β and γ frequency synchronization by dendritic GABAergic synapses and gap junctions in a network of cortical interneurons

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 beta frequency but were ineffective in phasing at gamma rhythm. Electrical interactions of RSNPCs were transmitted via two to eight gap junctions between dendritic shafts and/or spines. Elicited at beta and gamma 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 beta and gamma 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.