GABA-A receptors (GABA-ARs) are typically expressed at synaptic or nonsynaptic sites
mediating phasic and tonic inhibition, respectively. These two forms of inhibition
conjointly control various network oscillations. To disentangle their roles in thalamocortical
rhythms, we focally deleted synaptic, gamma2 subunit-containing GABA-ARs in the thalamus
using viral intervention in mice. After successful removal of gamma2 subunit clusters,
spontaneous and evoked GABAergic synaptic currents disappeared in thalamocortical
cells when the presynaptic, reticular thalamic (nRT) neurons fired in tonic mode.
However, when nRT cells fired in burst mode, slow phasic GABA-AR-mediated events persisted,
indicating a dynamic, burst-specific recruitment of nonsynaptic GABA-ARs. In vivo,
removal of synaptic GABA-ARs reduced the firing of individual thalamocortical cells
but did not abolish slow oscillations or sleep spindles. We conclude that nonsynaptic
GABA-ARs are recruited in a phasic manner specifically during burst firing of nRT
cells and provide sufficient GABA-AR activation to control major thalamocortical oscillations.
