Laminar Distribution of Fos/Calcium-Binding Protein and Fos/Neurofilament Protein-Labeled Neurons in Rat Motor and Sensory Cortex after Picrotoxin-Induced Seizures

doi:10.1006/exnr.1997.6744

Experimental Neurology

Volume 149, Issue 2, February 1998, Pages 373-383

https://doi.org/10.1006/exnr.1997.6744 Get rights and content

Abstract

Cerebrocortical Fos induction after picrotoxin-induced seizure occurs in spiny neurons and, to a lesser extent, in neurons defined by calcium-binding protein immunoreactivity. In motor and sensory cortex of rats we have defined the laminar distribution of Fos expression in these neurons. Initially we defined the laminar distributions of parvalbumin-, calbindin-D 28K-, and calretinin-immunoreactive aspiny neurons; these were unique for each class and similar across cortical regions. Spiny cells defined by SMI32 immunoreactivity were distributed with two peaks and there were differences between cortical regions. Parvalbumin-immunoreactive neurons exhibited peak numbers where numbers of SMI32-immunoreactive neurons were low. The distribution of Fos induction across laminae matched that of its class for calbindin-D 28K and calretinin neurons; however, Fos induction was less in infragranular compared with supragranular for parvalbumin in motor cortex and SMI32 containing neurons in both cortices. In both these latter cell classes Fos induction was inversely correlated with neuronal size. It is suggested that cell size within some cell classes is one factor that determines the extent of Fos induction within that class following seizures.

References (36)

Y. Ben-Ari et al.
Electrographic, clinical and pathological alterations following systemic administration of kainic acid, bicuculline or pentetrazole: Metabolic mapping using the deoxyglucose method with special reference to the pathology of epilepsy
Neuroscience
(1981)
E. Bullitt et al.
The effect of stimulus duration on noxious-stimulus induced c-fos expression in the rodent spinal cord
Brain Res.
(1992)
M.J. Campbell et al.
A subpopulation of primate corticocortical neurons is distinguished by somatodendritic distribution of neurofilament protein
Brain Res.
(1991)
M.R. Celio
Calbindin D-28k and parvalbumin in the rat nervous system
Neuroscience
(1990)
J. Defelipe et al.
The pyramidal neuron of the cerebral cortex: Morphological and chemical characteristics of the synaptic inputs
Prog. Neurobiol.
(1992)
H. Demeulemeester et al.
Calbindin D-28k and parvalbumin immunoreactivity is confined to two separate neuronal subpopulations in the cat visual cortex, whereas partial coexistence is shown in the dorsal lateral geniculate nucleus
Neurosci. Lett.
(1989)
P. Gass et al.
Induction of immediate early gene encoded proteins in the rat hippocampus after bicuculline-induced seizures: Differential expression of krox-24, fos and jun proteins
Neuroscience
(1992)
J.J. Hiscock et al.
Fos induction in subtypes of cerebrocortical neurons in rat after picrotoxin-induced seizures
Brain Res.
(1996)
K.J. Jeffery et al.
Induction of Fos-like immunoreactivity and the maintenance of long-term potentiation in the dentate gyrus of unanesthetized rats
Mol. Brain Res.
(1990)
P. Lanaud et al.
Temporal and spatial patterns of expression of c-fos, zif/268, c-jun and jun-B mRNAs in the rat brain following seizures evoked focally from the deep prepiriform cortex
Exp. Neurol.
(1993)

I.J. Llewellyn-Smith et al.

Retrograde tracing with cholera toxin B-gold or with immunocytochemically detected cholera toxin B in central nervous system

Methods Neurosci.

(1992)

W. Loscher et al.

Which animal models should be used in the search for new antiepileptic drugs? A proposal based on experimental and clinical considerations

Epilepsy Res.

(1988)

A. Medvedev et al.

Frontal cortex leads other brain structures in generalised spike-and-wave spindles and seizure spikes induced by picrotoxin

Electroenceph. Clin. Neurophysiol.

(1996)

J.I. Morgan et al.

Proto-oncogene transcription factors and epilepsy

TiPS

(1991)

J.H. Morrison et al.

A monoclonal antibody to non-phosphorylated neurofilament protein marks the vulnerable cortical neurons in Alzheimer's disease

Brain Res.

(1987)

A. Resibois et al.

Calretinin in rat brain: An immunohistochemical study

Neuroscience

(1992)

J.H. Rogers

Immunohistochemical markers in rat cortex: co-localization of calretinin and calbindin-D28k with neuropeptides and GABA

Brain Res.

(1992)

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Light-induced Fos expression in phosphate-activated glutaminase- and neurofilament protein-immunoreactive neurons in cat primary visual cortex
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Previous double-stainings in the cat visual cortex [E. Van der Gucht, S. Clerens, K. Cromphout, F. Vandesande, L. Arckens, Differential expression of c-fos in subtypes of GABAergic cells following sensory stimulation in the cat primary visual cortex, Eur. J. Neurosci. 16 (2002) 1620–1626] showed that a minority of Fos-immunoreactive nuclei was located in distinct subclasses of inhibitory neurons following sensory stimulation. This report describes double-stainings between Fos and phosphate-activated glutaminase (PAG) or Fos and neurofilament protein (SMI-32) revealing that, following a short-term visual experience, Fos is also expressed in neurochemically distinct subpopulations of non-GABAergic, pyramidal neurons in supra- and infragranular layers of cat area 17.
The effect on motor cortical neuronal development of focal lesions to the sub-cortical white matter in the neonatal rat: A model for periventricular leukomalacia
2003, International Journal of Developmental Neuroscience
Citation Excerpt :
They also participate in the dynamic properties of the axonal cytoskeleton during neuronal differentiation, axon outgrowth and guidance (Nixon and Shea, 1992). In the mature neocortex SMI-32, antibodies label a sub-population of pyramidal cells that contain the non-phosphorylated neurofilament triplet protein (Hiscock and Mackenzie, 1998). The monoclonal antibody SMI-32 recognises an epitope present in neurofilaments in the non-phosphorylated state and visualises neuronal cell bodies, dendrites and some thick axons (Sternberger and Sternberger, 1983).
Periventricular leukomalacia (PVL) is either a diffuse or cystic lesion of the periventricular white matter that leaves the overlying cortical grey matter largely intact. It is believed to result from hypoxia occurring pre- or perinatally and is a major cause of cerebral palsy. We have modelled PVL in rats comparing the effects of discrete injections of 3-nitropropionic acid (3-NP), a mitochondrial toxin, ibotenic acid (IBA), a glutamate analogue, or saline into the sub-cortical white matter on postnatal day 7 (P7). Following recovery times ranging from 3 days to 4 weeks, forebrain sections were Nissl stained or immunostained for Bax, cJun, calbindin (CB), parvalbumin (PV) or non-phosphorylated neurofilaments (NPNF). Compared to saline injections, ibotenic acid caused large lesions of both grey and white matter not characteristic of periventricular leukomalacia. 3-Nitropropionic acid injections caused small focal lesions restricted to the sub-cortical white matter. 3-Nitropropionic acid treatment initially increased expression of the apoptosis promoting proteins Bax and cJun, as well as non-phosphorylated neurofilaments in cortical layer V overlying the injection site. Non-phosphorylated neurofilament expression distal to the lesion was decreased representing a loss of cortical axons, but persisted and even increased with time within the cortex, demonstrating persistence of the parent cell bodies and local sprouting of neurites. There were significantly fewer calbindin and parvalbumin positive neurones in the motor cortex (MC) side ipsilateral to the 3-nitropropionic acid injection compared to the contralateral side. These persistent differences in expression of activity sensitive calcium binding proteins suggest alterations in local cortical circuitry without substantial loss of grey matter as is characteristic of periventricular leukomalacia. Changes in expression of Bax, cJun and non-phosphorylated neurofilaments during normal development are also described.
Fos induction in cortical interneurons during spontaneous wakefulness of rats in a familiar or enriched environment
2002, Brain Research Bulletin
Citation Excerpt :
The present study demonstrates that in animals examined at the end of a period of wakefulness in a familiar environment Fos is induced in a minor proportion of local circuit neurons that express Pv or Cb in the parietal cortex, whereas no Fos induction was found in Cb- or Pv-positive interneurons of the cingulate cortex. Our data on Fos induction in cortical inhibitory cells during relatively “quiet” wakefulness are in line with previous evidence, obtained in different experimental paradigms of cortical activation such as epilepsy [10,14] and thalamic stimulation [2], demonstrating c-fos induction in relatively small proportions of cortical interneurons, as defined by their colocalization with calcium-binding proteins. In the animals that had been exposed to an enriched environment, however, Fos induction was detected in a much higher number of cortical neurons than in the behaviorally unstimulated cases.
It has been repeatedly reported that Fos is spontaneously induced in several brain structures, including the cerebral cortex, during wakefulness. To ascertain whether cortical interneurons are involved in this state-dependent oscillation of gene regulation, we combined Fos immunocytochemistry with immunostaining of either parvalbumin or calbindin, known markers of cortical interneurons. Immunopositive neurons were examined in the sensorimotor and cingulate cortex. In rats perfused in basal conditions, a minor proportion (around 8%) of Fos-immunoreactive neurons in the parietal cortex were also parvalbumin- or calbindin-immunoreactive; these double immunostained cells accounted for 13% of the parvalbumin- and 34% of the calbindin-labeled neurons. Colocalization of Fos with either calcium-binding protein was instead not observed in the cingulate cortex. In rats stimulated by novel environmental cues during the period of wakefulness preceding perfusion, Fos-positive neurons increased markedly relative to unstimulated animals, and involved the majority of the calbindin- or parvalbumin-labeled cell populations (60–75% and over 95%, respectively). In the neuronal populations in which Fos was induced by exposure to the enriched environment, the proportion of calbindin- and parvalbumin-labeled cells was larger than in the unstimulated cases, and the increment was statistically significant in the cingulate cortex. The results demonstrate that Fos induction occurring in the cortex during undisturbed wakefulness in a familiar environment involves a minor proportion of interneurons. Furthermore, the findings indicate that the addition of novel environmental stimuli results in an increase of Fos-expressing neurons whose recruitment, at least in the cingulate cortex, involves a higher proportion of interneurons than of projection neurons.
Excitatory and inhibitory neurons express c-Fos in barrel-related columns after exploration of a novel environment
2002, Neuroscience
Recent work has shown that behaviorally meaningful sensory information processing is accompanied by the induction of several transcription factors in the barrel cortex of rodents. It is now generally accepted that stimulus–transcription coupling is an important step in the sequence of events leading to long-term plastic changes in neuronal structure and function. Nevertheless, so far few data are available as to what types of neurons are involved in such a genomic response. Here, we determined the morphological and neurochemical identity of neurons in rat barrel cortex showing a c-Fos-immunoreactive nucleus after exploration of an enriched environment. Double stainings of c-Fos and glial fibrillary acidic protein excluded astrocytes as a possible cell type expressing this transcription factor. By morphological phenotyping with intracellular Lucifer Yellow injections, it was found that a large majority were probably excitatory pyramidal cells, but inhibitory interneurons were also found to contain c-Fos-immunoreactive nuclei. By neurochemical phenotyping of GABAergic interneurons with specific antibodies, a significant induction was found, in a layer-dependent manner, for the populations of glutamic acid decarboxylase-, parvalbumin-, calbindin- and vasoactive intestinal polypeptide-immunoreactive neurons but not for calretinin-immunoreactive cells in experimental compared to control columns.
From these data we conclude that thalamic afferents effectively drive cortical excitatory as well as inhibitory intracortical circuits. Thus, the adaptations of receptive field properties of cortical neurons after different manipulations of the sensory periphery are likely to be caused by plastic changes in excitatory and inhibitory networks.
Theta-burst transcranial magnetic stimulation alters cortical inhibition
2011, Journal of Neuroscience
Immediate-early gene expression in the barrel cortex
2006, Somatosensory and Motor Research

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Regular ArticleLaminar Distribution of Fos/Calcium-Binding Protein and Fos/Neurofilament Protein-Labeled Neurons in Rat Motor and Sensory Cortex after Picrotoxin-Induced Seizures

Abstract

Neuroscience

Brain Res.

Brain Res.

Neuroscience

Prog. Neurobiol.

Neurosci. Lett.

Neuroscience

Brain Res.

Mol. Brain Res.

Exp. Neurol.

Methods Neurosci.

Epilepsy Res.

Electroenceph. Clin. Neurophysiol.

TiPS

Brain Res.

Neuroscience

Brain Res.

Regular Article
Laminar Distribution of Fos/Calcium-Binding Protein and Fos/Neurofilament Protein-Labeled Neurons in Rat Motor and Sensory Cortex after Picrotoxin-Induced Seizures