A Golgi study of neuronal types in the neostriatum of monkeys

doi:10.1016/0006-8993(76)90669-7

Brain Research

Volume 114, Issue 2, 17 September 1976, Pages 245-256

https://doi.org/10.1016/0006-8993(76)90669-7 Get rights and content

Abstract

Examination of the neostriatum of monkeys prepared by the Golgi-Kopsch perfusion method revealed the presence of at least 6 neuronal types. The spiny type I is medium size with a high density of dendritic spines. The axon extends well beyond the dendritic field and gives off many collaterals. The spiny type II is either medium or large size, has long thick dendrites with a relatively low density of spines, and an axon similar to that of the previous type but with fewer collaterals. The aspiny type I is medium size with varicose dendrites and a thin axon arborizing in the immediate vicinity of the soma. The aspiny type II is large, with many thick and thin varicose dendrites. The aspiny type III is medium size with smooth dendrites and an axon ramifying profusely within the dendritic field. The neurogliform cell is small with many branching processes.

Findings indicate that the neostriatum has 2 distinct types of spiny neurons with long axons (spiny I and II), some of which may contribute to the efferent systems. There are also 2 (aspiny I and III) or perhaps as many as 4 categories (aspiny I, II, III and neurogliform) of typical Golgi type II cells. Large neurons belong to 2 separate populations, one with dendritic spines and a long axon (large version of spiny II), and one with varicosities and presumably a short axon (aspiny II). A realistic interpretation of neurophysiologic data on the neostriatum must take into account all cell types instead of the current view of considering it as a pool of interneurons with few output cells.

References (21)

BuchwaldN.A. et al.
Caudate intracellular response to thalamic and cortical inputs
Exp. Neurol.
(1973)
GrofováI.
The identificaton of striatal and pallidal neurons projecting to substantia nigra. An experimental study by means of retrograde axonal transport of horseradish peroxidase
Brain Research
(1975)
HullC.D. et al.
Intracellular responses of caudate neurons to temporally and spatially combined stimuli
Exp. Neurol.
(1973)
KitaiS.T. et al.
Nigro-caudate and caudato-nigral relationship: an electrophysiological study
Brain Research
(1975)
DejerineJ.
DiFiglia-SekulerM. et al.
A Golgi study of the neostriatum in monkeys
Neurosc. Abstr.
(1975)
FoixC. et al.
Les Noyaux Gris Centraux et la Région Mésencéphalo-sous-optique
FoxC.A. et al.
The spiny neurons in the primate striatum: a Golgi and electron microscopic study
J. Hirnforsch.
(1972)
FoxC.A. et al.
The aspiny neurons and the glia in the primate striatum: a Golgi and electron microscopic study
J. Hirnforsch.
(1972)
FoxC.A. et al.
Further observations on Ramón y Cajal's ‘dwarf’ or ‘neurogliaform’ neurons and the olgodendroglia in the primate striatum
J. Hirnforsch.
(1974)

There are more references available in the full text version of this article.

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A Golgi study of neuronal types in the neostriatum of monkeys

Abstract

Exp. Neurol.

Brain Research

Exp. Neurol.

Brain Research

A Golgi study of the neostriatum in monkeys

Neurosc. Abstr.

Les Noyaux Gris Centraux et la Région Mésencéphalo-sous-optique

The spiny neurons in the primate striatum: a Golgi and electron microscopic study

J. Hirnforsch.

The aspiny neurons and the glia in the primate striatum: a Golgi and electron microscopic study

J. Hirnforsch.

Further observations on Ramón y Cajal's ‘dwarf’ or ‘neurogliaform’ neurons and the olgodendroglia in the primate striatum

J. Hirnforsch.