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.

Figure 1.

Response of PrV cells to controlled whisker deflection. PSTHs and the polar plot in A show responses of a SA unit to directional deflection of whisker D3. Normalized number of spikes per deflection within a time window of 10 ms after stimulus onset was used to build the polar plot; the arrow is the vector sum of angular responses. Traces and raster display in B show ON responses of a representative SA unit; note the very high frequency of action potentials (∼1 kHz); dotted line, stimulus waveform. C, Distribution of tuning index across a population of 16 SA and 27 RA units. Scatter plots in D show correlation between tuning indices computed from normalized values of spike counts per stimulus (10 ms time window) and first-spike latency (regression lines: SA, y = 1.21x − 0.22; RA, y = 1.02x − 0.06; RA and SA, y = 1.02x − 0.07). E, Circular-circular correlograms between preferred deflection angle computed as the vector sum of normalized values of spike counts per stimulus (10 ms time window) and first-spike latency. The gray line is the curve of a perfect correlation. In these circular plots, the vector sum derived from first-spike latency is represented on the circular axis, and the vector sum derived from spike counts is represented on the radial axis.

Figure 2.

Consistency of latency and spike-count directional tuning in PrV. The absolute angular difference between preferred directions estimated by the normalized values of first-spike latency and spike-counts is plotted as a function of the directional tuning index of PrV cells. Note the important difference for the least tuned cells (gray column). These three cells correspond to cells 39, 40 and 41 in supplemental Figure S1, available at www.jneurosci.org as supplemental material; they were excluded from the circular-circular correlation analysis (see Fig. 1E).

Figure 3.

Inhibition shapes the angular tuning of PrV neurons. Single cell PSTH in A and population PSTH in B show the suppression of background discharges induced by current injection (bar labeled DC under the PSTHs) when whiskers were deflected in the least effective direction. Intracellular recordings in C show a cell that responded with a spike on the crest of an EPSP at a deflection angle of 135°, and with an IPSP at a deflection angle of 45° (5 superimposed traces; note the opposite pattern of excitation/inhibition at stimulus offset).

Figure 4.

Blockade of inhibition reduces the angular tuning of PrV cells. Lesion of the inhibitory connections between the SpVi and the PrV significantly reduces the tuning index of PrV cells in comparison with normal rats (p < 0.0003 for the combined populations of SA and RA units; compare histograms in A with histograms of Fig. 1C). A short-lasting suppression of background discharges induced by current injection (bar labeled DC under the PSTHs) was still present when whiskers were deflected in the least effective direction (arrow in B). This population PSTH was built from the responses of 8 cells where no excitation preceded inhibition. C, When inhibition was fully blocked by local injection of gabazine and strychnine, tuning indices were further reduced with respect to normal rats (p < 0.0001), and background discharges were no more suppressed when whiskers were deflected in the least effective direction (D). Note that in B and D, the magnitude of ON and OFF responses was cropped.

Figure 5.

Broadening of the angular tuning domain of PrV cells after blockade of inhibition by gabazine and strychnine. Graphs show the average attenuation of response magnitude as a function of the angular distance from the best direction for RA (A) and SA (B) units (gray line, control rats; black line, rats injected with gabazine and strychnine).