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 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.
Fournier
Betty
B
Laboratoire Développement et Vieillissement du Système Nerveux, Unité Mixte de Recherche 7102 Neurobiologie des Processus Adaptatifs, Centre National de la Recherche Scientifique et Université Pierre et Marie Curie, Paris 75005, France.
Lohof
Ann M
AM
Bower
Adrian J
AJ
Mariani
Jean
J
Sherrard
Rachel M
RM
D000818:Animals; D000831:Animals, Newborn; D001931:Brain Mapping; D064026:Calbindins; D002531:Cerebellum / Q000166:cytology / Q000254:growth & development* / Q000502:physiology; D005456:Fluorescent Dyes / Q000493:pharmacokinetics; D007839:Functional Laterality / Q000502:physiology; D007150:Immunohistochemistry / Q000379:methods; D066298:In Vitro Techniques; D008564:Membrane Potentials / Q000187:drug effects / Q000502:physiology / Q000528:radiation effects; D026901:Membrane Transport Proteins / Q000378:metabolism; D009434:Neural Pathways / Q000166:cytology / Q000254:growth & development* / Q000378:metabolism; D009847:Olivary Nucleus / Q000166:cytology* / Q000254:growth & development* / Q000528:radiation effects; D011689:Purkinje Cells / Q000378:metabolism* / Q000528:radiation effects; D051381:Rats; D017208:Rats, Wistar; D064030:S100 Calcium Binding Protein G / Q000378:metabolism; D050599:Vesicular Glutamate Transport Protein 2; D014916:Whole-Body Irradiation / Q000379:methods
D064026:Calbindins; D005456:Fluorescent Dyes; D026901:Membrane Transport Proteins; D064030:S100 Calcium Binding Protein G; C493475:Slc17a6 protein, rat; D050599:Vesicular Glutamate Transport Protein 2