Inhibitory postsynaptic currents (IPSCs) of the thalamic reticular (RT) nucleus are dramatically slower than in the neighboring ventrobasal (VB) neurons. It has been suggested that α3-subunit-containing receptors underlie slow IPSCs in RT neurons, while rapid synaptic currents in the VB nucleus are due to γ-aminobutyric acid A receptors (GABAARs), including the α1-subunit. In our recent study [Barberis et al. (2007) Eur. J. Neurosci., 25, 2726–2740] we have found that profound differences in kinetics of currents mediated by α3β2γ2 and α1β2γ3 receptors resulted from distinct binding and desensitization properties. However, a direct comparison between kinetics of neuronal GABAARs from RT and VB neurons and α3- and α1-subunit-containing receptors has not been made. For this purpose, current responses to ultrafast GABA applications were recorded from patches excised from neurons in VB and RT areas. Deactivation kinetics determined for RT and VB neurons closely resembled that in currents mediated by α3β2γ2 and α1β2γ2 receptors. In RT neurons, currents elicited by non-saturating [GABA] had a remarkably slow onset, a hallmark of α3-subunit-containing receptors. In VB and RT neurons, single-channel currents elicited by brief GABA pulses had similar characteristics to those of α1β2γ2 and α3β2γ2 receptors. However, in stationary conditions, similarity between single-channel currents in neurons and respective recombinant receptors was less apparent. We propose that the non-stationary kinetics of GABAergic currents in VB and RT nuclei mimic that of currents mediated by α1- and α3-subunit-containing receptors. The dissimilarity between stationary kinetics of neuronal and recombinant receptors probably reflects differences between GABAARs mediating phasic and tonic currents in these neurons.