Two classes of excitatory synaptic responses in rat thalamic reticular neurons

The thalamic reticular nucleus (nRt), composed of GABAergic cells providing inhibition of relay neurons in dorsal thalamus, receives excitation from neocortex and thalamus. The two excitatory pathways promoting feedback or feedforward inhibition of thalamocortical neurons, contribute to sensory processing and rhythm generation. While synaptic inhibition within nRt has been carefully characterized, little is known regarding the biophysics of synaptic excitation. To characterize the functional properties of thalamocortical and corticothalamic connections to nRt, we recorded minimal electrically-evoked EPSCs from nRt cells in vitro. A hierarchical clustering algorithm distinguished two types of events. Type 1 events had larger amplitudes and faster kinetics, largely mediated by AMPA receptors, whereas Type 2 responses had more prominent NMDA receptor contribution. Type 1 responses showed subnormal axonal propagation and paired pulse depression, consistent with thalamocortical inputs. Furthermore responses kinetically similar to Type 1 events were evoked by glutamate-mediated activation of thalamic neurons. Type 2 responses, by contrast, likely arise from corticothalamic inputs, with larger NMDA conductance and weak Mg²⁺-dependent block, suggesting that NMDA receptors are critical for cortical excitation of reticular neurons. The long-lasting action of NMDA receptors would promote reticular cells burst firing and produce powerful inhibitory output to relay neurons proposed to be important in triggering epilepsy. This work provides the first complete voltage clamp analysis of kinetics and voltage dependence of AMPA and NMDA responses of TC and CT synapses in nRt, and will be critical in optimizing biologically realistic neural network models of thalamocortical circuits relevant to sensory processing and thalamocortical oscillations.

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