Response properties of mouse trigeminal ganglion neurons

Abstract

We used controlled whisker deflections to examine the response properties of 208 primary afferent neurons in the trigeminal ganglion of adult mice. Proportions of rapidly adapting (RA, 47%) and slowly adapting (SA, 53%) neurons were equivalent, and most cells had low or no spontaneous activity. We quantified angular tuning and sensitivity to deflection amplitude and velocity. Both RA and SA units fired more frequently to larger deflections and faster deflections, but RA units were more sensitive to differences in velocity whereas SA units were more sensitive to deflection amplitudes. Almost all neurons were tuned for deflection angle, and the average response to the maximally effective direction was more than fourfold greater than the average response in the opposite direction; SA units were more tuned than RA units. Responses of primary afferent whisker-responsive neurons are qualitatively similar to those of the rat. However, average firing rates of both RA and SA neurons in the mouse are less sensitive to differences in deflection velocity, and RA units, unlike those in the rat, display amplitude sensitivity. Subtle observed differences between mice and rats may reflect greater mechanical compliance in mice of the whisker hairs and of the tissue in which they are embedded.

Figure 1

PSTHs depicting the response of a typical rapidly adapting neuron (A) and slowly adapting neuron (B) to whisker deflections in different directions. PSTHs having 1 ms bins were constructed from responses to ten deflections in each of the eight directions indicated (see figurine for orientation). The bottom-most PSTH is the response accumulated over all stimuli/angles. The duration of each trial was 500 ms with the ramp-and-hold stimulus centered in time (indicated at the bottom). Scale: horizontal = 50 ms; vertical = 8 spikes for the individual angle PSTHs, 35 spikes for the RA All-angle PSTH and 30 for the SA All-angle PSTH. Below each set of PSTHs is a polar plot constructed from responses evoked by stimulus onset; the maximal angle response is indicated in spikes/stimulus. Arrows indicate vector angle and magnitude.

Figure 2

(A) Population PSTHs constructed from the responses of 98 RA neurons accumulated overall deflection angles. Inset shows population 70 ms long PSTHs constructed from the ON response of RA units in the mouse (black) and rat (gray); PSTHs were scaled to probability of spike per 1 ms bin. Stimulus onsets and offset occur at the 146 and 350 ms bins. (B) Population PSTHs from 110 SAs; conventions as in panel A. (C) Bar graphs illustrating the proportion of trigeminal ganglion neurons that display different levels of spontaneous firing. (D) Scatter plots of the relationship between spontaneous activity and maximum-angle plateau firing rates of SA neurons.

Figure 3

Average ON and OFF response magnitudes evoked by each cell's maximally effective (Max) angle and averaged over all eight angles (Mean) for All neurons, 98 RA neurons and 110 SA neurons. Error bars=standard error of the mean.

Figure 4

Angular tuning and directional consistency of RA and SA neurons. (A) Population polar plots of RA (black; n98) and SA (gray; n110) units. For each cell ON response magnitudes were normalized to the response evoked by the maximally effective angle. Individual polar plots were then rotated downwards and averaged across the population. (B) Vector angles and magnitudes calculated population polar plots in panel A. (C) Bar graphs depicting average angular tuning indices, calculated as the ratio of the maximal angle response (in spikes/stimulus onset) to the mean over all eight angles. Error bars=standard error of the mean. Asterisk denotes a statistically significant difference (p<0.05) between the two populations. (D) Directional consistency indices. SA neurons are more likely to respond to a given deflection direction regardless of the starting position of the deflection (see text).

Figure 5

Amplitude and velocity sensitivity of 23 SA (panel A) and 21 RA (panel B) neurons. Population PSTHs having 1 ms bins depicting responses evoked at two deflection amplitudes and velocities. PSTHs (time 0) are aligned to stimulus onsets; ramp durations are considerably longer for the 1.0mm amplitude, 10 mm/s stimuli. Arrows indicate peak of the PSTHs for 10 mm/s deflections. Insets for the 10 mm/s PSTHs in B show the small RA ON responses at higher resolution. The top panel (12-fold magnification of y-axis). Inset in the left lower panel (1000 mm deflection at 100 mm/s) shows overlaid population PSTHs ON responses to 1000 mm (black) and 500 mm (gray) deflections. For each neuron, the whisker was deflected ten times in its maximally effective direction.

Figure 6

Stimulus-response functions of 23 SA and 21 RA calculated over different response windows (see legend in figure panels). (A, B) Whisker was deflected with different velocities at an amplitude of 1.0 mm. (C, D) Whisker was deflected 0.5 or 1.0 mm at 100 mm/s. Error bars=standard error of mean.