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The Journal of Neuroscience, August 1, 2001, 21(15):5824-5831

and  Frequency Synchronization by Dendritic GABAergic Synapses and Gap Junctions in a Network of Cortical Interneurons

János Szabadics^{1, 2}, Andrea Lorincz¹, and Gábor Tamás^{1, 2}

¹ Department of Comparative Physiology, University of Szeged, Szeged H-6726, Hungary, and ² Medical Research Council Anatomical Neuropharmacology Unit, University Department of Pharmacology, University of Oxford, Oxford, OX1 3TH, United Kingdom

Distinct interneuron populations innervate perisomatic and dendritic regions of cortical cells. Perisomatically terminating GABAergic inputs are effective in timing postsynaptic action potentials, and basket cells synchronize each other via gap junctions combined with neighboring GABAergic synapses. The function of dendritic GABAergic synapses in cortical rhythmicity, and their interaction with electrical synapses is not understood.

Using multiple whole-cell recordings in layers 2-3 of rat somatosensory cortex combined with light and electron microscopic determination of sites of interaction, we studied the interactions between regular spiking nonpyramidal cells (RSNPCs). Random samples of unlabeled postsynaptic targets showed that RSNPCs placed GABAergic synapses onto dendritic spines (53 ± 12%) and shafts (45 ± 10%) and occasionally somata (2 ± 4%). GABAergic interactions between RSNPCs were mediated by 4 ± 2 axodendritic synapses and phased postsynaptic activity at  frequency but were ineffective in phasing at  rhythm. Electrical interactions of RSNPCs were transmitted via two to eight gap junctions between dendritic shafts and/or spines. Elicited at  and  frequencies, gap junctional potentials timed postsynaptic spikes with a phase lag, however strong electrical coupling could synchronize presynaptic and postsynaptic activity. Combined unitary GABAergic and gap junctional connections of moderate strength produced  and  frequency synchronization of the coupled RSNPCs.

Our results provide evidence that dendritic GABAergic and/or gap junctional mechanisms effectively transmit suprathreshold information in a population of interneurons at behaviorally relevant frequencies. A coherent network of GABAergic cells targeting the dendrites could provide a pathway for rhythmic activity spatially segregated from perisomatic mechanisms of synchronization.

Key words: interneuron; synchronization; dendrite; gap junction; GABA; network

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Copyright © 2001 Society for Neuroscience  0270-6474/01/21155824-08$05.00/0

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