Areas 3a, 3b, and 1 of Human Primary Somatosensory Cortex: 1. Microstructural Organization and Interindividual Variability

doi:10.1006/nimg.1999.0440

NeuroImage

Volume 10, Issue 1, July 1999, Pages 63-83

https://doi.org/10.1006/nimg.1999.0440 Get rights and content

Abstract

This study defines cytoarchitectonic areas 3a, 3b, and 1 of the human primary somatosensory cortex by objective delineation of cytoarchitectonic borders and ensuing cytoarchitectonic classification. This avoids subjective evaluation of microstructural differences which has so far been the only way to structurally define cortical areas. Ten brains were fixed in formalin or Bodian's fixative, embedded in paraffin, sectioned as a whole in the coronal plane at 20 μm, and cell stained. Cell bodies were segmented from the background by adaptive thresholding. Equidistant density profiles (125 μm wide, spacing 300 or 150 μm) were extracted perpendicularly to the pial surface across cortical layers II–VI and processed with multivariate statistical procedures. Positions of significant differences in shape between adjacent groups of profiles were correlated with the cytoarchitectonic pattern. Statistically significant borders can be reproduced at corresponding positions across a series of nearby sections. They match visible changes in cytoarchitecture in the cell-stained sections. Area 3a lies in the fundus of the central sulcus, and area 3b in the rostral bank of the postcentral gyrus. Area 1 lies on its crown and reaches down into the postcentral sulcus. Interareal borders, however, do not match macrostructural landmarks of the postcentral gyrus, and they considerably vary in their positions relative to these landmarks across different brains. Hence, only genuine microstructural analysis can define the borders between these cortical areas. Additional significant borders which do not correlate with visible changes in cytoarchitecture can be found within areas 3b and 1. They may represent somatotopy and/or cortical representations of different somatosensory receptors.

References (61)

C.G. Cusick et al.
Representations of the face, teeth and oral cavity in areas 3b and 1 of somatosensory cortex in squirrel monkeys
Brain Res.
(1986)
H.M. Duvernoy et al.
Cortical blood vessels of the human brain
Brain Res. Bull.
(1981)
D.J. Felleman et al.
Representations of the body surface in areas 3b and 1 of postcentral parietal cortex of cebus monkeys
Brain Res.
(1983)
Y. Iwamura et al.
Overlapping representation of fingers in the somatosensory cortex (area 2) of the conscious monkey
Brain Res.
(1980)
B. Merker
Silver staining of cell bodies by means of physical development
J. Neurosci. Methods
(1983)
P. Morosan et al.
Cytoarchitectonic mapping of cortical areas on the first transverse temporal gyrus and intersubject variability
NeuroImage
(1996)
J. Rademacher et al.
Localization and variability of cytoarchitectonic areas in the human superior temporal cortex
NeuroImage
(1996)
P.E. Roland et al.
Brain atlases—A new research tool
Trends Neurosci.
(1994)
P.E. Roland et al.
Functions and structures of the motor cortices in humans
Curr. Opin. Neurobiol.
(1996)
A. Schleicher et al.
Observer-independent method for microstructural parcellation of cerebral cortex: A quantitative approach to cytoarchitectonics
NeuroImage
(1999)

A. Wree et al.

Estimation of volume fractions in nervous tissue with an image analyzer

J. Neurosci. Methods

(1982)

K. Amunts et al.

The cytoarchitecture of Broca's region and its variability

NeuroImage

(1997)

P. Bailey et al.

The Isocortex of Man

(1951)

H. Braak

Architectonics of the Human Telencephalic Cortex

(1980)

K. Brodmann

Beiträge zur histologischen Lokalisation der Grosshirnrinde. Erste Mitteilung: Die Regio Rolandica

J. Psychol. Neurol.

(1903)

K. Brodmann

Beiträge zur histologischen Lokalisation der Grosshirnrinde. Sechste Mitteilung: Die Cortexgliederung des Menschen

J. Psychol. Neurol.

(1908)

K. Brodmann

Vergleichende Lokalisationslehre der Grosshirnrinde

(1909)

A.W. Campbell

Histological Studies on the Localization of Cerebral Function

(1905)

J. Decety et al.

Mapping motor representations with positron emission tomography

Nature

(1994)

S. Geyer et al.

Two different areas within the primary motor cortex of man

Nature

(1996)

S. Geyer et al.

Microstructure and function of the primary somatosensory cortex of man. An integrative study using cytoarchitectonic mapping and PET

NeuroImage

(1997)

S. Geyer et al.

Architectonic and receptor autoradiographic mapping of the human primary motor cortex

Hum. Brain Mapp.

(1995)

M. Hallett et al.

Involvement of primary motor cortex in motor imagery and mental practice

Behav. Brain Sci.

(1994)

Y. Iwamura et al.

Bilateral hand representation in the postcentral somatosensory cortex

Nature

(1994)

Y. Iwamura et al.

Converging patterns of finger representation and complex response properties of neurons in area 1 of the first somatosensory cortex of the conscious monkey

Exp. Brain Res.

(1983)

Y. Iwamura et al.

Functional subdivisions representing different finger regions in area 3 of the first somatosensory cortex of the conscious monkey

Exp. Brain Res.

(1983)

Y. Iwamura et al.

Diversity in receptive field properties of vertical neuronal arrays in the crown of the postcentral gyrus of the conscious monkey

Exp. Brain Res.

(1985)

Y. Iwamura et al.

Rostrocaudal gradients in the neuronal receptive field complexity in the finger region of the alert monkey's postcentral gyrus

Exp. Brain Res.

(1993)

N. Jain et al.

A histologically visible representation of the fingers and palm in primate area 3b and its immutability following long-term deafferentations

Cereb. Cortex

(1998)

J.H. Kaas et al.

Multiple representations of the body within the primary somatosensory cortex of primates

Science

(1979)

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Regular ArticleAreas 3a, 3b, and 1 of Human Primary Somatosensory Cortex: 1. Microstructural Organization and Interindividual Variability

Abstract

Brain Res.

Brain Res. Bull.

Brain Res.

Brain Res.

J. Neurosci. Methods

NeuroImage

NeuroImage

Trends Neurosci.

Curr. Opin. Neurobiol.

NeuroImage

J. Neurosci. Methods

The cytoarchitecture of Broca's region and its variability

NeuroImage

The Isocortex of Man

Architectonics of the Human Telencephalic Cortex

Beiträge zur histologischen Lokalisation der Grosshirnrinde. Erste Mitteilung: Die Regio Rolandica

J. Psychol. Neurol.

Beiträge zur histologischen Lokalisation der Grosshirnrinde. Sechste Mitteilung: Die Cortexgliederung des Menschen

J. Psychol. Neurol.

Vergleichende Lokalisationslehre der Grosshirnrinde

Histological Studies on the Localization of Cerebral Function

Mapping motor representations with positron emission tomography

Nature

Two different areas within the primary motor cortex of man

Nature

Microstructure and function of the primary somatosensory cortex of man. An integrative study using cytoarchitectonic mapping and PET

NeuroImage

Architectonic and receptor autoradiographic mapping of the human primary motor cortex

Hum. Brain Mapp.

Involvement of primary motor cortex in motor imagery and mental practice

Behav. Brain Sci.

Bilateral hand representation in the postcentral somatosensory cortex

Nature

Converging patterns of finger representation and complex response properties of neurons in area 1 of the first somatosensory cortex of the conscious monkey

Exp. Brain Res.

Functional subdivisions representing different finger regions in area 3 of the first somatosensory cortex of the conscious monkey

Exp. Brain Res.

Diversity in receptive field properties of vertical neuronal arrays in the crown of the postcentral gyrus of the conscious monkey

Exp. Brain Res.

Rostrocaudal gradients in the neuronal receptive field complexity in the finger region of the alert monkey's postcentral gyrus

Exp. Brain Res.

A histologically visible representation of the fingers and palm in primate area 3b and its immutability following long-term deafferentations

Cereb. Cortex

Multiple representations of the body within the primary somatosensory cortex of primates

Science

Regular Article
Areas 3a, 3b, and 1 of Human Primary Somatosensory Cortex: 1. Microstructural Organization and Interindividual Variability