Anatomy of cerebellar Purkinje cells in the rat determined by a specific immunohistochemical marker

doi:10.1016/0306-4522(84)90193-3

Neuroscience

Volume 11, Issue 4, April 1984, Pages 761-817, IN1-IN2

https://doi.org/10.1016/0306-4522(84)90193-3 Get rights and content

Abstract

In the present study we have used guanosine 3′: 5′-phosphate-dependent protein kinase antiserum, a specific immunohistochemical marker for cerebellar Purkinje cells, [Lohmann, Walter, Miller, Greengard and De Camilli (1981) Proc. natn. Acad. Sci. U.S.A. 78, 653–657], to carry out a detailed analysis of the architecture and projections of Purkinje cells in the adult rat. We have obtained a novel view of aspects of Purkinje cell morphology that were already known and, in addition, we have provided some new information, in particular on the targets of Purkinje cell axons and their pattern of innervation, and on the morphology and course of Purkinje cell axons. Furthermore, we have found a few cells positive for guanosine 3′: 5′ phosphate-dependent protein kinase which are very similar morphologically to Purkinje cells but are located outside of the cerebellar cortex.

A unique feature of Purkinje cells is their peculiar monoplanar shape. Not only do their dendritic arbors lie in planes perpendicular to the major axis of the folia, but their axons, including the collaterals, also travel roughly in the same planes. Thus, Purkinje cells can be imagined as lying in longitudinal sheets radiating from the deep cerebellar nuclei. In these sheets, Purkinje cell axons originating from cells located at different rostrocaudal levels of the cortex converge towards the deep cerebellar nuclei without intersecting each other. It is as a result of this precise organization that Purkinje cell axons reach the deep cerebellar nuclei with a mediolateral and rostrocaudal topology that closely reflects the position of their parent cells in the cerebellar cortex. In the subcortical rays of white matter, Purkinje cell axons are interspersed with other axons, being excluded only from longitudinal strips which correspond to the cerebellar raphes. Upon converging towards the deep cerebellar nuclei they segregate into tracts of white matter that alternate with tracts of white matter from which they are excluded. The great majority of Purkinje cell axons terminate in the deep cerebellar nuclei. Recurrent collaterals terminate in close proximity to the Purkinje cell layer. Dense innervation by these axons is found around large interneurons (Lugaro and Golgi cells) and around the Purkinje cell pinceaux. No direct input of recurrent collaterals to Purkinje cell somata is evident in immunostained material.

A substantial number of Purkinje cell axons continue beyond the cerebellar nuclei to innervate nearby regions in the brain stem. The most prominently innervated extracerebellar target region is the dorsal part of the lateral vestibular nucleus, which is as heavily innervated by Purkinje axons as the deep cerebellar nuclei are. All the other major parts of the vestibular formation and some adjacent nuclei (including the parabrachial nuclei, the prepositus hypoglossal nucleus and the nucleus of the solitary tract) are innervated to various degrees by Purkinje cells. In these regions heavily innervated cells are interspersed with cells which receive only a moderate degree of innervation and with cells which apparently lack Purkinje cell inputs. Upon reaching the deep cerebellar nuclei, axons destined to extracerebellar targets deviate from the planes of dendritic arborization of their parent cells. They converge into tight bundles which follow an irregular course and intersect each other to reach their targets. Axons travelling in the same bundle often appear to terminate on the same cell.

At all target sites Purkinje axons end as varicose terminals which synapse primarily with the perikarya and proximal dendrites of target cells. On the surface of these cells Purkinje cell terminals are often tightly apposed to form a compact mosaic. Both the course of Purkinje cell axons and their pattern of innervation of target cells are consistent with the possibility that contacts between Purkinje cells and their target neurons in the deep cerebellar nuclei and the brain stem are established early in ontogenesis.

Purkinje cell-like cells positive for guanosine 3′:5′-phosphate-dependent protein kinase not located in the cerebellar cortex were found predominantly at the dorsal surface of the brain stem and, in particular, in the cortex of the dorsal cochlear nucleus. Only on exception were they found in the cerebellar medulla or in nearby noncortical regions of the brain stem. While some of these cells might be ectopies, the significance of Purkinje cell-like cells in the dorsal cochlear nucleus, a region strikingly similar in architecture to the cerebellar cortex, remains to be established.

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^¶: Present address: Department of Anatomy, Medical College of Pennsylvania, 3200 Henry Avenue, Philadelphia, PA 19129, U.S.A.

^∥: Present address: Departments of Physiological Chemistry and Medicine, University of Wuerzburg, Koellikerstr. 2, 8700 Wuerzburg, West Germany.

^**: Present address: Laboratory of Molecular and Cellular Neuroscience, The Rockefeller University, 1230 York Avenue, New York, NY 10021, U.S.A.

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Anatomy of cerebellar Purkinje cells in the rat determined by a specific immunohistochemical marker

Abstract

Types of cells in the cochlear nuclei that project to the inferior colliculus of the cat

Anat. Rec.

Morphological development of the rat cerebellum and some of its mechanisms

Autoradiographic and histological studies of postnatal histogenesis. II. A longitudinal investigation of kinetics, migration, and transformation of cells, incorporating thymidine in infant rats with special reference to postnatal neurogenesis in some brain regions

J. comp. Neurol.

The projection of the vestibulocerebellum onto the vestibular nuclei in the cat

Archs ital. Biol.

An investigation of the cerebellar corticonuclear projections in the rat using an autoradiographic tracing method. I. Projections from the vermis

Brain Res.

An investigation of the cerebellar corticonuclear projections in the rat using an autoradiographic tracing method. II. Projections from the hemisphere

Brain Res.

An analysis of the morphology and cytology of HRP labelled Purkinje cells

Brain Res. Bull.

Anatomy of the vestibular nuclei and their connections

Neurological Anatomy

The vestibular nuclei in the cat

J. Anat.

The vestibular nuclei and their connections. Anatomy and functional correlations

Cerebellar Dentate Nucleus. Organization, Cytology and Transmitters

Chemical heterogeneity in cerebellar Purkinje cells: Existence and coexistence of glutamic acid decarboxylase-like and motilin-like immunoreactivities

On the intrinsic fibers of the cerebellum, its nuclei and efferent tract

Brain

Identification of cerebellar corticovestibular neurons retrogradely labeled with horseradish peroxidase

Neuroscience

Dendritic and axonal fields of Purkinje cells in developing and X-irradiated rat cerebellum. A comparative study using intracellular staining with horseradish peroxidase

Neuroscience

Synapsin I (Protein I), a nerve terminal-specific phosphoprotein. II. Its specific association with synaptic vesicles demonstrated by immunocytochemistry in agarose-embedded synaptosomes

J. cell Biol.

The fiber connections of the posterior parts of the cerebellum in the cat and rat

J. comp. Neurol.

Efferent connections of the flocculonodular lobe in Macaca mulatta

J. comp. Neurol.

Subsurface and cytoplasmic cisterns associated with mitochondria in pyramidal neurons of the rat dorsal cochlear nucleus

Neuroscience

A quantitative study of the Purkinje cell dendritic branchlets and their relationship to afferent fibers

J. Anat.

The primate cerebellar cortex: A Golgi and electron microscopic study

Stimulation of horseradish peroxidase by nitrogenous ligands

J. biol. Chem.

Monoclonal antibodies against T lymphocytes label Purkinje neurons of many species

Nature

Sulla fine anatomia degli organi centrali del sistema nervoso. I. Note preliminari sulla struttura, morfologia e vicendevoli rapporti delle cellule gangliari

Riv. sper. Freniat. Med. leg. Alien. ment.

Functional localization in the cerebellum of the albino rat

Expl Neurol.

Patterns of localization in the cerebellar corticonuclear projections of the albino rat

J. comp. Neurol.

Cerebellar corticonuclear and corticovestibular fibers of the anterior lobe vermis in a prosimian primate (Galago senegalensis)

J. comp. Neurol.

Cerebellar corticovestibular fibers of the flocculo-nodular lobe in a prosimian primate (Galago senegalensis)

J. comp. Neurol.

Topography of cerebellar corticonuclear fibers of the albino rat. Vermis of anterior and posterior lobes

Brain Behav. Evol.

Organization of cerebellar corticonuclear fiber systems

Experimental studies on the intrinsic fibers of the cerebellum. II. The corticonuclear projections

J. comp. Neurol.

Pericytes, like smooth muscle cells, have cGMP-dependent protein kinase (cGK) in high concentration

J. cell Biol.

On the conduction paths of the cerebellum. Experimental anatomical observations

Fine structural localization of a new Purkinje cell-specific glycoprotein subunit: Immuno-electron microscopical study

J. comp. Neurol.

Procion yellow and cobalt as tools for the study of structure-function relationships in vertebrate central nervous systems