Somatosensory processing in inhibitory feedback circuits of the thalamus

A major function of the mammalian thalamus is the relay of sensory signals to the cerebral cortex, and oscillatory rhythms generated by feedback circuits among thalamic and cortical neurons can alter the processing and perception of these signals. Thalamocortical (TC) neurons are a source of afferent input to, and are reciprocally inhibited by, neurons of the thalamic reticular (Rt) nucleus. During certain stages of sleep, circuits of TC and Rt neurons generate 7--12 Hz 'spindle' oscillations by discharging rhythmic spike bursts. In both neuronal types burst discharges are mediated by T-type Ca2+ channels which generate low-threshold spikes. Upon arousal, TC and Rt neurons transition to a sensory relay function and single spike tonic activity. The function of Rt-mediated inhibition and T-type Ca2+ channels in processing ascending sensory signals, however, remains unclear. We made extracellular single unit recordings in the somatosensory thalamus of lightly narcotized rats while applying controlled ramp-and-hold deflections to their mystacial vibrissae. TC units responded to vibrissa movements with sparse but temporally focused discharges. Rt units, by contrast, exhibited transient responses of long duration and high spike counts, regardless of their tonic vs. burst mode of spontaneous firing. Negative correlations of Rt response magnitudes with levels of pre-stimulus spontaneous activity suggested that they are mediated by T-type Ca2+ channels, which require hyperpolarization before activating their conductance. Consistent with this interpretation, microiontophoretic application of the glutamate receptor agonist, N-methyl-D-aspartate, which increased unit spontaneous activity, reduced or eliminated stimulus-evoked responses. During maintained deflections Rt units exhibit tonic, elevated discharge. TC units, by contrast, are more likely to exhibit tonic suppression of activity, and pharmacological antagonism of inhibition suggested that Rt contributes to this suppression. High-pass characterisitics were also evidenced in TC responses to sinusoidal deflections and were complemented by low-pass characteristics of Rt firing. These experiments demonstrate that Rt neurons are responsive to low-threshold tactile stimulation during both tonic and burst mode firing and suggest that T-type Ca2+ channels contribute to sensory processing. Because of their voltage-dependent properties, circuits of thalamic neurons may perform different sensory processing functions depending on an animal's behavioral state.