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A whole-brain analysis of functional connectivity and immediate early gene expression reveals functional network shifts after operant learning

https://oist.repo.nii.ac.jp/records/2000778
https://oist.repo.nii.ac.jp/records/2000778
74efc855-3efc-4465-bf78-ad6948059125
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1-s2.0-S1053811924003379-main.pdf 1-s2.0-S1053811924003379-main.pdf (4.7 MB)
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Item type 学術雑誌論文 / Journal Article(1)
PubDate 2025-02-26
Title
Title A whole-brain analysis of functional connectivity and immediate early gene expression reveals functional network shifts after operant learning
Language en
Language
Language eng
Keyword
Language en
Subject Scheme Other
Subject Functional connectivity | Early growth response 1 | Plasticity | Operant training | Immediate early gene
Resource Type
Resource Type Identifier http://purl.org/coar/resource_type/c_6501
Resource Type journal article
Access Right
Access Rights open access
Access Rights URI http://purl.org/coar/access_right/c_abf2
Author Kasahara, Kazumi

× Kasahara, Kazumi

en Kasahara, Kazumi

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Hikishima, Keigo

× Hikishima, Keigo

en Hikishima, Keigo

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Nakata, Mariko

× Nakata, Mariko

en Nakata, Mariko

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Tsurugizawa, Tomokazu

× Tsurugizawa, Tomokazu

en Tsurugizawa, Tomokazu

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Higo, Noriyuki

× Higo, Noriyuki

en Higo, Noriyuki

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Doya, Kenji

× Doya, Kenji

en Doya, Kenji

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Bibliographic Information en : NeuroImage

Volume Number 299, p. 120840, Issue Date 2024-09-10
Abstract
Description Type Abstract
Description Previous studies of operant learning have addressed neuronal activities and network changes in specific brain areas, such as the striatum, sensorimotor cortex, prefrontal/orbitofrontal cortices, and hippocampus. However, how changes in the whole-brain network are caused by cellular-level changes remains unclear. We, therefore, combined resting-state functional magnetic resonance imaging (rsfMRI) and whole-brain immunohistochemical analysis of early growth response 1 (EGR1), a marker of neural plasticity, to elucidate the temporal and spatial changes in functional networks and underlying cellular processes during operant learning. We used an 11.7-Tesla MRI scanner and whole-brain immunohistochemical analysis of EGR1 in mice during the early and late stages of operant learning. In the operant training, mice received a reward when they pressed left and right buttons alternately, and were punished with a bright light when they made a mistake. A group of mice (n = 22) underwent the first rsfMRI acquisition before behavioral sessions, the second acquisition after 3 training-session-days (early stage), and the third after 21 training-session-days (late stage). Another group of mice (n = 40) was subjected to histological analysis 15 min after the early or late stages of behavioral sessions. Functional connectivity increased between the limbic areas and thalamus or auditory cortex after the early stage of training, and between the motor cortex, sensory cortex, and striatum after the late stage of training. The density of EGR1-immunopositive cells in the motor and sensory cortices increased in both the early and late stages of training, whereas the density in the amygdala increased only in the early stage of training. The subcortical networks centered around the limbic areas that emerged in the early stage have been implicated in rewards, pleasures, and fears. The connectivities between the motor cortex, somatosensory cortex, and striatum that consolidated in the late stage have been implicated in motor learning. Our multimodal longitudinal study successfully revealed temporal shifts in brain regions involved in behavioral learning together with the underlying cellular-level plasticity between these regions. Our study represents a first step towards establishing a new experimental paradigm that combines rsfMRI and immunohistochemistry to link macroscopic and microscopic mechanisms involved in learning.
Language en
Publisher
Publisher Elsevier Inc.
ISSN
Source Identifier Type PISSN
Source Identifier 1053-8119
ISSN
Source Identifier Type EISSN
Source Identifier 1095-9572
PubMedNo.
Relation Type isIdenticalTo
Identifier Type PMID
Related Identifier 39241900
item_10001_relation_14
Relation Type isIdenticalTo
Identifier Type DOI
Related Identifier 10.1016/j.neuroimage.2024.120840
Rights
Rights © 2024 The Authors.
Rights
Rights Resource https://creativecommons.org/licenses/by-nc-nd/4.0/
Rights Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International
Related site
Relation Type isIdenticalTo
Identifier Type URI
Related Identifier https://www.sciencedirect.com/science/article/pii/S1053811924003379
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Version Type VoR
Version Type Resource http://purl.org/coar/version/c_970fb48d4fbd8a85
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