The spike-timing-dependent plasticity of VIP interneurons in motor cortex
The plasticity of inhibitory interneurons (INs) plays an important role in the organization and maintenance of cortical microcircuits. Given the many different IN types, there is an even greater diversity in synapse-type-specific plasticity learning rules at excitatory to excitatory (E→I), I→E, and...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2024-04-01
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| Series: | Frontiers in Cellular Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fncel.2024.1389094/full |
| _version_ | 1827277938798624768 |
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| author | Amanda R. McFarlan Amanda R. McFarlan Connie Guo Connie Guo Isabella Gomez Chaim Weinerman Tasha A. Liang P. Jesper Sjöström |
| author_facet | Amanda R. McFarlan Amanda R. McFarlan Connie Guo Connie Guo Isabella Gomez Chaim Weinerman Tasha A. Liang P. Jesper Sjöström |
| author_sort | Amanda R. McFarlan |
| collection | DOAJ |
| description | The plasticity of inhibitory interneurons (INs) plays an important role in the organization and maintenance of cortical microcircuits. Given the many different IN types, there is an even greater diversity in synapse-type-specific plasticity learning rules at excitatory to excitatory (E→I), I→E, and I→I synapses. I→I synapses play a key disinhibitory role in cortical circuits. Because they typically target other INs, vasoactive intestinal peptide (VIP) INs are often featured in I→I→E disinhibition, which upregulates activity in nearby excitatory neurons. VIP IN dysregulation may thus lead to neuropathologies such as epilepsy. In spite of the important activity regulatory role of VIP INs, their long-term plasticity has not been described. Therefore, we characterized the phenomenology of spike-timing-dependent plasticity (STDP) at inputs and outputs of genetically defined VIP INs. Using a combination of whole-cell recording, 2-photon microscopy, and optogenetics, we explored I→I STDP at layer 2/3 (L2/3) VIP IN outputs onto L5 Martinotti cells (MCs) and basket cells (BCs). We found that VIP IN→MC synapses underwent causal long-term depression (LTD) that was presynaptically expressed. VIP IN→BC connections, however, did not undergo any detectable plasticity. Conversely, using extracellular stimulation, we explored E→I STDP at inputs to VIP INs which revealed long-term potentiation (LTP) for both causal and acausal timings. Taken together, our results demonstrate that VIP INs possess synapse-type-specific learning rules at their inputs and outputs. This suggests the possibility of harnessing VIP IN long-term plasticity to control activity-related neuropathologies such as epilepsy. |
| first_indexed | 2024-04-24T07:44:44Z |
| format | Article |
| id | doaj.art-930c7419723f44d39e40bde5c0b521b1 |
| institution | Directory Open Access Journal |
| issn | 1662-5102 |
| language | English |
| last_indexed | 2024-04-24T07:44:44Z |
| publishDate | 2024-04-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cellular Neuroscience |
| spelling | doaj.art-930c7419723f44d39e40bde5c0b521b12024-04-19T04:24:40ZengFrontiers Media S.A.Frontiers in Cellular Neuroscience1662-51022024-04-011810.3389/fncel.2024.13890941389094The spike-timing-dependent plasticity of VIP interneurons in motor cortexAmanda R. McFarlan0Amanda R. McFarlan1Connie Guo2Connie Guo3Isabella Gomez4Chaim Weinerman5Tasha A. Liang6P. Jesper Sjöström7Centre for Research in Neuroscience, BRaIN Program, Department of Neurology and Neurosurgery, Research Institute of the McGill University Health Centre, Montreal General Hospital, Montreal, QC, CanadaIntegrated Program in Neuroscience, McGill University, Montreal, QC, CanadaCentre for Research in Neuroscience, BRaIN Program, Department of Neurology and Neurosurgery, Research Institute of the McGill University Health Centre, Montreal General Hospital, Montreal, QC, CanadaIntegrated Program in Neuroscience, McGill University, Montreal, QC, CanadaCentre for Research in Neuroscience, BRaIN Program, Department of Neurology and Neurosurgery, Research Institute of the McGill University Health Centre, Montreal General Hospital, Montreal, QC, CanadaCentre for Research in Neuroscience, BRaIN Program, Department of Neurology and Neurosurgery, Research Institute of the McGill University Health Centre, Montreal General Hospital, Montreal, QC, CanadaCentre for Research in Neuroscience, BRaIN Program, Department of Neurology and Neurosurgery, Research Institute of the McGill University Health Centre, Montreal General Hospital, Montreal, QC, CanadaCentre for Research in Neuroscience, BRaIN Program, Department of Neurology and Neurosurgery, Research Institute of the McGill University Health Centre, Montreal General Hospital, Montreal, QC, CanadaThe plasticity of inhibitory interneurons (INs) plays an important role in the organization and maintenance of cortical microcircuits. Given the many different IN types, there is an even greater diversity in synapse-type-specific plasticity learning rules at excitatory to excitatory (E→I), I→E, and I→I synapses. I→I synapses play a key disinhibitory role in cortical circuits. Because they typically target other INs, vasoactive intestinal peptide (VIP) INs are often featured in I→I→E disinhibition, which upregulates activity in nearby excitatory neurons. VIP IN dysregulation may thus lead to neuropathologies such as epilepsy. In spite of the important activity regulatory role of VIP INs, their long-term plasticity has not been described. Therefore, we characterized the phenomenology of spike-timing-dependent plasticity (STDP) at inputs and outputs of genetically defined VIP INs. Using a combination of whole-cell recording, 2-photon microscopy, and optogenetics, we explored I→I STDP at layer 2/3 (L2/3) VIP IN outputs onto L5 Martinotti cells (MCs) and basket cells (BCs). We found that VIP IN→MC synapses underwent causal long-term depression (LTD) that was presynaptically expressed. VIP IN→BC connections, however, did not undergo any detectable plasticity. Conversely, using extracellular stimulation, we explored E→I STDP at inputs to VIP INs which revealed long-term potentiation (LTP) for both causal and acausal timings. Taken together, our results demonstrate that VIP INs possess synapse-type-specific learning rules at their inputs and outputs. This suggests the possibility of harnessing VIP IN long-term plasticity to control activity-related neuropathologies such as epilepsy.https://www.frontiersin.org/articles/10.3389/fncel.2024.1389094/fullVIPinhibitory interneuronsplasticityspike-timing-dependent plasticitymotor cortex |
| spellingShingle | Amanda R. McFarlan Amanda R. McFarlan Connie Guo Connie Guo Isabella Gomez Chaim Weinerman Tasha A. Liang P. Jesper Sjöström The spike-timing-dependent plasticity of VIP interneurons in motor cortex Frontiers in Cellular Neuroscience VIP inhibitory interneurons plasticity spike-timing-dependent plasticity motor cortex |
| title | The spike-timing-dependent plasticity of VIP interneurons in motor cortex |
| title_full | The spike-timing-dependent plasticity of VIP interneurons in motor cortex |
| title_fullStr | The spike-timing-dependent plasticity of VIP interneurons in motor cortex |
| title_full_unstemmed | The spike-timing-dependent plasticity of VIP interneurons in motor cortex |
| title_short | The spike-timing-dependent plasticity of VIP interneurons in motor cortex |
| title_sort | spike timing dependent plasticity of vip interneurons in motor cortex |
| topic | VIP inhibitory interneurons plasticity spike-timing-dependent plasticity motor cortex |
| url | https://www.frontiersin.org/articles/10.3389/fncel.2024.1389094/full |
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