Theta and gamma oscillations in the rat hippocampus support the discrimination of object displacement in a recognition memory task

Episodic memory depends on the recollection of spatial and temporal aspects of past experiences in which the hippocampus plays a critical role. Studies on hippocampal lesions in rodents have shown that dentate gyrus (DG) and CA3 are necessary to detect object displacement in memory tasks. However, t...

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Main Authors: Lívia Neves, Bruno Lobão-Soares, Ana Paula de Castro Araujo, Alan Michel Bezerra Furtunato, Izabela Paiva, Nicholy Souza, Anne Kelly Morais, George Nascimento, Elaine Gavioli, Adriano Bretanha Lopes Tort, Flávio Freitas Barbosa, Hindiael Belchior
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-12-01
Series:Frontiers in Behavioral Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnbeh.2022.970083/full
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author Lívia Neves
Bruno Lobão-Soares
Bruno Lobão-Soares
Ana Paula de Castro Araujo
Ana Paula de Castro Araujo
Alan Michel Bezerra Furtunato
Izabela Paiva
Nicholy Souza
Anne Kelly Morais
George Nascimento
Elaine Gavioli
Elaine Gavioli
Adriano Bretanha Lopes Tort
Flávio Freitas Barbosa
Flávio Freitas Barbosa
Hindiael Belchior
Hindiael Belchior
author_facet Lívia Neves
Bruno Lobão-Soares
Bruno Lobão-Soares
Ana Paula de Castro Araujo
Ana Paula de Castro Araujo
Alan Michel Bezerra Furtunato
Izabela Paiva
Nicholy Souza
Anne Kelly Morais
George Nascimento
Elaine Gavioli
Elaine Gavioli
Adriano Bretanha Lopes Tort
Flávio Freitas Barbosa
Flávio Freitas Barbosa
Hindiael Belchior
Hindiael Belchior
author_sort Lívia Neves
collection DOAJ
description Episodic memory depends on the recollection of spatial and temporal aspects of past experiences in which the hippocampus plays a critical role. Studies on hippocampal lesions in rodents have shown that dentate gyrus (DG) and CA3 are necessary to detect object displacement in memory tasks. However, the understanding of real-time oscillatory activity underlying memory discrimination of subtle and pronounced displacements remains elusive. Here, we chronically implanted microelectrode arrays in adult male Wistar rats to record network oscillations from DG, CA3, and CA1 of the dorsal hippocampus while animals executed an object recognition task of high and low spatial displacement tests (HD: 108 cm, and LD: 54 cm, respectively). Behavioral analysis showed that the animals discriminate between stationary and displaced objects in the HD but not LD conditions. To investigate the hypothesis that theta and gamma oscillations in different areas of the hippocampus support discrimination processes in a recognition memory task, we compared epochs of object exploration between HD and LD conditions as well as displaced and stationary objects. We observed that object exploration epochs were accompanied by strong rhythmic activity in the theta frequency (6–12 Hz) band in the three hippocampal areas. Comparison between test conditions revealed higher theta band power and higher theta-gamma phase-amplitude coupling in the DG during HD than LD conditions. Similarly, direct comparison between displaced and stationary objects within the HD test showed higher theta band power in CA3 during exploration of displaced objects. Moreover, the discrimination index between displaced and stationary objects directly correlated with CA1 gamma band power in epochs of object exploration. We thus conclude that theta and gamma oscillations in the dorsal hippocampus support the successful discrimination of object displacement in a recognition memory task.
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spelling doaj.art-a849d1961d9e4a5c8c12f68eb8ddc5b02022-12-22T03:54:48ZengFrontiers Media S.A.Frontiers in Behavioral Neuroscience1662-51532022-12-011610.3389/fnbeh.2022.970083970083Theta and gamma oscillations in the rat hippocampus support the discrimination of object displacement in a recognition memory taskLívia Neves0Bruno Lobão-Soares1Bruno Lobão-Soares2Ana Paula de Castro Araujo3Ana Paula de Castro Araujo4Alan Michel Bezerra Furtunato5Izabela Paiva6Nicholy Souza7Anne Kelly Morais8George Nascimento9Elaine Gavioli10Elaine Gavioli11Adriano Bretanha Lopes Tort12Flávio Freitas Barbosa13Flávio Freitas Barbosa14Hindiael Belchior15Hindiael Belchior16Graduate Program in Psychobiology, Federal University of Rio Grande do Norte, Natal, RN, BrazilGraduate Program in Psychobiology, Federal University of Rio Grande do Norte, Natal, RN, BrazilDepartment of Biophysics and Pharmacology, Federal University of Rio Grande do Norte, Natal, RN, BrazilGraduate Program in Cognitive Neuroscience and Behavior, Federal University of Paraíba, João Pessoa, PB, BrazilDepartment of Psychology, Federal University of Paraíba, João Pessoa, PB, BrazilGraduate Program in Psychobiology, Federal University of Rio Grande do Norte, Natal, RN, BrazilBrain Institute, Federal University of Rio Grande do Norte, Natal, RN, BrazilGraduate Program in Psychobiology, Federal University of Rio Grande do Norte, Natal, RN, BrazilGraduate Program in Psychobiology, Federal University of Rio Grande do Norte, Natal, RN, BrazilDepartment of Biomedical Engineering, Federal University of Rio Grande do Norte, Natal, RN, BrazilGraduate Program in Psychobiology, Federal University of Rio Grande do Norte, Natal, RN, BrazilDepartment of Biophysics and Pharmacology, Federal University of Rio Grande do Norte, Natal, RN, BrazilBrain Institute, Federal University of Rio Grande do Norte, Natal, RN, BrazilGraduate Program in Cognitive Neuroscience and Behavior, Federal University of Paraíba, João Pessoa, PB, BrazilDepartment of Psychology, Federal University of Paraíba, João Pessoa, PB, BrazilGraduate Program in Psychobiology, Federal University of Rio Grande do Norte, Natal, RN, BrazilDepartment of Physical Education, Federal University of Rio Grande do Norte, Natal, RN, BrazilEpisodic memory depends on the recollection of spatial and temporal aspects of past experiences in which the hippocampus plays a critical role. Studies on hippocampal lesions in rodents have shown that dentate gyrus (DG) and CA3 are necessary to detect object displacement in memory tasks. However, the understanding of real-time oscillatory activity underlying memory discrimination of subtle and pronounced displacements remains elusive. Here, we chronically implanted microelectrode arrays in adult male Wistar rats to record network oscillations from DG, CA3, and CA1 of the dorsal hippocampus while animals executed an object recognition task of high and low spatial displacement tests (HD: 108 cm, and LD: 54 cm, respectively). Behavioral analysis showed that the animals discriminate between stationary and displaced objects in the HD but not LD conditions. To investigate the hypothesis that theta and gamma oscillations in different areas of the hippocampus support discrimination processes in a recognition memory task, we compared epochs of object exploration between HD and LD conditions as well as displaced and stationary objects. We observed that object exploration epochs were accompanied by strong rhythmic activity in the theta frequency (6–12 Hz) band in the three hippocampal areas. Comparison between test conditions revealed higher theta band power and higher theta-gamma phase-amplitude coupling in the DG during HD than LD conditions. Similarly, direct comparison between displaced and stationary objects within the HD test showed higher theta band power in CA3 during exploration of displaced objects. Moreover, the discrimination index between displaced and stationary objects directly correlated with CA1 gamma band power in epochs of object exploration. We thus conclude that theta and gamma oscillations in the dorsal hippocampus support the successful discrimination of object displacement in a recognition memory task.https://www.frontiersin.org/articles/10.3389/fnbeh.2022.970083/fullhippocampuslocal field potentialsrecognition memoryspatial displacement of objectspattern separation
spellingShingle Lívia Neves
Bruno Lobão-Soares
Bruno Lobão-Soares
Ana Paula de Castro Araujo
Ana Paula de Castro Araujo
Alan Michel Bezerra Furtunato
Izabela Paiva
Nicholy Souza
Anne Kelly Morais
George Nascimento
Elaine Gavioli
Elaine Gavioli
Adriano Bretanha Lopes Tort
Flávio Freitas Barbosa
Flávio Freitas Barbosa
Hindiael Belchior
Hindiael Belchior
Theta and gamma oscillations in the rat hippocampus support the discrimination of object displacement in a recognition memory task
Frontiers in Behavioral Neuroscience
hippocampus
local field potentials
recognition memory
spatial displacement of objects
pattern separation
title Theta and gamma oscillations in the rat hippocampus support the discrimination of object displacement in a recognition memory task
title_full Theta and gamma oscillations in the rat hippocampus support the discrimination of object displacement in a recognition memory task
title_fullStr Theta and gamma oscillations in the rat hippocampus support the discrimination of object displacement in a recognition memory task
title_full_unstemmed Theta and gamma oscillations in the rat hippocampus support the discrimination of object displacement in a recognition memory task
title_short Theta and gamma oscillations in the rat hippocampus support the discrimination of object displacement in a recognition memory task
title_sort theta and gamma oscillations in the rat hippocampus support the discrimination of object displacement in a recognition memory task
topic hippocampus
local field potentials
recognition memory
spatial displacement of objects
pattern separation
url https://www.frontiersin.org/articles/10.3389/fnbeh.2022.970083/full
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