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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| 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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| _version_ | 1846169481382985728 | 
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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. | 
| format | Article | 
| id | doaj-art-5b8caa43a723446a96e2f2ef4c86c52d | 
| institution | Kabale University | 
| issn | 2046-2441 | 
| language | English | 
| publishDate | 2024-11-01 | 
| publisher | The Royal Society | 
| record_format | Article | 
| 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 | 
| work_keys_str_mv | AT nishitabhembre learninginducedremodellingofinhibitorysynapsesinthemotorcortex AT annalisapaolino learninginducedremodellingofinhibitorysynapsesinthemotorcortex AT soorajsdas learninginducedremodellingofinhibitorysynapsesinthemotorcortex AT sumasriguntupalli learninginducedremodellingofinhibitorysynapsesinthemotorcortex AT laurarfenlon learninginducedremodellingofinhibitorysynapsesinthemotorcortex AT victoranggono learninginducedremodellingofinhibitorysynapsesinthemotorcortex | 
 
       