Postnatal development and adult organisation of the olivocerebellar projection map in the hypogranular cerebellum of the rat

The olivocerebellar system is characterised by a precise topographical organisation, in which distinct subsets of inferior olivary axons project to neurochemically heterogeneous Purkinje cell subpopulations, arranged into parasagittally oriented compartments in the cerebellar cortex. Adult climbing fibres and Purkinje cells are linked by a one‐to‐one relationship, which is established during postnatal development after a transitory phase of multiple climbing fibre innervation. The elimination of redundant climbing fibre synapses is thought to be regulated by granule cell‐mediated activity‐dependent processes. In order to assess whether this developmental remodelling is also important for the construction of the mature olivocerebellar projection map, we examined the hypogranular cerebella of rats treated by means of methylazoxymethanol acetate (MAM) during early postnatal life, in which multiple climbing fibre innervation persists in the adult. In these animals we investigated the distribution of calcitonin gene‐related peptide (CGRP)‐immunoreactive olivocerebellar axons and arbours during early postnatal development, and the correspondence between climbing fibre strips and zebrin II‐defined Purkinje cell bands in the adult. Our results show that: (1) the pattern of CGRP‐immunoreactive climbing fibres observed during the first three postnatal weeks is not disrupted after granule cell degeneration; and (2) the alignment between olivocerebellar axon subsets and zebrin II+/− Purkinje cell compartments is normally achieved in adult rats. In contrast, the climbing fibre‐Purkinje cell relationship is abnormal, and single arbours innervate restricted dendritic regions of several neighbouring target neurons. These results indicate that the normal distribution of olivocerebellar axon subsets to distinct cerebellar cortical compartments can be established independently from granule cell‐mediated remodelling processes. Thus, the postnatal climbing fibre plasticity, which is needed to achieve the normal climbing fibre‐Purkinje cell relationship, appears to be confined within the framework of a projection map established during earlier developmental phases. J. Comp. Neurol. 407:527–542, 1999. © 1999 Wiley‐Liss, Inc.

[1]  J. Lichtman,et al.  Synaptic segregation at the developing neuromuscular junction. , 1998, Science.

[2]  Karl Schilling,et al.  From zebra stripes to postal zones: deciphering patterns of gene expression in the cerebellum , 1998, Trends in Neurosciences.

[3]  P. Strata,et al.  Plasticity of the olivocerebellar pathway , 1998, Trends in Neurosciences.

[4]  P. Strata,et al.  Reestablishment of the olivocerebellar projection map by compensatory transcommissural reinnervation following unilateral transection of the inferior cerebellar peduncle in the newborn rat , 1997 .

[5]  C. Sotelo,et al.  The embryonic cerebellum contains topographic cues that guide developing inferior olivary axons. , 1997, Development.

[6]  Susumu Tonegawa,et al.  Persistent Multiple Climbing Fiber Innervationof Cerebellar Purkinje Cellsin Mice Lacking mGluR1 , 1997, Neuron.

[7]  H. Daniel,et al.  Incomplete regression of multiple climbing fibre innervation of cerebellar Purkinje cells in mGluR1 mutant mice , 1997, Neuroreport.

[8]  Richard Hawkes,et al.  Chapter 3 An anatomical model of cerebellar modules , 1997 .

[9]  J. Voogd,et al.  Transverse and longitudinal patterns in the mammalian cerebellum. , 1997, Progress in brain research.

[10]  K. Herrup,et al.  The compartmentalization of the cerebellum. , 1997, Annual review of neuroscience.

[11]  R J Smeyne,et al.  Correspondence between L7‐lacZ‐expressing purkinje cells and labeled olivocerebellar fibers during late embryogenesis in the mouse , 1996, The Journal of comparative neurology.

[12]  R. Hawkes,et al.  Partial ablation of the neonatal external granular layer disrupts mossy fiber topography in the adult rat cerebellum , 1996, The Journal of comparative neurology.

[13]  C. Sotelo,et al.  BEN As a Presumptive Target Recognition Molecule during the Development of the Olivocerebellar System , 1996, The Journal of Neuroscience.

[14]  P Strata,et al.  Topographically Organized Climbing Fibre Sprouting in the Adult Rat Cerebellum , 1996, The European journal of neuroscience.

[15]  S. Tonegawa,et al.  Impaired synapse elimination during cerebellar development in PKCγ mutant mice , 1995, Cell.

[16]  A. Joyner,et al.  A role for En-2 and other murine homologues of Drosophila segment polarity genes in regulating positional information in the developing cerebellum. , 1995, Development.

[17]  P. Strata,et al.  Reciprocal trophic interactions in the adult climbing fibre—Purkinje cell system , 1995, Progress in Neurobiology.

[18]  P Strata,et al.  Different climbing fibres innervate separate dendritic regions of the same purkinje cell in hypogranular cerebellum , 1995, The Journal of comparative neurology.

[19]  M L Johnson,et al.  Molecular compartmentation expressed in cerebellar cultures in the absence of neuronal activity and neuron‐glia interactions , 1995, The Journal of comparative neurology.

[20]  Youngnam Kang,et al.  Impairment of motor coordination, Purkinje cell synapse formation, and cerebellar long-term depression in GluRδ2 mutant mice , 1995, Cell.

[21]  N. Delhaye-bouchaud,et al.  Enlargement of olivo-cerebellar microzones in the agranular cerebellum of adult rats , 1994, Brain Research.

[22]  Karl Schilling,et al.  Control of segment-like patterns of gene expression in the mouse cerebellum , 1993, Neuron.

[23]  L. Eisenman,et al.  Evidence of early topographic organization in the embryonic olivocerebellar projection: A model system for the study of pattern formation processes in the central nervous system , 1993, Developmental dynamics : an official publication of the American Association of Anatomists.

[24]  C. Shatz,et al.  Developmental mechanisms that generate precise patterns of neuronal connectivity , 1993, Cell.

[25]  K. Herrup,et al.  Role of the target in synapse elimination: studies in cerebellum of developing lurcher mutants and adult chimeric mice , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  C. Sotelo,et al.  Early Development of Olivocerebellar Projections in the Fetal Rat Using CGRP Immunocytochemistry , 1992, The European journal of neuroscience.

[27]  C. Sotelo,et al.  Development of the olivocerebellar projection in the rat: II. Matching of the developmental compartmentations of the cerebellum and inferior olive through the projection map , 1992, The Journal of comparative neurology.

[28]  C. Sotelo,et al.  Development of the olivocerebellar projection in the rat: I. Transient biochemical compartmentation of the inferior olive , 1992, The Journal of comparative neurology.

[29]  S. Rabacchi,et al.  Involvement of the N-methyl D-aspartate (NMDA) receptor in synapse elimination during cerebellar development. , 1992, Science.

[30]  C. Sotelo,et al.  Purkinje Cell Heterogeneity: Its Role in Organizing the Topography of the Cerebellar Cortex Connections , 1992 .

[31]  R. Hawkes,et al.  Zebrins: Molecular Markers of Compartmentation in the Cerebellum , 1992 .

[32]  N. Delhaye-bouchaud,et al.  Extent of multiple innervation of cerebellar Purkinje cells by climbing fibers in adult X-irradiated rats. Comparison of different schedules of irradiation during the first postnatal week. , 1990, Brain research. Developmental brain research.

[33]  S. M. Catalano,et al.  Early climbing fiber interactions with Purkinje cells in the postnatal mouse cerebellum , 1990, The Journal of comparative neurology.

[34]  C. Sotelo,et al.  Expression of compartmentation antigen zebrin I in cerebellar transplants , 1990, The Journal of comparative neurology.

[35]  R. Hawkes,et al.  Zebrin II: A polypeptide antigen expressed selectively by purkinje cells reveals compartments in rat and fish cerebellum , 1990, The Journal of comparative neurology.

[36]  A. Rosina,et al.  CGRP expression in the rat olivocerebellar system during postnatal development , 1989, Brain Research.

[37]  R. Hawkes,et al.  Development of parasagittal zonation in the rat cerebellar cortex: MabQ113 antigenic bands are created postnatally by the suppression of antigen expression in a subset of Purkinje cells , 1988, The Journal of comparative neurology.

[38]  D. Hillman,et al.  Developmental factors related to abnormal cerebellar foliation induced by methylazoxymethanol acetate (MAM). , 1988, Brain research.

[39]  D. Hillman,et al.  Perinatal methylazoxymethanol acetate uncouples coincidence of orientation of cerebellar folia and parallel fibers , 1988, Neuroscience.

[40]  R. Hawkes,et al.  Parasagittal organization of the rat cerebellar cortex: Direct correlation between antigenic purkinje cell bands revealed by mabQ113 and the organization of the olivocerebellar projection , 1987, The Journal of comparative neurology.

[41]  C. Mulle,et al.  Peripheral maps and synapse elimination in the cerebellum of the rat.I. Representation of peripheral inputs through the climbing fiber pathway in the posterior vermis of the normal adult rat , 1987, Brain Research.

[42]  Y. Kubota,et al.  Transient appearance of calcitonin gene-related peptide-like immunoreactive fibers in the developing cerebellum of the rat , 1987, Brain Research.

[43]  N. Delhaye-bouchaud,et al.  Evidence for a multiple innervation of cerebellar Purkinje cells by climbing fibers in adult ferrets infected at birth by a mink enteritis virus. , 1987, Brain research.

[44]  C. Sotelo,et al.  Transient biochemical compartmentalization of Purkinje cells during early cerebellar development. , 1985, Developmental biology.

[45]  G. Paxinos The Rat nervous system , 1985 .

[46]  Jeff W. Lichtman,et al.  Principles of neural development , 1985 .

[47]  C. Sotelo,et al.  Asynchrony in the expression of guanosine 3′:5′-phosphate-dependent protein kinase by clusters of purkinje cells during the perinatal development of rat cerebellum , 1984, Neuroscience.

[48]  C. Sotelo,et al.  Postnatal development of the inferior olivary complex in the rat. II. Topographic organization of the immature olivocerebellar projection , 1984, The Journal of comparative neurology.

[49]  D. Purves,et al.  Regional innervation of rabbit ciliary ganglion cells by the terminals of preganglionic axons , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[50]  F. Crépel Regression of functional synapses in the immature mammalian cerebellum , 1982, Trends in Neurosciences.

[51]  Dale Purves,et al.  Geometry of neonatal neurones and the regulation of synapse elimination , 1981, Nature.

[52]  F. Crépel,et al.  Multiple innervation of cerebellar Purkinje cells by climbing fibres in staggerer mutant mouse , 1980, Nature.

[53]  M. Goetting,et al.  Regeneration in the cerebellum following methylazoxymethanol-induced destruction of the external germinal layer. Morphological and biochemical studies. , 1980, Developmental neuroscience.

[54]  F. Crépel,et al.  Distribution of climbing fibres on cerebellar Purkinje cells in X‐irradiated rats. An electrophysiological study. , 1979, The Journal of physiology.

[55]  A. Grinnell,et al.  Competitive interaction between foreign nerves innervating frog skeletal muscle. , 1979, The Journal of physiology.

[56]  G. M. Shambes,et al.  Fractured somatotopy in granule cell tactile areas of rat cerebellar hemispheres revealed by micromapping. , 1978, Brain, behavior and evolution.

[57]  D. Puro,et al.  Physiological properties of afferents and synaptic reorganization in the rat cerebellum degranulated by postnatal X-irradiation. , 1978, Journal of neurobiology.

[58]  J. Jansen,et al.  The elimination of synapses in multiply-innervated skeletal muscle fibres of the rat: dependence on distance between end-plates , 1977, Brain Research.

[59]  P. W. Russell Eggitt,et al.  Choosing Between Crops: Aspects that Affect the User [and Discussion] , 1977 .

[60]  J. Changeux,et al.  Anatomical, physiological and biochemical studies of the cerebellum from Reeler mutant mouse. , 1977, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[61]  J. Changeux,et al.  Selective stabilisation of developing synapses as a mechanism for the specification of neuronal networks , 1976, Nature.

[62]  F. Crépel,et al.  Multiple innervation of Purkinje cells by climbing fibers in the cerebellum of the Weaver Mutant Mouse. , 1976, Journal of neurobiology.

[63]  F. Crépel,et al.  Evidence for a multiple innervation of Purkinje cells by climbing fibers in the immature rat cerebellum. , 1976, Journal of neurobiology.

[64]  D. Woodward,et al.  Purkinje cell dendritic alterations after transient developmental injury of the external granular layer , 1975, Brain Research.

[65]  E. Frank,et al.  The interaction between foreign and original motor nerves innervating the soleus muscle of rats. , 1975, The Journal of physiology.

[66]  D. Armstrong Functional significance of connections of the inferior olive. , 1974, Physiological reviews.

[67]  J. Altman,et al.  Physiological and pharmacological properties of Purkinje cells in rat cerebellum degranulated by postnatal x-irradiation. , 1974, Journal of neurobiology.

[68]  Professor Dr. John C. Eccles,et al.  The Cerebellum as a Neuronal Machine , 1967, Springer Berlin Heidelberg.

[69]  T. Neales Effect of Boron Supply on the Sugars, Soluble in 80 per cent Ethanol, in Flax Seedlings , 1959, Nature.