Transient DREADD Manipulation of the Dorsal Dentate Gyrus in Rats Impairs Initial Learning of Place‐Outcome Associations

ABSTRACT The dentate gyrus subfield of the hippocampus is thought to be critically involved in the disambiguation of similar episodic experiences and places in a context‐dependent manner. However, most empirical evidence has come from lesion and gene knock‐out studies in rodents, in which the dentat...

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Vydáno v:Hippocampus Ročník 35; číslo 3; s. e70014 - n/a
Hlavní autoři: Lim, J., Souiki, A., Ahmad, P., Oomen, C. A., Huis in ’t Veld, G. J., Lansink, C. S., Pennartz, C. M. A., Olcese, U.
Médium: Journal Article
Jazyk:angličtina
Vydáno: Hoboken, USA John Wiley & Sons, Inc 01.05.2025
Wiley Subscription Services, Inc
Témata:
Animals
Association Learning - drug effects
Association Learning - physiology
Dentate gyrus
Dentate Gyrus - drug effects
Dentate Gyrus - physiology
Discrimination Learning - drug effects
Discrimination Learning - physiology
DREADDs
episodic memory
hippocampus
Learning
Male
place‐reward associations
Rats
Rats, Long-Evans
Reinforcement
Reward
episodic memory
place‐reward associations
DREADDs
dentate gyrus
rats
hippocampus
ISSN:1050-9631, 1098-1063, 1098-1063
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Abstract ABSTRACT The dentate gyrus subfield of the hippocampus is thought to be critically involved in the disambiguation of similar episodic experiences and places in a context‐dependent manner. However, most empirical evidence has come from lesion and gene knock‐out studies in rodents, in which the dentate gyrus is permanently perturbed and compensation of affected functions via other areas within the memory circuit could take place. The acute and causal role of the dentate gyrus herein remains therefore elusive. The present study aimed to investigate the acute role of the dorsal dentate gyrus in disambiguation learning using reversible inhibitory DREADDs. Rats were trained on a location discrimination task and learned to discriminate between a rewarded and unrewarded location with either small (similar condition) or large (dissimilar condition) separation. Reward contingencies switched after applying a reversal rule, allowing us to track the temporal engagement of the dentate gyrus during the task. Bilateral DREADD modulation of the dentate gyrus impaired the initial acquisition learning of place‐reward associations, but performance rapidly recovered to baseline levels within the same session. Modeling of the behavioral patterns revealed that reward sensitivity and alternation behavior were temporally associated with the DG‐dependent impairment during acquisition learning. Our study thus provides novel evidence that the dorsal dentate gyrus is acutely engaged during the initial acquisition learning of place‐reward associations.
AbstractList The dentate gyrus subfield of the hippocampus is thought to be critically involved in the disambiguation of similar episodic experiences and places in a context‐dependent manner. However, most empirical evidence has come from lesion and gene knock‐out studies in rodents, in which the dentate gyrus is permanently perturbed and compensation of affected functions via other areas within the memory circuit could take place. The acute and causal role of the dentate gyrus herein remains therefore elusive. The present study aimed to investigate the acute role of the dorsal dentate gyrus in disambiguation learning using reversible inhibitory DREADDs. Rats were trained on a location discrimination task and learned to discriminate between a rewarded and unrewarded location with either small (similar condition) or large (dissimilar condition) separation. Reward contingencies switched after applying a reversal rule, allowing us to track the temporal engagement of the dentate gyrus during the task. Bilateral DREADD modulation of the dentate gyrus impaired the initial acquisition learning of place‐reward associations, but performance rapidly recovered to baseline levels within the same session. Modeling of the behavioral patterns revealed that reward sensitivity and alternation behavior were temporally associated with the DG‐dependent impairment during acquisition learning. Our study thus provides novel evidence that the dorsal dentate gyrus is acutely engaged during the initial acquisition learning of place‐reward associations.
ABSTRACT The dentate gyrus subfield of the hippocampus is thought to be critically involved in the disambiguation of similar episodic experiences and places in a context‐dependent manner. However, most empirical evidence has come from lesion and gene knock‐out studies in rodents, in which the dentate gyrus is permanently perturbed and compensation of affected functions via other areas within the memory circuit could take place. The acute and causal role of the dentate gyrus herein remains therefore elusive. The present study aimed to investigate the acute role of the dorsal dentate gyrus in disambiguation learning using reversible inhibitory DREADDs. Rats were trained on a location discrimination task and learned to discriminate between a rewarded and unrewarded location with either small (similar condition) or large (dissimilar condition) separation. Reward contingencies switched after applying a reversal rule, allowing us to track the temporal engagement of the dentate gyrus during the task. Bilateral DREADD modulation of the dentate gyrus impaired the initial acquisition learning of place‐reward associations, but performance rapidly recovered to baseline levels within the same session. Modeling of the behavioral patterns revealed that reward sensitivity and alternation behavior were temporally associated with the DG‐dependent impairment during acquisition learning. Our study thus provides novel evidence that the dorsal dentate gyrus is acutely engaged during the initial acquisition learning of place‐reward associations.
The dentate gyrus subfield of the hippocampus is thought to be critically involved in the disambiguation of similar episodic experiences and places in a context-dependent manner. However, most empirical evidence has come from lesion and gene knock-out studies in rodents, in which the dentate gyrus is permanently perturbed and compensation of affected functions via other areas within the memory circuit could take place. The acute and causal role of the dentate gyrus herein remains therefore elusive. The present study aimed to investigate the acute role of the dorsal dentate gyrus in disambiguation learning using reversible inhibitory DREADDs. Rats were trained on a location discrimination task and learned to discriminate between a rewarded and unrewarded location with either small (similar condition) or large (dissimilar condition) separation. Reward contingencies switched after applying a reversal rule, allowing us to track the temporal engagement of the dentate gyrus during the task. Bilateral DREADD modulation of the dentate gyrus impaired the initial acquisition learning of place-reward associations, but performance rapidly recovered to baseline levels within the same session. Modeling of the behavioral patterns revealed that reward sensitivity and alternation behavior were temporally associated with the DG-dependent impairment during acquisition learning. Our study thus provides novel evidence that the dorsal dentate gyrus is acutely engaged during the initial acquisition learning of place-reward associations.The dentate gyrus subfield of the hippocampus is thought to be critically involved in the disambiguation of similar episodic experiences and places in a context-dependent manner. However, most empirical evidence has come from lesion and gene knock-out studies in rodents, in which the dentate gyrus is permanently perturbed and compensation of affected functions via other areas within the memory circuit could take place. The acute and causal role of the dentate gyrus herein remains therefore elusive. The present study aimed to investigate the acute role of the dorsal dentate gyrus in disambiguation learning using reversible inhibitory DREADDs. Rats were trained on a location discrimination task and learned to discriminate between a rewarded and unrewarded location with either small (similar condition) or large (dissimilar condition) separation. Reward contingencies switched after applying a reversal rule, allowing us to track the temporal engagement of the dentate gyrus during the task. Bilateral DREADD modulation of the dentate gyrus impaired the initial acquisition learning of place-reward associations, but performance rapidly recovered to baseline levels within the same session. Modeling of the behavioral patterns revealed that reward sensitivity and alternation behavior were temporally associated with the DG-dependent impairment during acquisition learning. Our study thus provides novel evidence that the dorsal dentate gyrus is acutely engaged during the initial acquisition learning of place-reward associations.
Author Huis in ’t Veld, G. J.
Pennartz, C. M. A.
Lim, J.
Ahmad, P.
Lansink, C. S.
Souiki, A.
Oomen, C. A.
Olcese, U.
AuthorAffiliation 1 Cognitive and Systems Neuroscience Group Swammerdam Institute for Life Sciences, University of Amsterdam Amsterdam the Netherlands
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Issue 3
Keywords episodic memory
place‐reward associations
DREADDs
dentate gyrus
rats
hippocampus
Language English
License Attribution
2025 The Author(s). Hippocampus published by Wiley Periodicals LLC.
This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
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Notes Funding
A. Souiki and P. Ahmad are contributed equally to this work.
This work was supported by ZonMw and Amsterdam Neuroscience.
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Snippet ABSTRACT The dentate gyrus subfield of the hippocampus is thought to be critically involved in the disambiguation of similar episodic experiences and places in...
The dentate gyrus subfield of the hippocampus is thought to be critically involved in the disambiguation of similar episodic experiences and places in a...
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StartPage e70014
SubjectTerms Animals
Association Learning - drug effects
Association Learning - physiology
Dentate gyrus
Dentate Gyrus - drug effects
Dentate Gyrus - physiology
Discrimination Learning - drug effects
Discrimination Learning - physiology
DREADDs
episodic memory
hippocampus
Learning
Male
place‐reward associations
Rats
Rats, Long-Evans
Reinforcement
Reward
Title Transient DREADD Manipulation of the Dorsal Dentate Gyrus in Rats Impairs Initial Learning of Place‐Outcome Associations
URI https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fhipo.70014
https://www.ncbi.nlm.nih.gov/pubmed/40326013
https://www.proquest.com/docview/3228938684
https://www.proquest.com/docview/3200816261
https://pubmed.ncbi.nlm.nih.gov/PMC12053149
Volume 35
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