Learning-induced remodelling of inhibitory synapses in the motor cortex

Robust structural and functional plasticity occurs at excitatory synapses in the motor cortex in response to learning. It is well established that local spinogenesis and the subsequent maintenance of newly formed spines are crucial for motor learning. However, despite local synaptic inhibition being...

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Main Authors: Nishita Bhembre, Annalisa Paolino, Sooraj S. Das, Sumasri Guntupalli, Laura R. Fenlon, Victor Anggono
Format: Article
Language:English
Published: The Royal Society 2024-11-01
Series:Open Biology
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Online Access:https://royalsocietypublishing.org/doi/10.1098/rsob.240109
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author Nishita Bhembre
Annalisa Paolino
Sooraj S. Das
Sumasri Guntupalli
Laura R. Fenlon
Victor Anggono
author_facet Nishita Bhembre
Annalisa Paolino
Sooraj S. Das
Sumasri Guntupalli
Laura R. Fenlon
Victor Anggono
author_sort Nishita Bhembre
collection DOAJ
description Robust structural and functional plasticity occurs at excitatory synapses in the motor cortex in response to learning. It is well established that local spinogenesis and the subsequent maintenance of newly formed spines are crucial for motor learning. However, despite local synaptic inhibition being essential for shaping excitatory synaptic input, less is known about the structural rearrangement of inhibitory synapses following learning. In this study, we co-expressed the structural marker tdTomato and a mEmerald-tagged intrabody against gephyrin to visualize inhibitory synapses in layer 2/3 cortical neurons of wild-type CD1 mice. We found that a 1-day accelerated rotarod paradigm induced robust motor learning in male and female adult CD1 mice. Histological analyses revealed a significant increase in the surface area of gephyrin puncta in neurons within the motor cortex but not in the somatosensory cortex upon motor learning. Furthermore, this learning-induced reorganization of inhibitory synapses only occurred in dendritic shafts and not in the spines. These data suggest that learning induces experience-dependent remodelling of existing inhibitory synapses to fine-tune intrinsic plasticity and input-specific modulation of excitatory connections in the motor cortex.
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institution Kabale University
issn 2046-2441
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publishDate 2024-11-01
publisher The Royal Society
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series Open Biology
spelling doaj-art-5b8caa43a723446a96e2f2ef4c86c52d2024-11-13T00:05:27ZengThe Royal SocietyOpen Biology2046-24412024-11-01141110.1098/rsob.240109Learning-induced remodelling of inhibitory synapses in the motor cortexNishita Bhembre0Annalisa Paolino1Sooraj S. Das2Sumasri Guntupalli3Laura R. Fenlon4Victor Anggono5Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, University of Queensland, Brisbane, Queensland 4072, AustraliaClem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, University of Queensland, Brisbane, Queensland 4072, AustraliaClem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, University of Queensland, Brisbane, Queensland 4072, AustraliaClem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, University of Queensland, Brisbane, Queensland 4072, AustraliaSchool of Biomedical Sciences, Faculty of Medicine, University of Queensland, Brisbane, Queensland 4072, AustraliaClem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, University of Queensland, Brisbane, Queensland 4072, AustraliaRobust structural and functional plasticity occurs at excitatory synapses in the motor cortex in response to learning. It is well established that local spinogenesis and the subsequent maintenance of newly formed spines are crucial for motor learning. However, despite local synaptic inhibition being essential for shaping excitatory synaptic input, less is known about the structural rearrangement of inhibitory synapses following learning. In this study, we co-expressed the structural marker tdTomato and a mEmerald-tagged intrabody against gephyrin to visualize inhibitory synapses in layer 2/3 cortical neurons of wild-type CD1 mice. We found that a 1-day accelerated rotarod paradigm induced robust motor learning in male and female adult CD1 mice. Histological analyses revealed a significant increase in the surface area of gephyrin puncta in neurons within the motor cortex but not in the somatosensory cortex upon motor learning. Furthermore, this learning-induced reorganization of inhibitory synapses only occurred in dendritic shafts and not in the spines. These data suggest that learning induces experience-dependent remodelling of existing inhibitory synapses to fine-tune intrinsic plasticity and input-specific modulation of excitatory connections in the motor cortex.https://royalsocietypublishing.org/doi/10.1098/rsob.240109learningplasticityinhibitionpostsynaptic densitygephyrin
spellingShingle Nishita Bhembre
Annalisa Paolino
Sooraj S. Das
Sumasri Guntupalli
Laura R. Fenlon
Victor Anggono
Learning-induced remodelling of inhibitory synapses in the motor cortex
Open Biology
learning
plasticity
inhibition
postsynaptic density
gephyrin
title Learning-induced remodelling of inhibitory synapses in the motor cortex
title_full Learning-induced remodelling of inhibitory synapses in the motor cortex
title_fullStr Learning-induced remodelling of inhibitory synapses in the motor cortex
title_full_unstemmed Learning-induced remodelling of inhibitory synapses in the motor cortex
title_short Learning-induced remodelling of inhibitory synapses in the motor cortex
title_sort learning induced remodelling of inhibitory synapses in the motor cortex
topic learning
plasticity
inhibition
postsynaptic density
gephyrin
url https://royalsocietypublishing.org/doi/10.1098/rsob.240109
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