Functional regionalization of the differentiating cerebellar Purkinje cell population occurs in an activity-dependent manner
IntroductionThe cerebellum is organized into functional regions each dedicated to process different motor or sensory inputs for controlling different locomotor behaviors. This functional regionalization is prominent in the evolutionary conserved single-cell layered Purkinje cell (PC) population. Fra...
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Frontiers Media S.A.
2023-04-01
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| Series: | Frontiers in Molecular Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnmol.2023.1166900/full |
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| author | Alessandro Dorigo Komali Valishetti Florian Hetsch Florian Hetsch Hideaki Matsui Hideaki Matsui Jochen C. Meier Kazuhiko Namikawa Reinhard W. Köster |
| author_facet | Alessandro Dorigo Komali Valishetti Florian Hetsch Florian Hetsch Hideaki Matsui Hideaki Matsui Jochen C. Meier Kazuhiko Namikawa Reinhard W. Köster |
| author_sort | Alessandro Dorigo |
| collection | DOAJ |
| description | IntroductionThe cerebellum is organized into functional regions each dedicated to process different motor or sensory inputs for controlling different locomotor behaviors. This functional regionalization is prominent in the evolutionary conserved single-cell layered Purkinje cell (PC) population. Fragmented gene expression domains suggest a genetic organization of PC layer regionalization during cerebellum development. However, the establishment of such functionally specific domains during PC differentiation remained elusive.Methods and resultsWe show the progressive emergence of functional regionalization of PCs from broad responses to spatially restricted regions in zebrafish by means of in vivo Ca2+-imaging during stereotypic locomotive behavior. Moreover, we reveal that formation of new dendritic spines during cerebellar development using in vivo imaging parallels the time course of functional domain development. Pharmacological as well as cell-type specific optogenetic inhibition of PC neuronal activity results in reduced PC dendritic spine density and an altered stagnant pattern of functional domain formation in the PC layer.DiscussionHence, our study suggests that functional regionalization of the PC layer is driven by physiological activity of maturing PCs themselves. |
| first_indexed | 2024-04-09T15:45:33Z |
| format | Article |
| id | doaj.art-a8fff6a6dafc47dcbb827ac3139fe5f1 |
| institution | Directory Open Access Journal |
| issn | 1662-5099 |
| language | English |
| last_indexed | 2024-04-09T15:45:33Z |
| publishDate | 2023-04-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Molecular Neuroscience |
| spelling | doaj.art-a8fff6a6dafc47dcbb827ac3139fe5f12023-04-27T04:50:00ZengFrontiers Media S.A.Frontiers in Molecular Neuroscience1662-50992023-04-011610.3389/fnmol.2023.11669001166900Functional regionalization of the differentiating cerebellar Purkinje cell population occurs in an activity-dependent mannerAlessandro Dorigo0Komali Valishetti1Florian Hetsch2Florian Hetsch3Hideaki Matsui4Hideaki Matsui5Jochen C. Meier6Kazuhiko Namikawa7Reinhard W. Köster8Cellular and Molecular Neurobiology, Technische Universität Braunschweig, Braunschweig, GermanyCellular and Molecular Neurobiology, Technische Universität Braunschweig, Braunschweig, GermanyCell Physiology, Zoological Institute, Technische Universität Braunschweig, Braunschweig, GermanyInstitute of Pathophysiology, University Medical Center, Johannes Gutenberg University, Mainz, GermanyCellular and Molecular Neurobiology, Technische Universität Braunschweig, Braunschweig, GermanyDepartment of Neuroscience of Disease, Brain Research Institute, Niigata University, Niigata, JapanCell Physiology, Zoological Institute, Technische Universität Braunschweig, Braunschweig, GermanyCellular and Molecular Neurobiology, Technische Universität Braunschweig, Braunschweig, GermanyCellular and Molecular Neurobiology, Technische Universität Braunschweig, Braunschweig, GermanyIntroductionThe cerebellum is organized into functional regions each dedicated to process different motor or sensory inputs for controlling different locomotor behaviors. This functional regionalization is prominent in the evolutionary conserved single-cell layered Purkinje cell (PC) population. Fragmented gene expression domains suggest a genetic organization of PC layer regionalization during cerebellum development. However, the establishment of such functionally specific domains during PC differentiation remained elusive.Methods and resultsWe show the progressive emergence of functional regionalization of PCs from broad responses to spatially restricted regions in zebrafish by means of in vivo Ca2+-imaging during stereotypic locomotive behavior. Moreover, we reveal that formation of new dendritic spines during cerebellar development using in vivo imaging parallels the time course of functional domain development. Pharmacological as well as cell-type specific optogenetic inhibition of PC neuronal activity results in reduced PC dendritic spine density and an altered stagnant pattern of functional domain formation in the PC layer.DiscussionHence, our study suggests that functional regionalization of the PC layer is driven by physiological activity of maturing PCs themselves.https://www.frontiersin.org/articles/10.3389/fnmol.2023.1166900/fullzebrafishcerebellumPurkinje cellfunctional regionalizationcalcium imagingoptogenetics |
| spellingShingle | Alessandro Dorigo Komali Valishetti Florian Hetsch Florian Hetsch Hideaki Matsui Hideaki Matsui Jochen C. Meier Kazuhiko Namikawa Reinhard W. Köster Functional regionalization of the differentiating cerebellar Purkinje cell population occurs in an activity-dependent manner Frontiers in Molecular Neuroscience zebrafish cerebellum Purkinje cell functional regionalization calcium imaging optogenetics |
| title | Functional regionalization of the differentiating cerebellar Purkinje cell population occurs in an activity-dependent manner |
| title_full | Functional regionalization of the differentiating cerebellar Purkinje cell population occurs in an activity-dependent manner |
| title_fullStr | Functional regionalization of the differentiating cerebellar Purkinje cell population occurs in an activity-dependent manner |
| title_full_unstemmed | Functional regionalization of the differentiating cerebellar Purkinje cell population occurs in an activity-dependent manner |
| title_short | Functional regionalization of the differentiating cerebellar Purkinje cell population occurs in an activity-dependent manner |
| title_sort | functional regionalization of the differentiating cerebellar purkinje cell population occurs in an activity dependent manner |
| topic | zebrafish cerebellum Purkinje cell functional regionalization calcium imaging optogenetics |
| url | https://www.frontiersin.org/articles/10.3389/fnmol.2023.1166900/full |
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