Late appearance of parvalbumin-immunoreactive neurons in the rodent cerebral cortex does not follow an ‘inside-out’ sequence

doi:10.1016/0304-3940(92)90360-J

Neuroscience Letters

Volume 142, Issue 2, 17 August 1992, Pages 147-150

https://doi.org/10.1016/0304-3940(92)90360-J Get rights and content

Abstract

Parvalbumin (PARV), a Ca²⁺-binding protein believed to play a role in neuronal excitability, is contained in certain GABAergic inhibitory neurons of the cerebral cortex. Here we report that expression of PARV in the developing neocortex of rats and mice occurs with a sequence which does not follow the usual ‘inside-out’ gradient of cortical development. Thus, PARV-immunoreactive neurons appear first in layer V and only thereafter in the remaining cortical layers. An adult-like pattern of immunoreactivity is reached simultaneously in layers II–III and VIb. These observations indicate that the mechanisms regulating the functional maturation of PARV-containing inhibitory neurons are different from those that generally govern developmental processes in the cortex.

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Doublecortin expression in adult cat and primate cerebral cortex relates to immature neurons that develop into GABAergic subgroups
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DCX-immunoreactive (DCX+) cells occur in the piriform cortex in adult mice and rats, but also in the neocortex in adult guinea pigs and rabbits. Here we describe these cells in adult domestic cats and primates. In cats and rhesus monkeys, DCX+ cells existed across the allo- and neocortex, with an overall ventrodorsal high to low gradient at a given frontal plane. Labeled cells formed a cellular band in layers II and upper III, exhibiting dramatic differences in somal size (5–20 μm), shape (unipolar, bipolar, multipolar and irregular), neuritic complexity and labeling intensity. Cell clusters were also seen in this band, and those in the entorhinal cortex extended into deeper layers as chain-like structures. Densitometry revealed a parallel decline of the cells across regions with age in cats. Besides the cellular band, medium-sized cells with weak DCX reactivity resided sparsely in other layers. Throughout the cortex, virtually all DCX+ cells co-expressed polysialylated neural cell adhesion molecule. Medium to large mature-looking DCX+ cells frequently colocalized with neuron-specific nuclear protein and γ-aminobutyric acid (GABA), and those with a reduced DCX expression also partially co-labeled for glutamic acid decarboxylase, parvalbumin, calbindin, β-nicotinamide adenine dinucleotide phosphate diaphorase and neuronal nitric oxide synthase. Similar to cats and monkeys, small and larger DCX+ cells were detected in surgically removed human frontal and temporal cortices. These data suggest that immature neurons persist into adulthood in many cortical areas in cats and primates, and that these cells appear to undergo development and differentiation to become functional subgroups of GABAergic interneurons.
Doublecortin-expressing cells are present in layer II across the adult guinea pig cerebral cortex: Partial colocalization with mature interneuron markers
2008, Experimental Neurology
Doublecortin-immunoreactive (DCX+) cells were detected across the allo- and neo-cortical regions in the adult guinea pig cerebrum, localized to layer II specifically at its border with layer I. The density of labeled cells declined with age, whereas no apparent apoptotic activity was detectable over the cortex including layer II. DCX+ cells varied in somal size, labeling intensity, nuclear appearance, and complexity of processes. These cells were often arranged in clusters with cells of similar morphology sometimes packed tightly together. They exhibited complete colocalization with polysialylated neural cell adhesion molecule (PSA-NCAM) and neuron-specific type III β-tubulin (TuJ1). Medium to large-sized DCX+ cells had well-developed neuritic processes, and expressed neuron-specific nuclear protein (NeuN). Large mature-looking cells with weak DCX reactivity invariably displayed heavy NeuN reactivity, implicating a transitional stage of these labeled cells. These “transitional” cells also consistently exhibited weak reactivity for γ-aminobutyric acid (GABA), glutamate decarboxylase (GAD67), β-nicotinamide adenine dinucleotide phosphate diaphorase (NADPH-d) and neuronal nitric oxide synthase (nNOS), suggestive of them being young GABAergic/nitrinergic interneurons. Our data indicate that DCX+ cells exist widely in the adult guinea pig cerebral cortex, with a predominant localization in upper layer II. The morphological variation and differential expression of neuronal markers in these cells implicate that they might be developing neurons, and that they are probably differentiating into GABAergic interneurons. This population of cells might be involved in interneuron plasticity in the adult mammalian cerebral cortex.
Recruitment of Parvalbumin-Positive Interneurons Determines Hippocampal Function and Associated Behavior
2007, Neuron
Citation Excerpt :
In GluR-APVCre−/− mice, a reduction of the AMPA current is expected to occur only at later developmental stages for two reasons. First, Cre recombinase is not expressed before the second postnatal week since it is under control of the parvalbumin promoter (Solbach and Celio, 1991; Soriano et al., 1992). Second, some time is required before Cre-mediated recombination occurs in both GluR-A alleles.
Perisomatic inhibition provided by a subgroup of GABAergic interneurons plays a critical role in timing the output of pyramidal cells. To test their contribution at the network and the behavioral level, we generated genetically modified mice in which the excitatory drive was selectively reduced either by the knockout of the GluR-D or by conditional ablation of the GluR-A subunit in parvalbumin-positive cells. Comparable cell type-specific reductions of AMPA-mediated currents were obtained. Kainate-induced gamma oscillations exhibited reduced power in hippocampal slices from GluR-D^−/− and GluR-A^PVCre−/− mice. Experimental and modeling data indicated that this alteration could be accounted for by imprecise spike timing of fast-spiking cells (FS) caused by smaller interneuronal EPSPs. GluR-D^−/− and GluR-A^PVCre−/− mice exhibited similar impairments in hippocampus-dependent tasks. These findings directly show the effects of insufficient recruitment of fast-spiking cells at the network and behavioral level and demonstrate the role of this subpopulation for working and episodic-like memory.
Parvalbumin deficiency affects network properties resulting in increased susceptibility to epileptic seizures
2004, Molecular and Cellular Neuroscience
Networks of GABAergic interneurons are of utmost importance in generating and promoting synchronous activity and are involved in producing coherent oscillations. These neurons are characterized by their fast-spiking rate and by the expression of the Ca²⁺-binding protein parvalbumin (PV). Alteration of their inhibitory activity has been proposed as a major mechanism leading to epileptic seizures and thus the role of PV in maintaining the stability of neuronal networks was assessed in knockout (PV−/−) mice. Pentylenetetrazole induced generalized tonic–clonic seizures in all genotypes, but the severity of seizures was significantly greater in PV−/− than in PV+/+ animals. Extracellular single-unit activity recorded from over 1000 neurons in vivo in the temporal cortex revealed an increase of units firing regularly and a decrease of cells firing in bursts. In the hippocampus, PV deficiency facilitated the GABA_Aergic current reversal induced by high-frequency stimulation, a mechanism implied in the generation of epileptic activity. We postulate that PV plays a key role in the regulation of local inhibitory effects exerted by GABAergic interneurons on pyramidal neurons. Through an increase in inhibition, the absence of PV facilitates synchronous activity in the cortex and facilitates hypersynchrony through the depolarizing action of GABA in the hippocampus.
Vicia villosa agglutinin labels a subset of neurons coexpressing both the mu opioid receptor and parvalbumin in the developing rat subiculum
1996, Developmental Brain Research
Vicia villosa agglutinin (VVA), anti-parvalbumin antiserum and an affinity-purified anti-mu opioid receptor antibody were used to triple-label neurons in the postnatal rat subiculum. VVA labeled a subset of mu opioid receptor-positive neurons that were also immunoreactive for parvalbumin. The morphology of the triple-labeled neurons was heterogeneous, and included multipolar, ovoid and pyramidal-shaped neurons. Neurons single-labeled for the mu opioid receptor, VVA or parvalbumin were also morphologically heterogeneous. The postnatal development of mu opioid receptor immunoreactivity (IR), parvalbumin-IR and VVA binding was investigated using triple-labeling immunocytochemistry. Mu opioid receptor-IR appeared first and was present at postnatal day 1 (P1). Parvalbumin-IR was first observed in somata at P10, followed by proximal and distal dendrites at P15 and P20 respectively. Faint VVA labeling was seen first at P10 and surrounded a limited number of neurons. The intensity of labeling and the number of neurons labeled with VVA increased between P10 and P20; however, both measures remained below adult levels at P20. This study further illustrates the neurochemical heterogeneity of interneurons in the hippocampal formation and shows the developmentally early appearance of mu opioid receptor-IR compared to the late appearance of VVA binding and parvalbumin-IR.
Developmental expression of parvalbumin mRNA in the cerebral cortex and hippocampus of the rat
1995, Molecular Brain Research
Parvalbumin (PARV) belongs to the family of calcium-binding proteins bearing the EF hand domain. Immunocytochemical studies in the cerebral cortex have demonstrated that neurons containing PARV include two types of GABAergic interneurons, namely, basket and axo-axonic chandelier cells. The present study examines the onset and pattern of PARV mRNA expression during the development of rat neocortex and hippocampus by means of ‘in situ’ hybridization with an oligonucleotide probe corresponding to rat PARV cDNA. In animals aged P0–P6 no signal was detected above background in neocortex or hippocampus. At P8, a few cortical cells displayed a number of silver grains just above background levels. By P10 PARV mRNA-expressing cells in the neocortex were detected almost exclusively in layer V of somatosensory, frontal and cingulate cortices. At P12 PARV mRNA was mainly detected in layers IV, V and VIa. By P14 there was a marked overall increase in the entire neocortex, including layer II–III, both in the number of cells and in their intensity of labelling. Further maturation in the pattern of PARV mRNA concentration was observed between P16 and P21. In the hippocampus low hybridization was observed at P10–P12. In subsequent stages both the number of positive cells and the intensity of labelling increased steadily. No clear-cut radial gradients for the expression of PARV mRNA were observed in the hippocampul region. Our results show that the developmental radial gradient followed by PARV mRNA expression in the neocortex does not follow an ‘inside-out’ gradient, consistent with previous immunocytochemical findings. Taken together, these data indicate that the developmental sequence followed by the PARV protein directly reflects mRNA abundance and suggest that PARV mRNA expression correlates with the functional maturation of cortical interneurons.

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View full text

Late appearance of parvalbumin-immunoreactive neurons in the rodent cerebral cortex does not follow an ‘inside-out’ sequence

Abstract

Dev. Brain Res.

Cell Calcium

Neuroscience

Cell Calcium

J. Biol. Chem.

Brain Res.

Brain Res.

Neuroscience

Neurosci. Lett.

Cell Calcium

Neuroscience

Autoradiographic study of cell migration during histogenesis of cerebral cortex in mouse

Nature

Area-Specific morphological and neurochemical maturation of non-pyramidal neurons in the rat hippocampus as revealed by parvalbumin immunochemistry

Anat. Embryol.

Parvalbumin in most gamma-amino-butyric acid-containing neurons of the rat cerebral cortex

Science

Visualization of chandelier cell axons by parvalbumin immunoreactivity in monkey cerebral cortex

Ontogeny of the calcium-binding protein calbindin D-28K in the rat nervous system

Anat. Embryol.