Improved Perceptual Learning by Control of Extracellular GABA Concentration by Astrocytic Gap Junctions

Abstract

Learning of sensory cues is believed to rely on synchronous pre- and postsynaptic neuronal firing. Evidence is mounting that such synchronicity is not merely caused by properties of the underlying neuronal network but could also depend on the integrity of gap junctions that connect neurons and astrocytes in networks too. In this perspective, we set out to investigate the effect of astrocytic gap junctions on perceptual learning, introducing a model for coupled neuron-astrocyte networks. In particular, we focus on the fact that astrocytes are rich of GABA transporters (GATs) which can either uptake or release GABA depending on the astrocyte membrane potential, which is a function of local neural activity. We show that GABAergic signaling is a crucial component of intracolumnar neuronal synchronization, thereby promoting learning by neurons in the same cell assembly that are activated by a shared sensory cue. At the same time, we show that this effect can critically depend on astrocytic gap junctions insofar as these latter could synchronize extracellular GABA levels around many neurons and throughout entire cell assemblies. These results are supported by extensive computational arguments and predict that astrocytic gap junctions could improve perceptual learning by controlling extracellular GABA.