Experience shapes chandelier cell function and structure in the visual cortex
Detailed characterization of interneuron types in primary visual cortex (V1) has greatly contributed to understanding visual perception, yet the role of chandelier cells (ChCs) in visual processing remains poorly characterized. Using viral tracing we found that V1 ChCs predominantly receive monosyna...
| Main Authors: | , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2024-01-01
|
| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/91153 |
| _version_ | 1827309022574804992 |
|---|---|
| author | Koen Seignette Nora Jamann Paolo Papale Huub Terra Ralph O Porneso Leander de Kraker Chris van der Togt Maaike van der Aa Paul Neering Emma Ruimschotel Pieter R Roelfsema Jorrit S Montijn Matthew W Self Maarten HP Kole Christiaan N Levelt |
| author_facet | Koen Seignette Nora Jamann Paolo Papale Huub Terra Ralph O Porneso Leander de Kraker Chris van der Togt Maaike van der Aa Paul Neering Emma Ruimschotel Pieter R Roelfsema Jorrit S Montijn Matthew W Self Maarten HP Kole Christiaan N Levelt |
| author_sort | Koen Seignette |
| collection | DOAJ |
| description | Detailed characterization of interneuron types in primary visual cortex (V1) has greatly contributed to understanding visual perception, yet the role of chandelier cells (ChCs) in visual processing remains poorly characterized. Using viral tracing we found that V1 ChCs predominantly receive monosynaptic input from local layer 5 pyramidal cells and higher-order cortical regions. Two-photon calcium imaging and convolutional neural network modeling revealed that ChCs are visually responsive but weakly selective for stimulus content. In mice running in a virtual tunnel, ChCs respond strongly to events known to elicit arousal, including locomotion and visuomotor mismatch. Repeated exposure of the mice to the virtual tunnel was accompanied by reduced visual responses of ChCs and structural plasticity of ChC boutons and axon initial segment length. Finally, ChCs only weakly inhibited pyramidal cells. These findings suggest that ChCs provide an arousal-related signal to layer 2/3 pyramidal cells that may modulate their activity and/or gate plasticity of their axon initial segments during behaviorally relevant events. |
| first_indexed | 2024-03-08T15:49:52Z |
| format | Article |
| id | doaj.art-7d6f60c30957421c817c55ef04f49efd |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-24T19:24:20Z |
| publishDate | 2024-01-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-7d6f60c30957421c817c55ef04f49efd2024-03-25T16:24:53ZengeLife Sciences Publications LtdeLife2050-084X2024-01-011210.7554/eLife.91153Experience shapes chandelier cell function and structure in the visual cortexKoen Seignette0https://orcid.org/0000-0002-7398-6291Nora Jamann1Paolo Papale2https://orcid.org/0000-0002-6249-841XHuub Terra3Ralph O Porneso4https://orcid.org/0009-0005-9659-525XLeander de Kraker5Chris van der Togt6Maaike van der Aa7Paul Neering8Emma Ruimschotel9Pieter R Roelfsema10https://orcid.org/0000-0002-1625-0034Jorrit S Montijn11Matthew W Self12https://orcid.org/0000-0001-5731-579XMaarten HP Kole13https://orcid.org/0000-0002-3883-5682Christiaan N Levelt14https://orcid.org/0000-0002-1813-6243Department of Molecular Visual Plasticity, Netherlands Institute for Neuroscience, Amsterdam, NetherlandsDepartment of Axonal Signaling, Netherlands Institute for Neuroscience, Amsterdam, Netherlands; Department of Biology Cell Biology, Neurobiology and Biophysics, Faculty of Science, Utrecht University, Utrecht, NetherlandsDepartment of Vision & Cognition, Netherlands Institute for Neuroscience, Amsterdam, NetherlandsDepartment of Molecular Visual Plasticity, Netherlands Institute for Neuroscience, Amsterdam, NetherlandsDepartment of Molecular Visual Plasticity, Netherlands Institute for Neuroscience, Amsterdam, NetherlandsDepartment of Molecular Visual Plasticity, Netherlands Institute for Neuroscience, Amsterdam, NetherlandsDepartment of Molecular Visual Plasticity, Netherlands Institute for Neuroscience, Amsterdam, Netherlands; Department of Vision & Cognition, Netherlands Institute for Neuroscience, Amsterdam, NetherlandsDepartment of Molecular Visual Plasticity, Netherlands Institute for Neuroscience, Amsterdam, NetherlandsDepartment of Molecular Visual Plasticity, Netherlands Institute for Neuroscience, Amsterdam, Netherlands; Department of Vision & Cognition, Netherlands Institute for Neuroscience, Amsterdam, NetherlandsDepartment of Molecular Visual Plasticity, Netherlands Institute for Neuroscience, Amsterdam, NetherlandsDepartment of Vision & Cognition, Netherlands Institute for Neuroscience, Amsterdam, Netherlands; Laboratory of Visual Brain Therapy, Sorbonne Université, Institut National de la Santé et de la Recherche Médicale, Centre National de la Recherche Scientifique, Institut de la Vision, Paris, France; Department of Integrative Neurophysiology, Centre for Neurogenomics and Cognitive Research, VU University, Amsterdam, Netherlands; Department of Psychiatry, Academic Medical Center, University of Amsterdam, Amsterdam, NetherlandsDepartment of Cortical Structure & Function, Netherlands Institute for Neuroscience, Amsterdam, NetherlandsDepartment of Vision & Cognition, Netherlands Institute for Neuroscience, Amsterdam, NetherlandsDepartment of Axonal Signaling, Netherlands Institute for Neuroscience, Amsterdam, Netherlands; Department of Biology Cell Biology, Neurobiology and Biophysics, Faculty of Science, Utrecht University, Utrecht, NetherlandsDepartment of Molecular Visual Plasticity, Netherlands Institute for Neuroscience, Amsterdam, Netherlands; Department of Molecular and Cellular Neurobiology, Center for Neurogenomics and Cognitive Research, VU University Amsterdam, Amsterdam, NetherlandsDetailed characterization of interneuron types in primary visual cortex (V1) has greatly contributed to understanding visual perception, yet the role of chandelier cells (ChCs) in visual processing remains poorly characterized. Using viral tracing we found that V1 ChCs predominantly receive monosynaptic input from local layer 5 pyramidal cells and higher-order cortical regions. Two-photon calcium imaging and convolutional neural network modeling revealed that ChCs are visually responsive but weakly selective for stimulus content. In mice running in a virtual tunnel, ChCs respond strongly to events known to elicit arousal, including locomotion and visuomotor mismatch. Repeated exposure of the mice to the virtual tunnel was accompanied by reduced visual responses of ChCs and structural plasticity of ChC boutons and axon initial segment length. Finally, ChCs only weakly inhibited pyramidal cells. These findings suggest that ChCs provide an arousal-related signal to layer 2/3 pyramidal cells that may modulate their activity and/or gate plasticity of their axon initial segments during behaviorally relevant events.https://elifesciences.org/articles/91153axo-axonicprediction errorchandelierinhibititionarousalmost exciting input |
| spellingShingle | Koen Seignette Nora Jamann Paolo Papale Huub Terra Ralph O Porneso Leander de Kraker Chris van der Togt Maaike van der Aa Paul Neering Emma Ruimschotel Pieter R Roelfsema Jorrit S Montijn Matthew W Self Maarten HP Kole Christiaan N Levelt Experience shapes chandelier cell function and structure in the visual cortex eLife axo-axonic prediction error chandelier inhibitition arousal most exciting input |
| title | Experience shapes chandelier cell function and structure in the visual cortex |
| title_full | Experience shapes chandelier cell function and structure in the visual cortex |
| title_fullStr | Experience shapes chandelier cell function and structure in the visual cortex |
| title_full_unstemmed | Experience shapes chandelier cell function and structure in the visual cortex |
| title_short | Experience shapes chandelier cell function and structure in the visual cortex |
| title_sort | experience shapes chandelier cell function and structure in the visual cortex |
| topic | axo-axonic prediction error chandelier inhibitition arousal most exciting input |
| url | https://elifesciences.org/articles/91153 |
| work_keys_str_mv | AT koenseignette experienceshapeschandeliercellfunctionandstructureinthevisualcortex AT norajamann experienceshapeschandeliercellfunctionandstructureinthevisualcortex AT paolopapale experienceshapeschandeliercellfunctionandstructureinthevisualcortex AT huubterra experienceshapeschandeliercellfunctionandstructureinthevisualcortex AT ralphoporneso experienceshapeschandeliercellfunctionandstructureinthevisualcortex AT leanderdekraker experienceshapeschandeliercellfunctionandstructureinthevisualcortex AT chrisvandertogt experienceshapeschandeliercellfunctionandstructureinthevisualcortex AT maaikevanderaa experienceshapeschandeliercellfunctionandstructureinthevisualcortex AT paulneering experienceshapeschandeliercellfunctionandstructureinthevisualcortex AT emmaruimschotel experienceshapeschandeliercellfunctionandstructureinthevisualcortex AT pieterrroelfsema experienceshapeschandeliercellfunctionandstructureinthevisualcortex AT jorritsmontijn experienceshapeschandeliercellfunctionandstructureinthevisualcortex AT matthewwself experienceshapeschandeliercellfunctionandstructureinthevisualcortex AT maartenhpkole experienceshapeschandeliercellfunctionandstructureinthevisualcortex AT christiaannlevelt experienceshapeschandeliercellfunctionandstructureinthevisualcortex |