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Developmental modifications of olivocerebellar topography: The granuloprival cerebellum reveals multiple routes from the inferior olive
Correct function of neural circuits depends on highly organized neuronal connections, refined from less precise projections through synaptic elimination, collateral regression, or neuronal death. We examined regressive phenomena that define olivocerebellar topography during maturation from Purkinje...
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Published in: | Journal of comparative neurology (1911) 2005-09, Vol.490 (1), p.85-97 |
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description | Correct function of neural circuits depends on highly organized neuronal connections, refined from less precise projections through synaptic elimination, collateral regression, or neuronal death. We examined regressive phenomena that define olivocerebellar topography during maturation from Purkinje cell polyinnervation to monoinnervation. We used bilateral retrograde tracing to determine the source of olivocerebellar afferents to posterior vermis lobules VII–VIII in a model of retained immature Purkinje cell polyinnervation, the granuloprival cerebellum. In controls, labelled neurons were found only in the contralateral inferior olive (ION) clustered in a small ventromedial locus that is congruent with known olivocerebellar topography. In granuloprival animals, olivary labelling appeared more dispersed and was present in homologous ipsilateral regions. Double‐labelled neurons were never seen. Retrograde tracing following unilateral olivocerebellar transection in adult granuloprival rats revealed: 1) the origin of the normal (remaining) path projecting through the contralateral inferior peduncle was more localized than in irradiated nonpedunculotomized rats, 2) a small double‐crossed path, and 3) a projection that ascends the peduncle ipsilateral to the ION of origin, part of which crosses the midline within the cerebellum. Electrophysiological and immunohistochemical assessment in the neonatal cerebellum revealed that transcommissural paths are not present during development but sprout within the irradiated cerebellum. Therefore, the olivocerebellar projection in the granuloprival rat, as a model of the immature path, shows parasagittal organization similar to that of controls in its normally crossed path but possesses additional abnormal projections. Thus, maturation of olivocerebellar topography involves removal of whole developmental paths to define laterality plus synapse elimination within largely predefined parasagittal zones. J. Comp. Neurol. 490:85–97, 2005. © 2005 Wiley‐Liss, Inc. |
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We examined regressive phenomena that define olivocerebellar topography during maturation from Purkinje cell polyinnervation to monoinnervation. We used bilateral retrograde tracing to determine the source of olivocerebellar afferents to posterior vermis lobules VII–VIII in a model of retained immature Purkinje cell polyinnervation, the granuloprival cerebellum. In controls, labelled neurons were found only in the contralateral inferior olive (ION) clustered in a small ventromedial locus that is congruent with known olivocerebellar topography. In granuloprival animals, olivary labelling appeared more dispersed and was present in homologous ipsilateral regions. Double‐labelled neurons were never seen. Retrograde tracing following unilateral olivocerebellar transection in adult granuloprival rats revealed: 1) the origin of the normal (remaining) path projecting through the contralateral inferior peduncle was more localized than in irradiated nonpedunculotomized rats, 2) a small double‐crossed path, and 3) a projection that ascends the peduncle ipsilateral to the ION of origin, part of which crosses the midline within the cerebellum. Electrophysiological and immunohistochemical assessment in the neonatal cerebellum revealed that transcommissural paths are not present during development but sprout within the irradiated cerebellum. Therefore, the olivocerebellar projection in the granuloprival rat, as a model of the immature path, shows parasagittal organization similar to that of controls in its normally crossed path but possesses additional abnormal projections. Thus, maturation of olivocerebellar topography involves removal of whole developmental paths to define laterality plus synapse elimination within largely predefined parasagittal zones. J. Comp. Neurol. 490:85–97, 2005. © 2005 Wiley‐Liss, Inc.</description><identifier>ISSN: 0021-9967</identifier><identifier>ISSN: 0092-7317</identifier><identifier>EISSN: 1096-9861</identifier><identifier>EISSN: 1550-7130</identifier><identifier>DOI: 10.1002/cne.20648</identifier><identifier>PMID: 16041715</identifier><language>eng</language><publisher>Hoboken: Wiley Subscription Services, Inc., A Wiley Company</publisher><subject>Animals ; Animals, Newborn ; Brain Mapping ; Calbindins ; Cerebellum - cytology ; Cerebellum - growth & development ; Cerebellum - physiology ; climbing fibers ; Cognitive Sciences ; Fluorescent Dyes - pharmacokinetics ; Functional Laterality - physiology ; Immunohistochemistry - methods ; In Vitro Techniques ; inferior olivary complex ; Life Sciences ; Membrane Potentials - drug effects ; Membrane Potentials - physiology ; Membrane Potentials - radiation effects ; Membrane Transport Proteins - metabolism ; Neural Pathways - cytology ; Neural Pathways - growth & development ; Neural Pathways - metabolism ; Neurons and Cognition ; Olivary Nucleus - cytology ; Olivary Nucleus - growth & development ; Olivary Nucleus - radiation effects ; plasticity ; Purkinje Cells - metabolism ; Purkinje Cells - radiation effects ; Rats ; Rats, Wistar ; S100 Calcium Binding Protein G - metabolism ; synapse elimination ; Vesicular Glutamate Transport Protein 2 ; Whole-Body Irradiation - methods ; X-irradiation</subject><ispartof>Journal of comparative neurology (1911), 2005-09, Vol.490 (1), p.85-97</ispartof><rights>Copyright © 2005 Wiley‐Liss, Inc.</rights><rights>Copyright (c) 2005 Wiley-Liss, Inc.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4268-c5997a2c97a0d5c45c8539ff2fcd8c7eb990bbcc17cac0861d6e4c03594a5f333</citedby><cites>FETCH-LOGICAL-c4268-c5997a2c97a0d5c45c8539ff2fcd8c7eb990bbcc17cac0861d6e4c03594a5f333</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/16041715$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-00082209$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Fournier, Betty</creatorcontrib><creatorcontrib>Lohof, Ann M.</creatorcontrib><creatorcontrib>Bower, Adrian J.</creatorcontrib><creatorcontrib>Mariani, Jean</creatorcontrib><creatorcontrib>Sherrard, Rachel M.</creatorcontrib><title>Developmental modifications of olivocerebellar topography: The granuloprival cerebellum reveals multiple routes from the inferior olive</title><title>Journal of comparative neurology (1911)</title><addtitle>J. Comp. Neurol</addtitle><description>Correct function of neural circuits depends on highly organized neuronal connections, refined from less precise projections through synaptic elimination, collateral regression, or neuronal death. We examined regressive phenomena that define olivocerebellar topography during maturation from Purkinje cell polyinnervation to monoinnervation. We used bilateral retrograde tracing to determine the source of olivocerebellar afferents to posterior vermis lobules VII–VIII in a model of retained immature Purkinje cell polyinnervation, the granuloprival cerebellum. In controls, labelled neurons were found only in the contralateral inferior olive (ION) clustered in a small ventromedial locus that is congruent with known olivocerebellar topography. In granuloprival animals, olivary labelling appeared more dispersed and was present in homologous ipsilateral regions. Double‐labelled neurons were never seen. Retrograde tracing following unilateral olivocerebellar transection in adult granuloprival rats revealed: 1) the origin of the normal (remaining) path projecting through the contralateral inferior peduncle was more localized than in irradiated nonpedunculotomized rats, 2) a small double‐crossed path, and 3) a projection that ascends the peduncle ipsilateral to the ION of origin, part of which crosses the midline within the cerebellum. Electrophysiological and immunohistochemical assessment in the neonatal cerebellum revealed that transcommissural paths are not present during development but sprout within the irradiated cerebellum. Therefore, the olivocerebellar projection in the granuloprival rat, as a model of the immature path, shows parasagittal organization similar to that of controls in its normally crossed path but possesses additional abnormal projections. Thus, maturation of olivocerebellar topography involves removal of whole developmental paths to define laterality plus synapse elimination within largely predefined parasagittal zones. J. Comp. Neurol. 490:85–97, 2005. © 2005 Wiley‐Liss, Inc.</description><subject>Animals</subject><subject>Animals, Newborn</subject><subject>Brain Mapping</subject><subject>Calbindins</subject><subject>Cerebellum - cytology</subject><subject>Cerebellum - growth & development</subject><subject>Cerebellum - physiology</subject><subject>climbing fibers</subject><subject>Cognitive Sciences</subject><subject>Fluorescent Dyes - pharmacokinetics</subject><subject>Functional Laterality - physiology</subject><subject>Immunohistochemistry - methods</subject><subject>In Vitro Techniques</subject><subject>inferior olivary complex</subject><subject>Life Sciences</subject><subject>Membrane Potentials - drug effects</subject><subject>Membrane Potentials - physiology</subject><subject>Membrane Potentials - radiation effects</subject><subject>Membrane Transport Proteins - metabolism</subject><subject>Neural Pathways - cytology</subject><subject>Neural Pathways - growth & development</subject><subject>Neural Pathways - metabolism</subject><subject>Neurons and Cognition</subject><subject>Olivary Nucleus - cytology</subject><subject>Olivary Nucleus - growth & development</subject><subject>Olivary Nucleus - radiation effects</subject><subject>plasticity</subject><subject>Purkinje Cells - metabolism</subject><subject>Purkinje Cells - radiation effects</subject><subject>Rats</subject><subject>Rats, Wistar</subject><subject>S100 Calcium Binding Protein G - metabolism</subject><subject>synapse elimination</subject><subject>Vesicular Glutamate Transport Protein 2</subject><subject>Whole-Body Irradiation - methods</subject><subject>X-irradiation</subject><issn>0021-9967</issn><issn>0092-7317</issn><issn>1096-9861</issn><issn>1550-7130</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2005</creationdate><recordtype>article</recordtype><recordid>eNqFkc1u1DAUhS0EokNhwQsgr5BYpLXj2InZVdM_pFEBqahLy3GuGYMTT-1kYJ6gr11PZ9quEBvbuv7OuVf3IPSekiNKSHlsBjgqiaiaF2hGiRSFbAR9iWb5jxZSivoAvUnpFyFESta8RgdUkIrWlM_Q3SmswYdVD8OoPe5D56wzenRhSDhYHLxbBwMRWvBeRzyGVfgZ9Wq5-Yyvl4Dze5iyPrp1lj-CU49j9tU-4X7yo1t5wDFMIyRsY-jxmJVusBBdiA8t4C16ZTMO7_b3IfpxfnY9vywWXy--zE8WhalK0RSGS1nr0uSDdNxU3DScSWtLa7rG1NBKSdrWGFobbUjeQiegMoRxWWluGWOH6NPOd6m9ylP3Om5U0E5dnizUtpaX1JQlkWua2Y87dhXD7QRpVL1LZruHAcKUlGhIw6is_wvSmvGKCvrc3cSQUgT7NAIlahulylGqhygz-2FvOrU9dM_kPrsMHO-AP87D5t9Oan519mhZ7BQujfD3SaHjbyVqVnN1c3Whypvz0-_fOFMVuweXe7pU</recordid><startdate>20050912</startdate><enddate>20050912</enddate><creator>Fournier, Betty</creator><creator>Lohof, Ann M.</creator><creator>Bower, Adrian J.</creator><creator>Mariani, Jean</creator><creator>Sherrard, Rachel M.</creator><general>Wiley Subscription Services, Inc., A Wiley Company</general><general>John Wiley & Sons</general><scope>BSCLL</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7TK</scope><scope>7X8</scope><scope>1XC</scope></search><sort><creationdate>20050912</creationdate><title>Developmental modifications of olivocerebellar topography: The granuloprival cerebellum reveals multiple routes from the inferior olive</title><author>Fournier, Betty ; Lohof, Ann M. ; Bower, Adrian J. ; Mariani, Jean ; Sherrard, Rachel M.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4268-c5997a2c97a0d5c45c8539ff2fcd8c7eb990bbcc17cac0861d6e4c03594a5f333</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2005</creationdate><topic>Animals</topic><topic>Animals, Newborn</topic><topic>Brain Mapping</topic><topic>Calbindins</topic><topic>Cerebellum - cytology</topic><topic>Cerebellum - growth & development</topic><topic>Cerebellum - physiology</topic><topic>climbing fibers</topic><topic>Cognitive Sciences</topic><topic>Fluorescent Dyes - pharmacokinetics</topic><topic>Functional Laterality - physiology</topic><topic>Immunohistochemistry - methods</topic><topic>In Vitro Techniques</topic><topic>inferior olivary complex</topic><topic>Life Sciences</topic><topic>Membrane Potentials - drug effects</topic><topic>Membrane Potentials - physiology</topic><topic>Membrane Potentials - radiation effects</topic><topic>Membrane Transport Proteins - metabolism</topic><topic>Neural Pathways - cytology</topic><topic>Neural Pathways - growth & development</topic><topic>Neural Pathways - metabolism</topic><topic>Neurons and Cognition</topic><topic>Olivary Nucleus - cytology</topic><topic>Olivary Nucleus - growth & development</topic><topic>Olivary Nucleus - radiation effects</topic><topic>plasticity</topic><topic>Purkinje Cells - metabolism</topic><topic>Purkinje Cells - radiation effects</topic><topic>Rats</topic><topic>Rats, Wistar</topic><topic>S100 Calcium Binding Protein G - metabolism</topic><topic>synapse elimination</topic><topic>Vesicular Glutamate Transport Protein 2</topic><topic>Whole-Body Irradiation - methods</topic><topic>X-irradiation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Fournier, Betty</creatorcontrib><creatorcontrib>Lohof, Ann M.</creatorcontrib><creatorcontrib>Bower, Adrian J.</creatorcontrib><creatorcontrib>Mariani, Jean</creatorcontrib><creatorcontrib>Sherrard, Rachel M.</creatorcontrib><collection>Istex</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><jtitle>Journal of comparative neurology (1911)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Fournier, Betty</au><au>Lohof, Ann M.</au><au>Bower, Adrian J.</au><au>Mariani, Jean</au><au>Sherrard, Rachel M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Developmental modifications of olivocerebellar topography: The granuloprival cerebellum reveals multiple routes from the inferior olive</atitle><jtitle>Journal of comparative neurology (1911)</jtitle><addtitle>J. Comp. Neurol</addtitle><date>2005-09-12</date><risdate>2005</risdate><volume>490</volume><issue>1</issue><spage>85</spage><epage>97</epage><pages>85-97</pages><issn>0021-9967</issn><issn>0092-7317</issn><eissn>1096-9861</eissn><eissn>1550-7130</eissn><abstract>Correct function of neural circuits depends on highly organized neuronal connections, refined from less precise projections through synaptic elimination, collateral regression, or neuronal death. We examined regressive phenomena that define olivocerebellar topography during maturation from Purkinje cell polyinnervation to monoinnervation. We used bilateral retrograde tracing to determine the source of olivocerebellar afferents to posterior vermis lobules VII–VIII in a model of retained immature Purkinje cell polyinnervation, the granuloprival cerebellum. In controls, labelled neurons were found only in the contralateral inferior olive (ION) clustered in a small ventromedial locus that is congruent with known olivocerebellar topography. In granuloprival animals, olivary labelling appeared more dispersed and was present in homologous ipsilateral regions. Double‐labelled neurons were never seen. Retrograde tracing following unilateral olivocerebellar transection in adult granuloprival rats revealed: 1) the origin of the normal (remaining) path projecting through the contralateral inferior peduncle was more localized than in irradiated nonpedunculotomized rats, 2) a small double‐crossed path, and 3) a projection that ascends the peduncle ipsilateral to the ION of origin, part of which crosses the midline within the cerebellum. Electrophysiological and immunohistochemical assessment in the neonatal cerebellum revealed that transcommissural paths are not present during development but sprout within the irradiated cerebellum. Therefore, the olivocerebellar projection in the granuloprival rat, as a model of the immature path, shows parasagittal organization similar to that of controls in its normally crossed path but possesses additional abnormal projections. Thus, maturation of olivocerebellar topography involves removal of whole developmental paths to define laterality plus synapse elimination within largely predefined parasagittal zones. J. Comp. Neurol. 490:85–97, 2005. © 2005 Wiley‐Liss, Inc.</abstract><cop>Hoboken</cop><pub>Wiley Subscription Services, Inc., A Wiley Company</pub><pmid>16041715</pmid><doi>10.1002/cne.20648</doi><tpages>13</tpages></addata></record> |
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subjects | Animals Animals, Newborn Brain Mapping Calbindins Cerebellum - cytology Cerebellum - growth & development Cerebellum - physiology climbing fibers Cognitive Sciences Fluorescent Dyes - pharmacokinetics Functional Laterality - physiology Immunohistochemistry - methods In Vitro Techniques inferior olivary complex Life Sciences Membrane Potentials - drug effects Membrane Potentials - physiology Membrane Potentials - radiation effects Membrane Transport Proteins - metabolism Neural Pathways - cytology Neural Pathways - growth & development Neural Pathways - metabolism Neurons and Cognition Olivary Nucleus - cytology Olivary Nucleus - growth & development Olivary Nucleus - radiation effects plasticity Purkinje Cells - metabolism Purkinje Cells - radiation effects Rats Rats, Wistar S100 Calcium Binding Protein G - metabolism synapse elimination Vesicular Glutamate Transport Protein 2 Whole-Body Irradiation - methods X-irradiation |
title | Developmental modifications of olivocerebellar topography: The granuloprival cerebellum reveals multiple routes from the inferior olive |
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