Monoclonal antibody to glial fibrillary acidic protein reveals a parcellation of individual barrels in the early postnatal mouse somatosensory cortex

doi:10.1016/0006-8993(86)90232-5

Brain Research

Volume 380, Issue 2, 20 August 1986, Pages 341-348

https://doi.org/10.1016/0006-8993(86)90232-5 Get rights and content

Abstract

The relative dispositions of cells in immature and mature barrel field cortices that bind antibody to glial fibrillary acidic protein (GFAP) were examined and photographed under the light microscope. Light micrographs demonstrate that radially oriented glial cells are present in the barrel field of postnatal day 6 cortices and that they are located predominantly within the presumptive barrel sides and/or septae, thus sharply delineating individual barrels from each other. The relative dispositions of radial glial fibers observed at this time implicate glia in development of topographic order during early postnatal development of the somatosensory cortex. In contrast, no such delineation could be detected in the cortices of more mature mice, because GFAP-positive astrocytes are present throughout the barrel field and are not confined to barrel sides. This ephemeral nature of the GFAP-delineated barrel field is of interest with respect to the recently reported ephemeral lectin-delineated barrel field.

References (31)

BurgessS.K. et al.
Autoradiographic quantitation of β-adrenergic receptors on neural cells in primary cultures. II. Comparison of receptors on various types of immunocytochemically identified cells
Brain Research
(1985)
JeanmonodD. et al.
Mouse somatosensory cortex: alterations in the barrelfield following receptor injury at different early postnatal ages
Neuroscience
(1981)
LidovH.G.W. et al.
The organization of the catecholamine innervation of somatosensory cortex: the barrel field of the mouse
Brain Research
(1978)
WeltC. et al.
Somatosensory cortical barrels and thalamic barreloids in reeler mutant mice
Neuroscience
(1977)
WhiteE.L.
Ultrastructure and synaptic contacts in barrels of mouse S1 cortex
Brain Research
(1976)
WilsonC.J. et al.
A simple and rapid section embedding technique for sequential light and electron microscopic examination of individually stained central neurons
J. Neurosci. Meth.
(1979)
WoolseyT.A. et al.
The structural organization of layer IV in the somatosensory region (S1) of the mouse cerebral cortex: the description of a cortical field composed of discrete cytoarchitectonic units
Brain Research
(1970)
CooperN.G.F. et al.
Lectin binding sites in the postnatal mouse cerebral cortex: ephemeral appearance of the barrel field
Soc. Neurosci. Abstr.
(1985)
Cooper, N.G.F. and Steindler, D.A., Lectins demarcate the barrel subfield in the somatosensory cortex of the early...
CurcioC.A. et al.
Stability of neuron number in cortical barrels of aging mice
J. Comp. Neurol.
(1982)

CusickC.G. et al.

Corticocortical and collateral thalamocortical connections of postcentral somatosensory cortical areas in squirrel monkeys: a double-labeling study with radiolabeled wheat germ agglutinin and what germ agglutinin conjugated to horseradish peroxidase

Somatosens. Res.

(1985)

GrahamR.C.J. et al.

The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique

J. Histochem. Cytochem.

(1966)

KillackeyH.P. et al.

The formation of afferent patterns in the somatosensory cortex of the neonatal rat

J. Comp. Neurol.

(1979)

NobleM. et al.

Glia are a unique substrate for the in vitro growth of central nervous system neurons

J. Neurosci.

(1984)

RakicP.

Mode of cell migration to the superfacial layers of fetal monkey neocortex

J. Comp. Neurol.

(1972)

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Glia help determine and modulate the physical structure of the neuronal connectome. Astrocytes form barriers to neuronal connectivity (Cooper and Steindler, 1986), guide neurite outgrowth (Kanemaru et al., 2007), modulate volume transmission within the extracellular space (Nicholson and Syková, 1998), and moderate structural dynamics of dendritic spines (Nishida and Okabe, 2007). Astrocytes stimulate synaptogenesis (Eroglu et al., 2009; Allen et al., 2012) and remove synapses (Tasdemir-Yilmaz and Freeman, 2014).
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Furthermore, using NG2 knockout mice we demonstrated that NG2 CSPG expression in the cortex is not necessary for normal barrel development. Extracellular and cell surface CSPGs were initially found to be elevated in the barrel septa compared to barrel hollows (Cooper and Steindler 1986a) coincident with preferential distribution of GFAP+ astrocytes in the barrel septa (Cooper and Steindler 1986b). This observation suggested that these axon growth inhibitory molecules might play a role in the formation of the whisker pattern in the cortex by guiding the thalamocortical axons (TCAs) into the corresponding barrel hollow and preventing them from crossing into adjacent barrels.
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Monoclonal antibody to glial fibrillary acidic protein reveals a parcellation of individual barrels in the early postnatal mouse somatosensory cortex

Abstract

Brain Research

Neuroscience

Brain Research

Neuroscience

Brain Research

J. Neurosci. Meth.

Brain Research

Lectin binding sites in the postnatal mouse cerebral cortex: ephemeral appearance of the barrel field

Soc. Neurosci. Abstr.

Stability of neuron number in cortical barrels of aging mice

J. Comp. Neurol.

Corticocortical and collateral thalamocortical connections of postcentral somatosensory cortical areas in squirrel monkeys: a double-labeling study with radiolabeled wheat germ agglutinin and what germ agglutinin conjugated to horseradish peroxidase

Somatosens. Res.

The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique

J. Histochem. Cytochem.

The formation of afferent patterns in the somatosensory cortex of the neonatal rat

J. Comp. Neurol.

Glia are a unique substrate for the in vitro growth of central nervous system neurons

J. Neurosci.

Mode of cell migration to the superfacial layers of fetal monkey neocortex

J. Comp. Neurol.