Development of the spinocerebellar projection in the prenatal mouse

An abundance of information is available concerning the spinocerebellar projection in adult mammals. However, only a few studies have attempted a developmental analysis of this important projection system in early postnatal and/or prenatal animals. The present study provides an analysis of the development of the projection from the spinal cord to the cerebellum in fetal mice using anterograde tracing techniques in an in vitro preparation. After applications of biocytin to the caudal cervical spinal cord, anterogradely labelled fibers were present in the brainstem of embryonic day 12 (E12/13) mice, however, there was no indication of label in the cerebellum. At E13/14, labelled fibers were evident in the rostrolateral portions of the cerebellum/isthmus region. By E15/16, labelled spinocerebellar fibers had progressed farther into the cerebellum and were seen crossing the midline in a very superficial position. At older ages, the number of crossing fibers increased, and they became more ventrally positioned within the cerebellum. At E17/18 and E18/19, labelled spinocerebellar fibers were observed to branch and invade deeper portions of the cerebellum including the cerebellar nuclei. However, at E18/19, there was no indication of the parasagittal organization characteristic of this projection in the adult animal. The results of this study indicate that spinocerebellar fibers are present within the cerebellum significantly earlier than the development and differentiation of their primary targets, the granule cells. Furthermore, these data suggest that spinocerebellar fibers may form associations with cerebellar nuclear cells during fetal development. © 1995 Wiley‐Liss, Inc.

[1]  J. Petras Spinocerebellar neurons in the rhesus monkey , 1977, Brain Research.

[2]  C. Sotelo,et al.  Development of the spinocerebellar system in the postnatal rat , 1985, The Journal of comparative neurology.

[3]  R. Sidman,et al.  An autoradiographic analysis of histogenesis in the mouse cerebellum. , 1961, Experimental neurology.

[4]  J. Altman,et al.  Embryonic development of the rat cerebellum. III. Regional differences in the time of origin, migration, and settling of Purkinje cells , 1985, The Journal of comparative neurology.

[5]  J. Voogd,et al.  Development of the cerebellar cortical efferent projection: an in-vitro anterograde tracing study in rat brain slices. , 1991, Brain research. Developmental brain research.

[6]  P. Rakic Prenatal genesis of connections subserving ocular dominance in the rhesus monkey , 1976, Nature.

[7]  W. Armstrong,et al.  A biotin-containing compound N-(2-aminoethyl)biotinamide for intracellular labeling and neuronal tracing studies: Comparison with biocytin , 1991, Journal of Neuroscience Methods.

[8]  J. Altman,et al.  Embryonic development of the rat cerebellum. II. Translocation and regional distribution of the deep neurons , 1985, The Journal of comparative neurology.

[9]  K W Ashwell,et al.  Ontogeny of afferents to the fetal rat cerebellum. , 1992, Acta anatomica.

[10]  B. Wiksten The central cervical nucleus — A source of spinocerebellar fibres, demonstrated by retrograde transport of horseradish peroxidase , 1975, Neuroscience Letters.

[11]  J. Petras,et al.  The origin of spinocerebellar pathways. II. The nucleus centrobasalis of the cervical enlargement and the nucleus dorsalis of the thoracolumbar spinal cord , 1977, The Journal of comparative neurology.

[12]  E. Friauf,et al.  Pre‐ and postnatal development of efferent connections of the cochlear nucleus in the rat , 1993, The Journal of comparative neurology.

[13]  L. Eisenman,et al.  Spinocerebellar projection in the meander tail mutant mouse: organization in the granular posterior lobe and the agranular anterior lobe , 1991, Brain Research.

[14]  E. G. Jones,et al.  The organization and postnatal development of the commissural projection of the rat somatic sensory cortex , 1976, The Journal of comparative neurology.

[15]  R. Hawkes,et al.  The modular cerebellum , 1991, Progress in Neurobiology.

[16]  M. Matsushita,et al.  The central cervical nucleus as cell origin of a spinocerebellar tract arising from the cervical cord: a study in the cat using horseradish peroxidase , 1975, Brain Research.

[17]  R. Dom,et al.  Spino-cerebellar fibers of the opossum Didelphis marsupialis virginiana. , 1971, Brain research.

[18]  R. Lund,et al.  Development of the geniculocortical pathway in rat , 1977, The Journal of comparative neurology.

[19]  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.

[20]  P. Rakić Prenatal development of the visual system in rhesus monkey. , 1977, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[21]  C. Shatz,et al.  The relationship between the geniculocortical afferents and their cortical target cells during development of the cat's primary visual cortex , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  R. Faull,et al.  A comparative study of the neurons of origin of the spinocerebellar afferents in the rat, Cat and squirrel monkey based on the retrograde transport of horseradish peroxidase , 1978, The Journal of comparative neurology.

[23]  C. Sotelo,et al.  Cerebellar development: afferent organization and Purkinje cell heterogeneity. , 1991, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[24]  D. Whitlock A neurohistological and neurophysiological study of afferent fiber tracts and receptive areas of the avian cerebellum , 1952, The Journal of comparative neurology.

[25]  J. Altman Autoradiographic and histological studies of postnatal neurogenesis. III. Dating the time of production and onset of differentiation of cerebellar microneurons in rats , 1969, The Journal of comparative neurology.

[26]  J. Altman,et al.  Embryonic development of the rat cerebellum. I. Delineation of the cerebellar primordium and early cell movements , 1985, The Journal of comparative neurology.

[27]  N. Okado,et al.  Spinocerebellar projections to lobules I and II of the anterior lobe in the cat, as studied by retrograde transport of horseradish peroxidase , 1981, The Journal of comparative neurology.

[28]  T. Ueyama,et al.  Projections from the spinal cord to the cerebellar nuclei in the rabbit and rat. , 1973, Experimental neurology.

[29]  M. King,et al.  Biocytin: a versatile anterograde neuroanatomical tract-tracing alternative , 1989, Brain Research.

[30]  G. Martin,et al.  The early development of major projections from caudal levels of the spinal cord to the brainstem and cerebellum in the gray short-tailed Brazilian opossum, Monodelphis domestica. , 1993, Brain research. Developmental brain research.

[31]  C. Sotelo,et al.  Organization of spinocerebellar projection map in three types of agranular cerebellum: Purkinje cells vs. granule cells as organizer element , 1988, The Journal of comparative neurology.

[32]  C. Sherrington,et al.  GOWER'S TRACT AND SPINAL BORDER CELLS , 1940 .

[33]  R. Dom,et al.  Observations on the development of brainstem‐spinal systems in the north american opossum , 1978, The Journal of comparative neurology.

[34]  J. Petras,et al.  The origin of spinocerebellar pathways. I. The nucleus cervicalis centralis of the cranial cervical spinal cord , 1977, The Journal of comparative neurology.

[35]  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.