The innervation of parvalbumin-containing interneurons by VIP-immunopositive interneurons in the primary somatosensory cortex of the adult rat

Abstract

gamma-Aminobutyric acid (GABA)ergic interneurons of neocortex consist of many subgroups with extremely heterogeneous morphological, physiological and molecular properties. To explore the putative effect of the vasoactive intestinal polypeptide-immunopositive (VIP +) neurons on neocortical circuitry, the number and distribution of VIP + boutons were analysed on somatodendritic domains of 272 parvalbumin immunopositive (PV +) 3D-reconstructed neurons. The synaptic nature of 91% of somatic and 76% of dendritic contacts was verified by electron microscopy. The target PV + neurons were separated in two significantly different groups by means of cluster analysis. The first group (Cluster 1, 26%) received on average five times more VIP + synapses than those of the second group. The second group (Cluster 2, 74%) contained cells that were poorly innervated by VIP + boutons or did not have either somatic or dendritic or any VIP innervation at all. The cells of Cluster 1 had a soma size and total dendritic length significantly smaller than that of Cluster 2, however, they received three times more dendritic synapses, which resulted in a five times higher VIP + synaptic density on dendrites. Our results showed that although most of the PV + cells are innervated by VIP + boutons at a varying degree, some 6% of PV + cells received no input from VIP + interneurons. This suggests a refined morphological basis to influence the majority of the PV + interneurons, which are very effectively controlling pyramidal cell firing. Together with metabolic and neuromodulatory effects of VIP, this would probably result in an enhanced responsiveness of the latter cell type to tactile stimuli.