Elsevier

Neuroscience

Volume 88, Issue 1, January 1999, Pages 37-55
Neuroscience

Postsynaptic targets of somatostatin-immunoreactive interneurons in the rat hippocampus

https://doi.org/10.1016/S0306-4522(98)00302-9Get rights and content

Abstract

Two characteristic interneuron types in the hippocampus, the so-called hilar perforant path-associated cells in the dentate gyrus and stratum oriens/lacunosum-moleculare neurons in the CA3 and CA1 regions, were suggested to be involved in feedback circuits. In the present study, interneurons identical to these cell populations were visualized by somatostatin-immunostaining, then reconstructed, and processed for double-immunostaining and electron microscopy to establish their postsynaptic target selectivity. A combination of somatostatin-immunostaining with immunostaining for GABA or other interneuron markers revealed a quasi-random termination pattern. The vast majority of postsynaptic targets were GABA-negative dendritic shafts and spines of principal cells (76%), whereas other target elements contained GABA (8%). All of the examined neurochemically defined interneuron types (parvalbumin-, calretinin-, vasoactive intestinal polypeptide-, cholecystokinin-, substance P receptor-immunoreactive neurons) received innervation from somatostatin-positive boutons.

Recent anatomical and electrophysiological data showed that the main excitatory inputs of somatostatin-positive interneurons originate from local principal cells. The present data revealed a massive GABAergic innervation of distal dendrites of local principal cells by these feedback driven neurons, which are proposed to control the efficacy and plasticity of entorhinal synaptic input as a function of local principal cell activity and synchrony.

Section snippets

Perfusion and preparation of tissue sections

Eight male Wistar rats (300–350 g, two-months-old; Charles River, Budapest, Hungary) were deeply anaesthetized by Equithesin (chlornembutal, 0.3 ml/100 g), and perfused through the heart first with saline followed by a phosphate-buffered (PB, 0.1 M) fixative containing 4% paraformaldehyde, 0.15% picric acid and 0.05% glutaraldehyde in the case of series A (n=5) for single somatostatin-immunostaining and for somatostatin–parvalbumin, somatostatin–CCK, somatostatin–calretinin, somatostatin–VIP,

General pattern of somatostatin-immunostaining in the hippocampus

Somatostatin-immunoreactive neurons showed the same basic morphological features as observed in several previous studies in the rat21, 34, 36, 38, 50, 64with some additional morphological details due to the enhanced sensitivity of the present antiserum. Briefly, cell bodies were located in stratum oriens of the CA1, stratum oriens and stratum lucidum of the CA3 regions and in the hilus of the dentate gyrus (Fig. 1A). Occasionally, some cells were also found in stratum radiatum of the CA1 and

Discussion

On the basis of morphological characteristics, somatostatin-immunoreactive interneurons could be separated into three distinct subtypes, (i) HIPP cells of the dentate gyrus, (ii) conventional O-LM cells in stratum oriens of the CA1 and CA3 regions and (iii) neurons with dendrites similar to O-LM cells, but with a characteristically different axon. The first two subtypes have dense axonal projections to stratum lacunosum-moleculare (O-LM) or stratum moleculare (HIPP), where entorhinal afferents

Conclusion

The present data demonstrate that somatostatin-containing GABAergic interneurons driven in a feedback manner terminate predominantly on the most distal dendritic segments of pyramidal cells in conjunction with entorhinal afferents (i.e. they are O-LM and HIPP cells). We propose that, if the role of theta oscillation is to separate signal transmission from background firing in time,[19]then these feedback dendritic inhibitory cells may help confine time periods when entorhinal synapses on

Acknowledgements

We are grateful to Dr T. J. Görcs for antisera against somatostatin, vasoactive intestinal polypeptide and cholecystokinin, to Dr K. G. Baimbridge and to Dr J. H. Rogers for antisera against parvalbumin and calretinin, respectively, and to Dr P. Somogyi for antisera against GABA. The valuable discussions with Drs A. M. Thomson, Gy. Buzsáki, H. Markram and R. Miles concerning the activation of O-LM cells, and the time-course of back-propagating action potentials and disynaptic IPSPs are highly

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