Disruption of awake sharp-wave ripples does not affect memorization of locations in repeated-acquisition spatial memory tasks

Abstract
Data availability
Article and author information
Metrics

Abstract

Storing and accessing memories is required to successfully perform day-to-day tasks, for example for engaging in a meaningful conversation. Previous studies in both rodents and primates have correlated hippocampal cellular activity with behavioral expression of memory. A key role has been attributed to awake hippocampal replay - a sequential reactivation of neurons representing a trajectory through space. However, it is unclear if awake replay impacts immediate future behavior, gradually creates and stabilizes long-term memories over a long period of time (hours and longer), or enables the temporary memorization of relevant events at an intermediate time scale (seconds to minutes). In this study, we aimed to address the uncertainty around the timeframe of impact of awake replay by collecting causal evidence from behaving rats. We detected and disrupted sharp wave ripples (SWRs) - signatures of putative replay events - using electrical stimulation of the ventral hippocampal commissure in rats that were trained on three different spatial memory tasks. In each task, rats were required to memorize a new set of locations in each trial or each daily session. Interestingly, the rats performed equally well with or without SWR disruptions. These data suggest that awake SWRs - and potentially replay - does not affect the immediate behavior nor the temporary memorization of relevant events at a short timescale that are required to successfully perform the spatial tasks. Based on these results we hypothesize that the impact of awake replay on memory and behavior is long-term and cumulative over time.

Data availability

Falcon software for closed-loop ripple detection and code for analysis are publicly available at http://www.bitbucket.org/kloostermannerflab. Source data are deposited in the following Figshare repository: https://figshare.com/s/4c0fcdad7e4890d7ba93.

The following data sets were generated

1. Lies Deceuninck
2. Fabian Kloosterman
(2022) Disruption of awake sharp-wave ripples have no effect on the immediate behavior nor create short-lasting memories
Figshare, 4c0fcdad7e4890d7ba93.

https://figshare.com/s/4c0fcdad7e4890d7ba93

Article and author information

Author details

Lies Deceuninck

Department of Physics and Astronomy, KU Leuven, Leuven, Belgium

For correspondence
lies.deceuninck@nerf.be

Competing interests
The authors declare that no competing interests exist.
Fabian Kloosterman

Faculty of Psychology and Educational Sciences, KU Leuven, Leuven, Belgium

For correspondence
kloosterman.fabian@gmail.com

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-6680-9660

Funding

Fonds Wetenschappelijk Onderzoek (PhD fellowship 11D9322N)

Lies Deceuninck

Fonds Wetenschappelijk Onderzoek (project grant G077321N)

Fabian Kloosterman

KU Leuven (grant C14/17/042)

Fabian Kloosterman

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 experiments were carried out in accordance with protocols approved by KU Leuven animal ethics committee (P119/2015 and P175/2020) and in accordance with the European Council Directive, 2010/63/EU.

Copyright

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