evaluate whether replay detection methods are successfully detecting true events and correctly rejecting non-events, the evaluation and comparison of different replay methods is challenging. To circumvent this problem, we present a new framework for evaluating replay, tested using hippocampal neural recordings from rats exploring two novel linear tracks. Using this two-track paradigm, our framework selects replay events based on their temporal fidelity (sequence-based detection), and evaluates the detection performance using each event's track discriminability, where sequenceless decoding across both tracks is used to quantify whether the track replaying is also the most likely track being reactivated.

Data availability

https://github.com/bendor-lab/replay_detection_cross_validation

The following previously published data sets were used

1. Tirole M
2. Huelin M
3. Takigawa M
4. Kukovska L
5. Bendor D
(2023) Experience-driven rate modulation is reinstated during hippocampal replay
Dryad Digital Repository, doi:10.5061/dryad.ksn02v76h.

https://doi.org/10.5061/dryad.ksn02v76h

Article and author information

Author details

Masahiro Takigawa

Institute of Behavioural Neuroscience, University College London, London, United Kingdom

For correspondence
Masahiro.takigawa.17@ucl.ac.uk

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-0162-9017
Marta Huelin Gorriz

Institute of Behavioural Neuroscience, University College London, London, United Kingdom

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-0281-0627
Margot Tirole

Institute of Behavioural Neuroscience, University College London, London, United Kingdom

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-0674-6690
Daniel Bendor

Institute of Behavioural Neuroscience, University College London, London, United Kingdom

For correspondence
d.bendor@ucl.ac.uk

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-6621-793X

Funding

Medical Research Council (Graduate student scholarship,MR/N013867/1)

Masahiro Takigawa

European Research Council (Starter Grant,CHIME)

Daniel Bendor

Human Frontier Science Program (Young Investigator Award,RGY0067/2016)

Daniel Bendor

Biotechnology and Biological Sciences Research Council (Research Grant,BB/T005475/1)

Daniel Bendor

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All experimental procedures and post-operative care were approved and carried out in accordance with the UK Home Office, subject to the restrictions and provisions contained within the Animal Scientific Procedures Act of 1986. Experiments were conducted under PPL P61EA6A72 (Bendor).

Copyright

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.