Elsevier

Neuroscience

Volume 85, Issue 3, 24 April 1998, Pages 677-701
Neuroscience

Neurochemical features and synaptic connections of large physiologically-identified GABAergic cells in the rat frontal cortex

https://doi.org/10.1016/S0306-4522(97)00685-4Get rights and content

Abstract

Physiological and morphological properties of large non-pyramidal cells immunoreactive for cholecystokinin, parvalbumin or somatostatin were investigated in vitro in the frontal cortex of 18–22-day-old rats. These three peptides were expressed in separate populations including large cells. Cholecystokinin cells and parvalbumin cells made boutons apposed to other cell bodies, but differed in their firing patterns in response to depolarizing current pulses. Parvalbumin cells belonged to fast-spiking cells. Parvalbumin fast-spiking cells also included chandelier cells. In contrast, cholecystokinin cells were found to be regular-spiking non-pyramidal cells or burst-spiking non-pyramidal cells with bursting activity from hyperpolarized potentials (two or more spikes on slow depolarizing humps). Large somatostatin cells belonged to the regular-spiking non-pyramidal category and featured wide or ascending axonal arbors (wide arbor cells and Martinotti cells) which did not seem to be apposed to the somata so frequently as large cholecystokinin and parvalbumin cells. For electron microscopic observations, another population of eight immunohistochemically-uncharacterized non-pyramidal cells were selected: (i) five fast spiking cells including one chandelier cell which are supposed to contain parvalbumin, and (ii) three large regular-spiking non-pyramidal cells with terminals apposed to somata, which are not considered to include somatostatin cells, but some of which may belong to cholecystokinin cells. The fast-spiking cells other than a chandelier cell and the large regular-spiking non-pyramidal cells made GABA-positive synapses on somata (4% and 12% of the synapses in two small to medium fast-spiking cells, 22% and 35% of the synapses in two large fast-spiking cells, and 10%, 18% and 37% of the synapses in three large regular-spiking non-pyramidal cells). A few terminals of the fast-spiking and regular-spiking non-pyramidal cells innervated GABAergic cells. About 30% of the fast-spiking cell terminals innervated spines, but few of the regular-spiking non-pyramidal cell terminals did. A fast-spiking chandelier cell made GABA-positive synapses on GABA-negative axon initial segments.

These results suggest that large GABAergic cells are heterogeneous in neuroactive substances, firing patterns and synaptic connections, and that cortical cells receive heterogeneous GABAergic somatic inputs.

Section snippets

Antibodies and antisera

A monoclonal antibody raised against CCK/Gastrin (No. 28.2 MoAb) was provided by CURE/UCLA/DDC Antibody/RIA Core.[57]As a control it was preabsorbed with an excess (10−6 M) of sulphated CCK-octapeptide (Peptide Inst. Inc., Japan), resulting in no stainings in the rat frontal cortex. The bulk of CCK-like immunoreactivity in the cerebral cortex is closely similar to the sulphated CCK octapeptide.[25]Therefore, the structures stained with this antibody in the present study were considered to be

Physiological and morphological properties of large immunohistochemically-identified non-pyramidal cells

First, we have investigated the immunohistochemical, physiological and morphological characteristics of large non-pyramidal cells, and which large cells had axon collaterals with boutons apposed to somata at the light microscopic level. In the rat frontal cortex, CCK-, somatostatin- and parvalbumin-immunoreactive neurons contained large non-pyramidal cells. Therefore, following three experiments were done: (1) It was confirmed that CCK, somatostatin and parvalbumin were expressed in separate

Discussion

The major findings of the present study in the frontal cortex of young rats can be summarized as follows (Fig. 13): (1) Large non-pyramidal cells in layers II/III included CCK RS/BSNP, somatostatin RSNP and parvalbumin FS cells. (2) Some of the axon terminals of large CCK RS/BSNP cells were apposed to other somata by multiple boutons. (3) Large somatostatin cells were RSNP cells with wide or ascending axonal arbors. (4) Parvalbumin cells included chandelier cells with vertical rows of axonal

Conclusions

The somata of cortical cells are innervated by subgroups of cells containing parvalbumin or neuropeptides. The same areas of dendrites may be innervated by multiple types of GABAergic terminals from separate populations of non-pyramidal cells with distinct physiological and chemical properties. Thus in some cases cortical cells are regulated by convergent GABAergic inputs from separate sources. To further understand the physiological roles of these GABAergic cells, it is necessary to clarify

Acknowledgements

This work was supported by the Frontier Research Program, RIKEN, and Grants-in-Aid from the Japanese Ministry of Education, Science, Sports and Culture. We thank Ms Naoko Wada and Ms Satoko Kato for technical assistance. We are grateful to Dr Robert Benoit for an antiserum against somatostatin 28. Antibody No. 28.2 MoAb raised against gastrin/CCK was provided by CURE/UCLA/DDC Antibody/RIA Core.

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