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The Journal of Neuroscience, May 16, 2007, 27(20):5373-5383; doi:10.1523/JNEUROSCI.0452-07.2007

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Development/Plasticity/Repair
Reinnervation of Late Postnatal Purkinje Cells by Climbing Fibers: Neosynaptogenesis without Transient Multi-Innervation

Mathieu Letellier,¹ Yannick Bailly,² Valérie Demais,³ Rachel M. Sherrard,⁴ Jean Mariani,^1,5 and Ann M. Lohof¹

¹Université Pierre et Marie Curie-Paris, Unité Mixte de Recherche (UMR) 7102–Neurobiologie des Processus Adaptatifs (NPA), and Centre National de la Recherche Scientifique (CNRS), UMR 7102–NPA, F-75005 Paris, France, ²Neurotransmission et Sécrétion Neuroendocrine, UMR 7168 Institut des Neurosciences Cellulaires et Intégratives, CNRS, and ³Plateforme d'Imagerie In Vitro, Institut Fédératif de Recherche 37 des Neurosciences, Université Louis Pasteur, F-67084 Strasbourg, France, ⁴School of Anatomy and Human Biology, University of Western Australia, Crawley 6009, Australia, and ⁵Assistance Publique–Hôpitaux de Paris Hôpital Charles Foix, Unité d'Explorations Fonctionnelles, F-94200, Ivry sur Seine, France

Correspondence should be addressed to Dr. Ann M. Lohof, Université Pierre et Marie Curie, Unité Mixte de Recherche 7102–Neurobiologie des Processus Adaptatifs, 9 quai St. Bernard, case 14, 75005 Paris, France. Email: ann.lohof{at}snv.jussieu.fr

Synaptic partner selection and refinement of projections are important in the development of precise and functional neuronal connections. We investigated the formation of new synaptic connections in a relatively mature system to test whether developmental events can be recapitulated at later stages (i.e., after the mature synaptic organization has been established), using a model of postlesional reinnervation in the olivo-cerebellar pathway.

During the development of this pathway, synaptic connections between climbing fibers (CFs) and Purkinje cells (PCs) are diffuse and redundant before synapse elimination refines the pattern. The regression of CFs during the first 2 postnatal weeks in the rat leads to mono-innervation of each PC. After unilateral transection of the rat olivo-cerebellar pathway and intracerebellar injection of BDNF 24 h after lesion, axons from the remaining inferior olive can sprout into the deafferented hemicerebellum and establish new contacts with denervated PCs at later developmental stages. We found that these contacts are first established on somatic thorns before the CFs translocate to the PC dendrites, recapitulating the morphological steps of normal CF–PC synaptogenesis, but on a relatively mature PC.

However, electrophysiology of PC reinnervation by transcommissural CFs in these animals showed that each PC is reinnervated by only one CF. This mono-innervation contrasts with the reinnervation of grafted immature PCs in the same cerebellum. Our results provide evidence that relatively mature PCs do not receive several olivary afferents during late reinnervation, suggesting a critical role of the target cell state in the control of CF–PC synaptogenesis. Thus, synapse exuberance and subsequent elimination are not a prerequisite to reach a mature relationship between synaptic partners.

Key words: cerebellum; synaptogenesis; reinnervation; Purkinje cell; climbing fiber; synapse elimination

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Received Oct. 23, 2006; revised March 21, 2007; accepted April 16, 2007.

Correspondence should be addressed to Dr. Ann M. Lohof, Université Pierre et Marie Curie, Unité Mixte de Recherche 7102–Neurobiologie des Processus Adaptatifs, 9 quai St. Bernard, case 14, 75005 Paris, France. Email: ann.lohof{at}snv.jussieu.fr

This article has been cited by other articles:

				M. Letellier, R. Wehrle, J. Mariani, and A. M. Lohof Synapse elimination in olivo-cerebellar explants occurs during a critical period and leaves an indelible trace in Purkinje cells PNAS, August 18, 2009; 106(33): 14102 - 14107. [Abstract] [Full Text] [PDF]

				M. L. Willson, C. McElnea, J. Mariani, A. M. Lohof, and R. M. Sherrard BDNF increases homotypic olivocerebellar reinnervation and associated fine motor and cognitive skill Brain, April 1, 2008; 131(4): 1099 - 1112. [Abstract] [Full Text] [PDF]

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