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The Journal of Neuroscience, June 1, 1998, 18(11):4255-4270
Differentially Interconnected Networks of GABAergic Interneurons in the Visual Cortex of the Cat
Gábor Tamás1, 2, Peter Somogyi1, and Eberhard H. Buhl1 1 Medical Research Council, Anatomical Neuropharmacology Unit, Department of Pharmacology, University of Oxford, Oxford, OX1 3TH, United Kingdom, and 2 Department of Comparative Physiology, József Attila University, Szeged, H-6726, Hungary
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 GABAergic 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 GABAA 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.
Key words: cerebral cortex; interneuron; inhibition; IPSP; GABA; synapse
Copyright © 1998 Society for Neuroscience 0270-6474/98/18114255-16$05.00/0
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