Gap-Junctional Coupling between Neurogliaform Cells and Various Interneuron Types in the Neocortex

Abstract

Electrical synapses contribute to the generation of synchronous activity in neuronal networks. Several types of cortical GABAergic neurons acting via postsynaptic GABA(A) receptors also form electrical synapses with interneurons of the same class, suggesting that synchronization through gap junctions could be limited to homogenous interneuron populations. Neurogliaform cells elicit combined GABA(A) and GABA(B) receptor-mediated postsynaptic responses in cortical pyramidal cells, but it is not clear whether neurogliaform cells are involved in networks linked by electrical coupling. We recorded from pairs, triplets, and quadruplets of cortical neurons in layers 2 and 3 of rat somatosensory cortex (postnatal day 20-35). Neurogliaform cells eliciting slow IPSPs on pyramidal cells also triggered divergent electrical coupling potentials on interneurons. Neurogliaform cells were electrically coupled to other neurogliaform cells, basket cells, regular-spiking nonpyramidal cells, to an axoaxonic cell, and to various unclassified interneurons showing diverse firing patterns and morphology. Electrical interactions were mediated by one or two electron microscopically verified gap junctions linking the somatodendritic domain of the coupled cells. Our results suggest that neurogliaform cells have a unique position in the cortical circuit. Apart from eliciting combined GABA(A) and GABA(B) receptor-mediated inhibition on pyramidal cells, neurogliaform cells establish electrical synapses and link multiple networks formed by gap junctions restricted to a particular class of interneuron. Widespread electrical connections might enable neurogliaform cells to monitor the activity of different interneurons acting on GABA(A) receptors at various regions of target cells.