Neurochemical phenotype of corticocortical connections in the macaque monkey: Quantitative analysis of a subset of neurofilament protein‐immunoreactive projection neurons in frontal, parietal, temporal, and cingulate cortices

Patrick R. Hof, Esther A. Nimchinsky, John Morrison

Research output: Contribution to journalArticle

131 Citations (Scopus)

Abstract

The neurochemical characteristics of the neuronal subsets that furnish different types of corticocortical connections have been only partially determined. In recent years, several cytoskeletal proteins have emerged as reliable markers to distinguish subsets of pyramidal neurons in the cerebral cortex of primates. In particular, previous studies using an antibody to nonphosphorylated neurofilament protein (SMI‐32) have revealed a consistent degree of regional and laminar specificity in the distribution of a subpopulation of pyramidal cells in the primate cerebral cortex. The density of neurofilament protein‐immunoreactive neurons was shown to vary across corticocortical pathways in macaque monkeys. In the present study, we have used the antibody SMI‐32 to examine further and to quantify the distribution of a subset of corticocortically projecting neurons in a series of long ipsilateral corticocortical pathways in comparison to short corticocortical, commissural, and limbic connections. The results demonstrate that the long association pathways interconnecting the frontal, parietal, and temporal neocortex have a high representation of neurofilament protein‐enriched pyramidal neurons (45–90%), whereas short corticocortical, callosal, and limbic pathways are characterized by much lower numbers of such neurons (4–35%). These data suggest that different types of corticocortical connections have differential representation of highly specific neuronal subsets that share common neurochemical characteristics, thereby determining regional and laminar cortical patterns of morphological and molecular heterogeneity. These differences in neuronal neurochernical phenotype among corticocortical circuits may have considerable influence on cortical processing and may be directly related to the type of integrative function subserved by each cortical pathway. Finally, it is worth noting that neurofilainent protein‐immunoreactive neurons are dramatically affected in the course of Alzheimer's disease. The present results support the hypothesis that neurofilament protein may be crucially linked to the development of selective neuronal vulnerability and subsequent disruption of corticocortical pathways that lead to the severe impairment of cognitive function commonly observed in age‐related dementing disorders. © Wiley‐Liss, Inc.

Original languageEnglish (US)
Pages (from-to)109-133
Number of pages25
JournalJournal of Comparative Neurology
Volume362
Issue number1
DOIs
StatePublished - Jan 1 1995
Externally publishedYes

Fingerprint

Parietal Lobe
Intermediate Filaments
Gyrus Cinguli
Macaca
Frontal Lobe
Temporal Lobe
Haplorhini
Pyramidal Cells
Neurofilament Proteins
Phenotype
Neurons
Cerebral Cortex
Primates
Cytoskeletal Proteins
Antibodies
Corpus Callosum
Neocortex
Cognition
Alzheimer Disease

Keywords

  • association cortex
  • cytoskeleton
  • neocortex
  • parallel distributed systems
  • pyramidal neurons

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

@article{d0760db40c244c12b258e408c66867b3,
title = "Neurochemical phenotype of corticocortical connections in the macaque monkey: Quantitative analysis of a subset of neurofilament protein‐immunoreactive projection neurons in frontal, parietal, temporal, and cingulate cortices",
abstract = "The neurochemical characteristics of the neuronal subsets that furnish different types of corticocortical connections have been only partially determined. In recent years, several cytoskeletal proteins have emerged as reliable markers to distinguish subsets of pyramidal neurons in the cerebral cortex of primates. In particular, previous studies using an antibody to nonphosphorylated neurofilament protein (SMI‐32) have revealed a consistent degree of regional and laminar specificity in the distribution of a subpopulation of pyramidal cells in the primate cerebral cortex. The density of neurofilament protein‐immunoreactive neurons was shown to vary across corticocortical pathways in macaque monkeys. In the present study, we have used the antibody SMI‐32 to examine further and to quantify the distribution of a subset of corticocortically projecting neurons in a series of long ipsilateral corticocortical pathways in comparison to short corticocortical, commissural, and limbic connections. The results demonstrate that the long association pathways interconnecting the frontal, parietal, and temporal neocortex have a high representation of neurofilament protein‐enriched pyramidal neurons (45–90{\%}), whereas short corticocortical, callosal, and limbic pathways are characterized by much lower numbers of such neurons (4–35{\%}). These data suggest that different types of corticocortical connections have differential representation of highly specific neuronal subsets that share common neurochemical characteristics, thereby determining regional and laminar cortical patterns of morphological and molecular heterogeneity. These differences in neuronal neurochernical phenotype among corticocortical circuits may have considerable influence on cortical processing and may be directly related to the type of integrative function subserved by each cortical pathway. Finally, it is worth noting that neurofilainent protein‐immunoreactive neurons are dramatically affected in the course of Alzheimer's disease. The present results support the hypothesis that neurofilament protein may be crucially linked to the development of selective neuronal vulnerability and subsequent disruption of corticocortical pathways that lead to the severe impairment of cognitive function commonly observed in age‐related dementing disorders. {\circledC} Wiley‐Liss, Inc.",
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author = "Hof, {Patrick R.} and Nimchinsky, {Esther A.} and John Morrison",
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T2 - Quantitative analysis of a subset of neurofilament protein‐immunoreactive projection neurons in frontal, parietal, temporal, and cingulate cortices

AU - Hof, Patrick R.

AU - Nimchinsky, Esther A.

AU - Morrison, John

PY - 1995/1/1

Y1 - 1995/1/1

N2 - The neurochemical characteristics of the neuronal subsets that furnish different types of corticocortical connections have been only partially determined. In recent years, several cytoskeletal proteins have emerged as reliable markers to distinguish subsets of pyramidal neurons in the cerebral cortex of primates. In particular, previous studies using an antibody to nonphosphorylated neurofilament protein (SMI‐32) have revealed a consistent degree of regional and laminar specificity in the distribution of a subpopulation of pyramidal cells in the primate cerebral cortex. The density of neurofilament protein‐immunoreactive neurons was shown to vary across corticocortical pathways in macaque monkeys. In the present study, we have used the antibody SMI‐32 to examine further and to quantify the distribution of a subset of corticocortically projecting neurons in a series of long ipsilateral corticocortical pathways in comparison to short corticocortical, commissural, and limbic connections. The results demonstrate that the long association pathways interconnecting the frontal, parietal, and temporal neocortex have a high representation of neurofilament protein‐enriched pyramidal neurons (45–90%), whereas short corticocortical, callosal, and limbic pathways are characterized by much lower numbers of such neurons (4–35%). These data suggest that different types of corticocortical connections have differential representation of highly specific neuronal subsets that share common neurochemical characteristics, thereby determining regional and laminar cortical patterns of morphological and molecular heterogeneity. These differences in neuronal neurochernical phenotype among corticocortical circuits may have considerable influence on cortical processing and may be directly related to the type of integrative function subserved by each cortical pathway. Finally, it is worth noting that neurofilainent protein‐immunoreactive neurons are dramatically affected in the course of Alzheimer's disease. The present results support the hypothesis that neurofilament protein may be crucially linked to the development of selective neuronal vulnerability and subsequent disruption of corticocortical pathways that lead to the severe impairment of cognitive function commonly observed in age‐related dementing disorders. © Wiley‐Liss, Inc.

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