Purkinje cell neurotransmission patterns cerebellar basket cells into zonal modules defined by distinct pinceau sizes
Ramón y Cajal proclaimed the neuron doctrine based on circuit features he exemplified using cerebellar basket cell projections. Basket cells form dense inhibitory plexuses that wrap Purkinje cell somata and terminate as pinceaux at the initial segment of axons. Here, we demonstrate that HCN1, Kv1.1,...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2020-09-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/55569 |
| _version_ | 1811236109445758976 |
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| author | Joy Zhou Amanda M Brown Elizabeth P Lackey Marife Arancillo Tao Lin Roy V Sillitoe |
| author_facet | Joy Zhou Amanda M Brown Elizabeth P Lackey Marife Arancillo Tao Lin Roy V Sillitoe |
| author_sort | Joy Zhou |
| collection | DOAJ |
| description | Ramón y Cajal proclaimed the neuron doctrine based on circuit features he exemplified using cerebellar basket cell projections. Basket cells form dense inhibitory plexuses that wrap Purkinje cell somata and terminate as pinceaux at the initial segment of axons. Here, we demonstrate that HCN1, Kv1.1, PSD95 and GAD67 unexpectedly mark patterns of basket cell pinceaux that map onto Purkinje cell functional zones. Using cell-specific genetic tracing with an Ascl1CreERT2 mouse conditional allele, we reveal that basket cell zones comprise different sizes of pinceaux. We tested whether Purkinje cells instruct the assembly of inhibitory projections into zones, as they do for excitatory afferents. Genetically silencing Purkinje cell neurotransmission blocks the formation of sharp Purkinje cell zones and disrupts excitatory axon patterning. The distribution of pinceaux into size-specific zones is eliminated without Purkinje cell GABAergic output. Our data uncover the cellular and molecular diversity of a foundational synapse that revolutionized neuroscience. |
| first_indexed | 2024-04-12T12:03:15Z |
| format | Article |
| id | doaj.art-29f6d9a6908545afa18e891bb5f2e5c6 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T12:03:15Z |
| publishDate | 2020-09-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-29f6d9a6908545afa18e891bb5f2e5c62022-12-22T03:33:46ZengeLife Sciences Publications LtdeLife2050-084X2020-09-01910.7554/eLife.55569Purkinje cell neurotransmission patterns cerebellar basket cells into zonal modules defined by distinct pinceau sizesJoy Zhou0https://orcid.org/0000-0003-1731-8800Amanda M Brown1https://orcid.org/0000-0002-1484-8972Elizabeth P Lackey2Marife Arancillo3Tao Lin4Roy V Sillitoe5https://orcid.org/0000-0002-6177-6190Department of Pathology and Immunology, Baylor College of Medicine, Houston, United States; Department of Neuroscience, Baylor College of Medicine, Houston, United States; Jan and Dan Duncan Neurological Research Institute of Texas Children’s Hospital, Houston, United StatesDepartment of Pathology and Immunology, Baylor College of Medicine, Houston, United States; Department of Neuroscience, Baylor College of Medicine, Houston, United States; Jan and Dan Duncan Neurological Research Institute of Texas Children’s Hospital, Houston, United StatesDepartment of Pathology and Immunology, Baylor College of Medicine, Houston, United States; Department of Neuroscience, Baylor College of Medicine, Houston, United States; Jan and Dan Duncan Neurological Research Institute of Texas Children’s Hospital, Houston, United StatesDepartment of Pathology and Immunology, Baylor College of Medicine, Houston, United States; Jan and Dan Duncan Neurological Research Institute of Texas Children’s Hospital, Houston, United StatesDepartment of Pathology and Immunology, Baylor College of Medicine, Houston, United States; Jan and Dan Duncan Neurological Research Institute of Texas Children’s Hospital, Houston, United StatesDepartment of Pathology and Immunology, Baylor College of Medicine, Houston, United States; Department of Neuroscience, Baylor College of Medicine, Houston, United States; Jan and Dan Duncan Neurological Research Institute of Texas Children’s Hospital, Houston, United States; Program in Developmental Biology, Baylor College of Medicine, Houston, United StatesRamón y Cajal proclaimed the neuron doctrine based on circuit features he exemplified using cerebellar basket cell projections. Basket cells form dense inhibitory plexuses that wrap Purkinje cell somata and terminate as pinceaux at the initial segment of axons. Here, we demonstrate that HCN1, Kv1.1, PSD95 and GAD67 unexpectedly mark patterns of basket cell pinceaux that map onto Purkinje cell functional zones. Using cell-specific genetic tracing with an Ascl1CreERT2 mouse conditional allele, we reveal that basket cell zones comprise different sizes of pinceaux. We tested whether Purkinje cells instruct the assembly of inhibitory projections into zones, as they do for excitatory afferents. Genetically silencing Purkinje cell neurotransmission blocks the formation of sharp Purkinje cell zones and disrupts excitatory axon patterning. The distribution of pinceaux into size-specific zones is eliminated without Purkinje cell GABAergic output. Our data uncover the cellular and molecular diversity of a foundational synapse that revolutionized neuroscience.https://elifesciences.org/articles/55569cerebelluminterneuronpinceauxinhibitioncircuitrypatterning |
| spellingShingle | Joy Zhou Amanda M Brown Elizabeth P Lackey Marife Arancillo Tao Lin Roy V Sillitoe Purkinje cell neurotransmission patterns cerebellar basket cells into zonal modules defined by distinct pinceau sizes eLife cerebellum interneuron pinceaux inhibition circuitry patterning |
| title | Purkinje cell neurotransmission patterns cerebellar basket cells into zonal modules defined by distinct pinceau sizes |
| title_full | Purkinje cell neurotransmission patterns cerebellar basket cells into zonal modules defined by distinct pinceau sizes |
| title_fullStr | Purkinje cell neurotransmission patterns cerebellar basket cells into zonal modules defined by distinct pinceau sizes |
| title_full_unstemmed | Purkinje cell neurotransmission patterns cerebellar basket cells into zonal modules defined by distinct pinceau sizes |
| title_short | Purkinje cell neurotransmission patterns cerebellar basket cells into zonal modules defined by distinct pinceau sizes |
| title_sort | purkinje cell neurotransmission patterns cerebellar basket cells into zonal modules defined by distinct pinceau sizes |
| topic | cerebellum interneuron pinceaux inhibition circuitry patterning |
| url | https://elifesciences.org/articles/55569 |
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