Sensory Learning Differentially Affects GABAergic Tonic Currents in Excitatory Neurons and Fast Spiking Interneurons in Layer 4 of Mouse Barrel Cortex

Pairing tactile stimulation of whiskers with a tail shock is known to result in expansion of cortical representation of stimulated vibrissae and in the increase in synaptic GABAergic transmission. However, the impact of such sensory learning in classical conditioning paradigm on GABAergic tonic currents has not been addressed. To this end, we performed whole cell patch-clamp slice recordings of tonic currents from neurons (excitatory regular spiking, regular spiking nonpyramidal, and fast spiking interneurons) of layer 4 of the barrel cortex from naive and trained mice. Interestingly, endogenous tonic GABAergic currents measured from the excitatory neurons in the cortical representation of “trained” vibrissae were larger than in the “naïve” or pseudoconditioned ones. On the contrary, sensory learning markedly reduced tonic currents in the fast spiking interneurons but not in regular spiking nonpyramidal neurons. Changes of tonic currents were accompanied by changes in the input resistances—decrease in regular spiking and increase in fast spiking neurons, respectively. Applications of nipecotic acid, a GABA uptake blocker, enhanced the tonic currents, but the impact of the sensory learning remained qualitatively the same as in the case of the tonic currents. Similar to endogenous tonic currents, sensory learning enhanced currents induced by THIP (superagonist for δ subunit–containing GABAA receptors) in regular spiking neurons, whereas the opposite was observed for the fast spiking interneurons. In conclusion, our data show that the sensory learning strongly affects the GABAergic tonic currents in a cell-specific manner and suggest that the underlying mechanism involves regulation of expression of δ subunit–containing GABAA receptors.