Interneurons Immunoreactive for Vasoactive Intestinal Polypeptide (VIP) are Extensively Innervated by Parvalbumin-Containing Boutons in Rat Primary Somatosensory Cortex

Sensory perception results from the synchronized action of large ensembles of cortical neurons. Receptive field properties of such neurons in sensory areas strongly depend on circuits utilizing the inhibitory amino acid transmitter γ-aminobutyric acid (GABA). GABAergic neurons often co-localize neuropeptides and/or calcium-binding proteins in a cell-type specific manner. We have taken advantage of this fact to study the synaptic circuitry involving presynaptic parvalbumin-containing boutons (originating from horizontally extensive basket cells) and postsynaptic VlP-immunoreactive GABAergic targets which mostly have a vertically oriented axonal field. Abundant appositions between parvalbumin-immunoreactive boutons and all VIP-stained neurons were observed at the light microscopic level. The numbers of contacts ranged between three and well over 20 for single VIP cells. The higher numbers were especially frequent in the supragranular and granular layers contacting the numerous bipolar, as well as multipolar VIP cells located there; but the VlP-immunoreactive neurons in the infragranular layers were also targeted by parvalbumin-immunoreactive boutons without exception, albeit in more variable, mostly lower numbers. Correlated electron microscopic investigations revealed that virtually all of these light microscopically observed appositions resembled symmetric synaptic specializations. The vast majority were located on the soma or proximal dendrites of the VIP-positive neurons. Since pyramidal cells, in turn, represent a major target for the parvalbumin and VIP synapses, the activation of these synapses may lead to coherent oscillations providing the necessary clock function to synchronize pyramidal cell discharges, both across and within cortical columns.