Response Transformation and Receptive-Field Synthesis in the Lemniscal Trigeminothalamic Circuit

Abstract

To understand how the lemniscal trigeminothalamic circuit (PrV → VPM) of the rodent whisker-to-barrel pathway transforms afferent signals, we applied ramp-and-hold deflections to individual whiskers of lightly narcotized rats while recording the extracellular responses of neurons in either the ventroposterior medial (VPM) thalamic nucleus or in brain stem nucleus principalis (PrV). In PrV, only those neurons antidromically determined to project to VPM were selected for recording. We found that VPM neurons exhibited smaller response magnitudes and greater spontaneous firing rates than those of their PrV inputs, but that both populations were similarly well tuned for stimulus direction. In addition, fewer VPM (74%) than PrV neurons (93%) responded with sustained, or tonic, discharges during the plateau phase of the stimulus. Neurons in both populations responded most robustly to deflections of a single, “principal whisker” (PW), and the majority of cells in both PrV (90%) and VPM (73%) also responded to deflections of at least one adjacent whisker (AW). AW responses in both nuclei occurred on average at longer latencies and were more temporally dispersed than PW responses. Lateral inhibition, as evidenced by AW-evoked activity suppression, was rare in PrV but prevalent in VPM. In both nuclei, however, suppression was weak, with AW responses being on average excitatory. Our results suggest that the receptive-field structures and response properties of individual VPM neurons can be explained in large part by input from one or a small number of PrV neurons, but that intrathalamic mechanisms act to further transform the afferent signal.