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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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