A voltage-gated potassium channel, Kv3.1b, is expressed by a subpopulation of large pyramidal neurons in layer 5 of the macaque monkey cortex

doi:10.1016/j.neuroscience.2004.08.005

Neuroscience

Volume 129, Issue 1, 2004, Pages 179-185

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Abstract

In the cerebral cortex, the voltage-gated potassium channel, Kv3.1b, a splicing variant of Kv3.1, has been associated with fast-firing interneurons. Here, we report strong expression of Kv3.1b-protein and mRNA in both Betz and Meynert pyramidal cells of the monkey, as shown by immunohistochemistry and in situ hybridization. Strong expression also occurs in large pyramidal neurons in layer 5 of several cortical areas. In addition, most of these Betz and layer 5 pyramids, and about 10% of the labeled Meynert cells weakly co-expressed the calcium binding protein parvalbumin. Electron microscopy shows that the expression of Kv3.1b is localized to the somal and proximal dendritic cytoplasmic membrane, as expected for a channel protein. These results suggest that some large pyramidal neurons may constitute a functional subpopulation, with a distinctive distribution of voltage-gated potassium channels capable of influencing their repetitive firing properties.

Section snippets

Perfusion and tissue preparation

Six adult macaque monkeys (Macaca mulatta and Macaca fuscata) were used in this study. All experimental protocols were approved by the Experimental Animal Committee of the RIKEN Institute, and were carried out in accordance with the National Institutes of Health Guide for the Care and Use of Laboratory Animals (NIH Publication No. 80–23; revised 1996). Every effort was made to minimize the number of animals used and any pain or discomfort. Animals were anesthetized with ketamine (11 mg/kg,

Results

Inspection of cortical areas after immunohistochemistry for Kv3.1b protein revealed abundant non-pyramidally shaped neurons through layers 2–6, with some in layer 1 as well. Their distribution, quantity, and shape together suggest that these are GABAergic interneurons, consistent with previous reports in rodents (Weiser et al., 1995; Sekirnjak et al., 1997). In addition, several pyramidal cell populations were strongly Kv3.1b-ir.

In layer 5 of primary motor cortex, large pyramidal neurons

Discussion

Our results show that Kv3.1b, both in its protein and mRNA, is strongly expressed in a subpopulation of large infragranular pyramidal neurons in the monkey cortex. EM study of Betz and Meynert cells further determines that the Kv3.1b protein is preferentially associated with the somal and proximal dendritic membranes, as expected for a channel protein. The strong expression of Kv3.1b in large infragranular pyramidal neurons raises the possibility that this group of cells has distinct

Acknowledgments

This work was supported by the Brain Science Institute, RIKEN, and by the NIBB Cooperative Research Program for gene expression and regulation (4-602). The authors would like to thank Ms Miyoko Bellinger, Ms Kyoko Shirasawa, Ms Yoshiko Abe, Ms Hiromi Mashiko and Mr. Adrian Knight for their excellent technical assistance; and Ms Hiroko Katsuno for elegant electron microscopic work.

References (50)

J. DeFelipe et al.
The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs
Prog Neurobiol
(1992)
W. Hartig et al.
Cortical neurons immunoreactive for the potassium channel Kv3.1b subunit are predominantly surrounded by perineuronal nets presumed as a buffering system for cations
Brain Res
(1999)
G. Leuba et al.
Colocalization of parvalbumin, calretinin and calbindin D-28k in human cortical and subcortical visual structures
J Chem Neuroanat
(1997)
H. Li et al.
Intrinsic collaterals of layer 6 Meynert cells and functional columns in primate V1
Neuroscience
(2003)
M. Matelli et al.
Patterns of cytochrome oxidase activity in the frontal agranular cortex of the macaque monkey
Behav Brain Res
(1985)
B.R. Payne et al.
Cytochrome oxidase patches and Meynert cells in monkey visual cortex
Neuroscience
(1989)
T.M. Preuss et al.
Parvalbumin-like immunoreactivity of layer V pyramidal cells in the motor and somatosensory cortex of adult primates
Brain Res
(1996)
B. Rudy et al.
Kv3 channels: voltage-gated K⁺ channels designed for high-frequency repetitive firing
Trends Neurosci
(2001)
C. Sekirnjak et al.
Subcellular localization of the K⁺ channel subunit Kv3.1b in selected rat CNS neurons
Brain Res
(1997)
S. Tominaga et al.
Immunocytochemical localization of alpha-, beta I-, beta II- and gamma-subspecies of protein kinase C in the motor and premotor cortices of the rhesus monkey
Neurosci Res
(1993)

A. Yamashita et al.

Axon trajectories in local circuits of the primary motor cortex in the macaque monkey (Macaca fuscata)

Neurosci Res

(2001)

G. Ugolini et al.

Collaterals of corticospinal and pyramidal fibres to the pontine grey demonstrated by a new application of the fluorescent fibre labelling technique

Brain Res

(1986)

G. Baranauskas et al.

Kv3.4 subunits enhance the repolarizing efficiency of Kv3.1 channels in fast-spiking neurons

Nat Neurosci

(2003)

A. Bertolotto et al.

Chondroitin sulfate proteoglycan surrounds a subset of human and rat CNS neurons

J Neurosci Res

(1991)

K. Brodmann

Vergleichende Lokalisationslehre der Grosshirnrinde

(1909)

E.W. Carroll et al.

Quantitative light and electron microscopic analysis of cytochrome oxidase-rich zones in the striate cortex of the squirrel monkey

J Comp Neurol

(1984)

V. Chan-Palay et al.

Meynert cells in the primate visual cortex

J Neurocytol

(1974)

Y. Chagnac-Amitai et al.

Burst generating and regular spiking layer 5 pyramidal neurons of rat neocortex have different morphological features

J Comp Neurol

(1990)

B.W. Connors et al.

Electrophysiological properties of neocortical neurons in vitro

J Neurophysiol

(1982)

E.A. DeYoe et al.

Antibody labeling of functional subdivisions in visual cortex: Cat-301 immunoreactivity in striate and extrastriate cortex of the macaque monkey

Vis Neurosci

(1990)

R. Douglas et al.

Neocortex

E.V. Evarts

Relation of discharge frequency to conduction velocity in pyramidal tract neurons

J Neurophysiol

(1965)

L. Gan et al.

When, where, and how much? Expression of the Kv3.potassium channel in high-frequency firing neurons

J Neurobiol

(1998)

M. Glickstein et al.

Corticopontine projection in the macaque: the distribution of labelled cortical cells after large injections of horseradish peroxidase in the pontine nuclei

J Comp Neurol

(1985)

M.P. Galea et al.

Multiple corticospinal neuron populations in the macaque monkey are specified by their unique cortical origins, spinal terminations, and connections

Cereb Cortex

(1994)

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A voltage-gated potassium channel, Kv3.1b, is expressed by a subpopulation of large pyramidal neurons in layer 5 of the macaque monkey cortex

Abstract

Section snippets

Perfusion and tissue preparation

Results

Discussion

Acknowledgments

Prog Neurobiol

Brain Res

J Chem Neuroanat

Neuroscience

Behav Brain Res

Neuroscience

Brain Res

Trends Neurosci

Brain Res

Neurosci Res

Neurosci Res

Brain Res

Kv3.4 subunits enhance the repolarizing efficiency of Kv3.1 channels in fast-spiking neurons

Nat Neurosci

Chondroitin sulfate proteoglycan surrounds a subset of human and rat CNS neurons

J Neurosci Res

Vergleichende Lokalisationslehre der Grosshirnrinde

Quantitative light and electron microscopic analysis of cytochrome oxidase-rich zones in the striate cortex of the squirrel monkey

J Comp Neurol

Meynert cells in the primate visual cortex

J Neurocytol

Burst generating and regular spiking layer 5 pyramidal neurons of rat neocortex have different morphological features

J Comp Neurol

Electrophysiological properties of neocortical neurons in vitro

J Neurophysiol

Antibody labeling of functional subdivisions in visual cortex: Cat-301 immunoreactivity in striate and extrastriate cortex of the macaque monkey

Vis Neurosci

Neocortex

Relation of discharge frequency to conduction velocity in pyramidal tract neurons

J Neurophysiol

When, where, and how much? Expression of the Kv3.potassium channel in high-frequency firing neurons

J Neurobiol

Corticopontine projection in the macaque: the distribution of labelled cortical cells after large injections of horseradish peroxidase in the pontine nuclei

J Comp Neurol

Multiple corticospinal neuron populations in the macaque monkey are specified by their unique cortical origins, spinal terminations, and connections

Cereb Cortex