Cortical relay neurons and interneurons in the N. ventralis posterolateralis of cats: A horseradish peroxidase, electron-microscopic, golgi and immunocytochemical study

doi:10.1016/0306-4522(83)90168-9

Neuroscience

Volume 9, Issue 3, July 1983, Pages 491-509

https://doi.org/10.1016/0306-4522(83)90168-9 Get rights and content

Abstract

After injections of horseradish peroxidase involving the whole primary (SI) and secondary somatosensory (SII) areas of adult cats, 16–21% out of 2220 counted neurons in the nucleus ventralis posterolateralis were unlabelled. The mean areas of perikarya of these neurons varied between111.8 ± 32.3 μm² and180.8 ± 48.6μm². The size of perikarya of retrogradely-labelled neuron ranged from256.9 ± 100.4μm² to409 ± 163 μm². Retrogradely-labelled and unlabelled neurons were examined under light- and high-voltage electron-microscopy. Besides ‘large’, mainly multipolar or oval fusiform perikarya, retrogradely-labelled neurons may display perikarya of ‘small’ size. Both types of neurons correlate well with Golgi-impregnated cells with a tufted dendritic pattern usually identified as thalamocortical neurons. On the other hand, the size and morphology of perikarya and initial dendrites of neurons unlabelled by retrograde transport of horseradish peroxidase correlate well with that of Golgi-impregnated neurons which are markedly different from the thalamocortical neurons, have very characteristic and profuse dendritic appendages and have been identified by previous investigators as Golgi Type II neurons.

In order to probe further whether these may correspond to the GABAergic interneurons proposed by previous evidence, an immunocytochemical approach was also applied at the light- and electron-microscope level, using an antiserum prepared in sheep against rat brain glutamate decar☐ylase. By this method it is shown that 19–21% of neurons in the nucleus ventralis posterolateralis of adult cats are glutamate decar☐ylase-positive and that the perikaryal size of these labelled neurons ranges between134.6 ± 44.5μm² and164.4 ± 47.3μm². Histogram distribution of the number and areas of the counted immunoreactive neurons closely matches that of unlabelled neurons in experiments with retrograde transport of horseradish peroxidase.

The results give support to previous evidence suggesting that part of population of neurons in the nucleus ventralis posterolateralis is represented by a distinct class of neurons which are apparently GABAergic.

Reference (59)

HardyH. et al.
A safer and more sensitive substitute for diaminobenzidine in the light microscopic demonstration of retrograde and anterograde axonal transport of HRP
Neuroscience Letters
(1977)
HouserC.R. et al.
GABA neurons are the major cell type of the nucleus reticularis thalami
Brain Res.
(1980)
LaemleL.
Cell populations of lateral geniculate nucleus of cat as determined with horseradish peroxidase
Brain Res.
(1975)
LeVayS. et al.
Proportions of interneurons in the cat's lateral geniculate nucleus
Brain Res.
(1979)
LinC.S. et al.
Percentage of relay cells in the cat's lateral geniculate nucleus
Brain Res.
(1977)
MonteroV.M. et al.
Synaptic terminals in the dorsal lateral geniculate nucleus from neurons of the thalamic reticular nucleus: a light- and electron-microscope autoradiographic study
Neuroscience
(1981)
OertelW.H. et al.
Immunocytochemical localization of glutamate decar☐ylase in rat cerebellum with a new antiserum
Neuroscience
(1981)
OertelW.H. et al.
Production of a specific antiserum to rat brain glutamic acid decar☐ylase by injection of antigen-antibody complex
Neroscience
(1981)
O'HaraP.T. et al.
Mode of termination of afferents from the thalamic reticular nucleus in the dorsal lateral geniculate nucleus of the rat
Brain Res.
(1980)
PennyG.R. et al.
Neurons of different sizes in the ventral nuclei project to different layers of somatic cortex in the cat
Brain Res.
(1982)

Hanker J. S., Ellis L. C., Jr., Rustioni A., Carson K.A., Reiner A., Eldred W. and Karten H. J. The ultrastructural...

HankerJ.S. et al.

A new specific, sensitive and non-carcinogenic reagent for the demonstration of horseradish peroxidase

Histochem. J.

(1977)

Iversen L. L. Identification of transmitter specific neurons in CNS by autoradiographic techniques. In Handbook of...

LandryP. et al.

Intracortical arborization and receptive fields of identified ventrobasal afferents to the primary somatic sensory cortex in the cat

J. comp. Neurol.

(1981)

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Cortical relay neurons and interneurons in the N. ventralis posterolateralis of cats: A horseradish peroxidase, electron-microscopic, golgi and immunocytochemical study

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The synaptic glomerulus and the intrinsic neuron in the dorsal laleral geniculate nucleus of the cat

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Morphology of functionally identified neurons in lateral geniculate nucleus of the cat

J. Neurophysiol.

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J. comp. Neurol.

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