Differentially interconnected networks of GABAergic interneurons in the visual cortex of the cat

Abstract

Networks of GABAergic neurons have been implicated in neuronal population synchronization. To define the extent of cellular interconnections, we determined the effect, number, and subcellular distribution of synapses between putative GARAergic neurons in layers II-IV of the cat visual cortex using paired intracellular recordings in vitro followed by correlated light and electron microscopy. All neurons having interneuronal electrophysiological properties were classified by their postsynaptic target profile and were identified as basket (BC; n = 6), dendrite-targeting (DTC; n = 1), and double bouquet (DBC; n = 2) cells. In four out of five anatomically fully recovered and reconstructed cell pairs, synaptic connections were found to be reciprocal. Generally BCs established synaptic junctions closer (21 ± 20 μm) to postsynaptic somata than did DBCs (43 ± 19 μm; p < 0.01). The unitary number of synapses (n values, 10, 7, and 20) in each of three BC-to-BC pairs was higher than that in three BC- to-DBC (n values, 1, 2, and 2) and three DBC-to-BC (n values, 1, 4, and 4) connections (p < 0.05). A BC innervated a DTC through two synaptic junctions. Unitary postsynaptic effects mediated by five BCs could be recorded in two BCs, two DBCs, and a DTC. The BCs elicited short-duration fast IPSPs, similar to those mediated by GABA(A) receptors. At a membrane potential of -55.0 ± 6.4 mV, unitary IPSPs (n = 5) had a mean amplitude of 919 ± 863 μV. Postsynaptic response failures were absent when an IPSP was mediated by several release sites. Thus, distinct GABAergic interneurons form reciprocally interconnected networks. The strength of innervation and the proximal placement of synapses suggest a prominent role for BCs in governing the activity of intracortical GABAergic networks in layers II-IV.