Feedforward Inhibition Determines the Angular Tuning of Vibrissal Responses in the Principal Trigeminal Nucleus

Abstract

Trigeminal neurons that relay vibrissal messages to the thalamus receive input from first-order afferents that are tuned to different directions of whisker motion. This raises the question of how directional tuning is maintained in central relay stations of the whisker system. In the present study we performed a detailed analysis of the angular tuning properties of cells in the principal trigeminal nucleus of the rat. We found that stimulus direction systematically influences response latency, so that the degree of directional tuning and the preferred deflection angle computed with first-spike latency yielded results nearly similar to those obtained with spike counts. Furthermore, we found that inhibition sharpens directional selectivity, and that pharmacological blockade of inhibition markedly decreases the angular tuning of cellular responses. These results indicate that the angular tuning of cells in the first relay station of the vibrissal system is determined by fast feedforward inhibition, which shapes excitatory inputs at the very beginning of synaptic integration.

Comparison of latency and rate coding for the direction of whisker deflection in the subcortical somatosensory pathway

“…It is well-established from previous work that neurons at all levels of the lemniscal whisker pathway code at least some information about the direction of whisker deflection by a spike-count code (Bale and Petersen 2009; Bellavance et al 2010;Lichtenstein et al 1990;Simons and Carvell 1989;Zucker and Welker 1969). Our findings show that a substantial subset of neurons code significant, additional information by latency.…”

“…Our findings show that a substantial subset of neurons code significant, additional information by latency. Evidence that neurons in the principal trigeminal nucleus also exhibit direction-tuned latencies (Bellavance et al 2010) together with our finding that latency information is present in a subset of VPM neurons indicates that the latency code is preserved across the subcortical lemniscal pathway. Our result that latency information is already present in the ganglion indicates that this latency code arises from receptor mechanisms in the whisker follicle.…”

“…Our result that latency information is already present in the ganglion indicates that this latency code arises from receptor mechanisms in the whisker follicle. However, the latency code is further sharpened by inhibitory circuitry in the brain stem (Bellavance et al 2010). Most of the information that cortical neurons convey about direction is present in the first poststimulus spike (Bale and Petersen 2009), suggesting the possibility of a cortical latency code [as has previously been reported for other parameters of whisker stimulation (Panzeri et al 2001;Petersen et al 2002b)].…”

“…Neurons at all levels of the whisker pathway convey information about direction by means of variations in spike count (Axelrad et al 1976;Waite 1973;Zucker and Welker 1969). Recently, it was shown that neurons in the principal nucleus of the brain stem also convey directional information by means of latency (Bellavance et al 2010). However, it is not known whether direction information is available from spike timing at other stages of the pathway nor is it known, quantitatively, how the information available from spike timing compares with that available from spike count.…”

Coding of Apparent Motion in the Thalamic Nucleus of the Rat Vibrissal Somatosensory System

“…In particular, these cross-whisker responses would rely heavily on excitatory inputs to PrV from the caudal subnucleus (spVc) and on inhibitory modulation by the interpolar subnucleus (spVi) (Furuta et al, 2008). The spVi modulation would contribute to sharpen directional tuning (Bellavance et al, 2010) and generate detectable cross-whisker suppression already in PrV Timofeeva et al, 2004). It would be most interesting to record in the trigeminal nuclei to establish whether selectivity to global motion is already present at that stage.…”