Processing of periodic whisker deflections by neurons in the ventroposterior medial and thalamic reticular nuclei

Rats employ rhythmic whisker movements to sample information in their sensory environment. To study frequency tuning and filtering characteristics of thalamic circuitry, we recorded single-unit responses of ventroposterior medial (VPm) and thalamic reticular (Rt) neurons to 1- to 40-Hz sinusoidal and pulsatile whisker deflection in lightly narcotized rats. Neuronal entrainment was assessed by a measure of the relative modulation (RM) of firing at the stimulus frequency given by the first harmonic (F1) of the cycle time histogram divided by the mean firing rate (F0). VPm signaling of both sinusoidal and periodic pulsatile whisker movements improved gradually over 1-16 and was maximal at 20-40 Hz. By contrast, the RM of Rt responses increased over 1-8 Hz, but deteriorated progressively over the 12- to 40-Hz range. In Rt, response adaptation occurred at lower stimulus frequencies and to a greater extent than in VPm. Within a train of high-frequency stimuli, Rt responses progressively decremented, possibly due to the accumulation of inhibition, whereas those of VPm neurons augmented. Mean firing rates in Rt increased 42 spikes/s over 1-40 Hz, providing tonic (low RM) inhibition during high-frequency stimulation that may enhance VPm signal-to-noise ratios. Consistent with this view, VPm mean firing rates increased only 13 spikes/s over 1-40 Hz, and inter-deflection activity was suppressed to a greater extent than stimulus-evoked responses. Rt inhibition is likely to act in concert with actions of neuromodulators in optimizing thalamic temporal signaling of high-frequency whisker movements.