J. Szabadics et al., beta and gamma frequency synchronization by dendritic GABAergic synapses and gap junctions in a network of cortical interneurons, J NEUROSC, 21(15), 2001, pp. 5824-5831
Distinct interneuron populations innervate perisomatic and dendritic region
s of cortical cells. Perisomatically terminating GABAergic inputs are effec
tive 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 cor
tex combined with light and electron microscopic determination of sites of
interaction, we studied the interactions between regular spiking nonpyramid
al cells (RSNPCs). Random samples of unlabeled postsynaptic targets showed
that RSNPCs placed GABAergic synapses onto dendritic spines (53 +/- 12%) an
d shafts (45 +/- 10%) and occasionally somata (2 +/-4%). GABAergic interact
ions between RSNPCs were mediated by 4 +/-2 axodendritic synapses and phase
d postsynaptic activity at beta frequency but were ineffective in phasing a
t 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 sp
ikes 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 frequen
cy 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 o
f GABAergic cells targeting the dendrites could provide a pathway for rhyth
mic activity spatially segregated from perisomatic mechanisms of synchroniz
ation.