A network of fast-spiking cells in the neocortex connected by electrical synapses

Abstract

Encoding of information in the cortex is thought to depend on synchronous firing of cortical neurons. Inhibitory neurons are known to be critical in the coordination of cortical activity, but how interaction among inhibitory cells promotes synchrony is not well understood. To address this issue directly, we have recorded simultaneously from pairs of fast-spiking (FS) cells, a type of gamma-aminobutyric acid (GABA)-containing neocortical interneuron. Here we report a high occurrence of electrical coupling among FS cells. Electrical synapses were not found among pyramidal neurons or between FS cells and other cortical cells. Some FS cells were interconnected by both electrical and GABAergic synapses. We show that communication through electrical synapses allows excitatory signalling among inhibitory cells and promotes their synchronous spiking. These results indicate that electrical synapses establish a network of fast-spiking cells in the neocortex which may play a key role in coordinating cortical activity.

Highly Energized Inhibitory Interneurons are a Central Element for Information Processing in Cortical Networks

“…49,[93][94][95][96][97][98] This special feature is well suited to synchronize basket cell spiking with high temporal fidelity in the hippocampus as well as in the neocortex. 8,16,24,99 In brief, an action potential exerts a shortlasting depolarization of electrically coupled basket cells, which is immediately curtailed by the subsequent strong IPSP. 16,100,101 This mechanism defines a short time window for mutual excitation of PV þ basket cells, thereby generating near-synchronous inhibition of multiple excitatory and inhibitory neurons in the network.…”

GABAergic synchronization in the limbic system and its role in the generation of epileptiform activity

“…Networks of fast-spiking interneurons co-expressing GABA and parvalbumine have been shown to promote synchronization via perisomatic interneuron-interneuron interaction in the hippocampus, in the entorhinal cortex, and in the neocortex (Gulyás et al, 1996;Tamás et al, 1998;Galarreta and Hestrin, 1999;Gibson et al, 1999;Bartos et al, 2002Bartos et al, , 2007Hájos et al, 2004). In addition, non-synaptic interactions through gap junctions may represent an additional mechanism for interneurons synchronization during gamma oscillations (Bartos et al, 2002;Tamás et al, 2000).…”

Electrical synapses between AII amacrine cells in the retina: Function and modulation

“…Mills and Massey, 1998) With the advent of the tight-seal, whole-cell recording technique (Hamill et al, 1981), it became possible to use single-electrode voltage-clamp recording and small mammalian cells for such investigations. Dual, whole-cell, voltage-clamp recordings between pairs of electrically coupled cells can be used to measure junctional conductances both at the single-channel level and at the macroscopic level (Galarreta and Hestrin, 1999;Gibson et al, 1999;Neyton and Trautmann, 1985). Apart from the indirect evidence from tracer coupling via chemical diffusion and visual receptive field measurements, the first direct evidence for functional electrical synapses between AII amacrine cells was obtained in our laboratory by dual patch-clamp recording from pairs of AII amacrine cells in rat retinal slices (Veruki and Hartveit, 2002a).…”