SA1 and RA afferent responses to static and vibrating gratings

Abstract

SA1 and RA afferent fibers differ both in their ability to convey information about the fine spatial structure of tactile stimuli and in their frequency sensitivity profiles. In the present study, we investigated the extent to which the spatial resolution of the signal conveyed by SA1 and RA fibers depends on the temporal properties of the stimulus. To that end, we recorded the responses evoked in SA1 and RA fibers of macaques by static and vibrating gratings that varied in spatial period, vibratory frequency, and amplitude. Gratings were oriented either parallel to the long axis of the finger (vertical) or perpendicular to it (horizontal). We examined the degree to which afferent responses were dependent on the spatial period, vibratory frequency, amplitude, and orientation of the gratings. We found that the spatial modulation of the afferent responses increased as the spatial period of the gratings increased; the spatial modulation was the same for static and vibrating gratings, despite large differences in evoked spike rates; the spatial modulation in SA1 responses was independent of stimulus amplitude over the range of amplitudes tested, whereas RA modulation decreased slightly as the stimulus amplitude increased; vertical gratings evoked stronger and more highly modulated responses than horizontal gratings; the modulation in SA1 responses was higher than that in RA responses at all frequencies and amplitudes. The behavioral consequences of these neurophysiological findings are examined in a companion paper.

FIG. 1

Top: bottom view of the 400-probe stimulator with every 4th probe included to show the internal structure. In the working stimulator, the pins, 0.3 mm in diameter and spaced 0.5 mm center-to-center, are driven by 400 motors, each independently controlled by computer. The range of motion of each probe is ~2 mm. The stimulator allows for the generation of arbitrary spatiotemporal stimuli. Bottom: illustrations of gratings at spatial periods 2 and 6 mm at every possible spatial offset. The 2-mm grating was offset by 0, 0.5, 1, and 1.5 mm; the 6-mm grating was offset by 0, 0.5, 1, 1.5, 2, 2.5, 3, 3.5, 4, 4.5, 5, and 5.5 mm.

FIG. 2

Spatial profile of the response of an SA1 (19_00) and an RA (11_03) fiber to gratings that vary in vibratory frequency and spatial period. Each colored trace corresponds to a different vibratory frequency (0 Hz refers to static gratings). Spike rates at each frequency are normalized by the mean spike rate at that frequency to show the similarity of the spatial profiles across vibratory frequencies. One cycle of each stimulus is shown in gray at the bottom of the figure. Afferent response are spatially modulated in a stimulus-dependent manner. The traces at different frequencies overlap to a large extent, suggesting that the degree of spatial modulation is independent of stimulus frequency. Insets: spatial modulation as a function of spatial period.

FIG. 3

Top: effect of spatial period on spatial modulation. Left: each trace corresponds to a temporal frequency. Spatial modulation increased with spatial period at all frequencies for both types of fibers. Right: modulation, averaged across frequencies, as a function of spatial period for SA1 (blue) and RA (red) fibers. SA1 modulation was higher than its RA counterpart at all frequencies and spatial periods. Bottom: effect of vibratory frequency on spatial modulation. Left: each trace corresponds to a spatial period, indicated to its right. Spatial modulation increased slightly with vibratory frequency. Right: Modulation, averaged across spatial periods, as a function of frequency. Temporal frequency had little systematic effect on spatial modulation (N_SA = 11, N_RA = 8).

FIG. 4

Spatial modulation as a function of spatial period before (- - - and · · ·) and after (—) the application of the anti-aliasing factor. The effects of aliasing are negligible for spatial periods ≥4 mm.

FIG. 5

Firing rates as a function of vibratory frequency for SA1 (left) and RA fibers. Each trace corresponds to a spatial period. The amplitudes were chosen such that the stimuli were equated in subjective intensity, as measured in a companion psychophysical study (Bensmaia et al. 2005). Firing rates evoked by gratings vibrating at 40 Hz were depressed for both SA1 and RA fibers. The specific reason for the drop in spike rate at 40 Hz is unclear. However, the decline is likely due to the way in which signals from the relevant populations of mechanoreceptive afferent fibers are combined to convey information about the subjective magnitude of the stimulus. When stimuli were set relative to the sensitivity of individual fibers, the neural response was no longer anomalous at 40 Hz.

FIG. 6

Effect of vibratory amplitude on spatial modulation. Each trace corresponds to a vibratory frequency. The orientation of the gratings was parallel to the axis of the finger and their spatial period was 6 mm. The intensity levels are expressed in decibels relative to the amplitudes matched for subjective intensity (0dB re: max corresponds to the amplitudes denoted by · · · in Fig. 7). Increasing the stimulus amplitude had no effect on the spatial modulation of SA1 responses. On the other hand, RA modulation decreased with amplitude (N_SA = 9, N_RA = 5).

FIG. 7

Stimulus intensities used in the 2 sets of recordings. · · ·. the stimulus intensities that were matched for subjective magnitude (Bensmaia et al. 2005). - - - and —, show the mean stimulus intensities when these were set according to SA1 and RA sensitivity, respectively (N_SA = 6, N_RA = 4). Inset: the mean spike rates for neurons of each type as a function of vibratory frequency.

FIG. 8

Top: Mean spatial modulation of responses evoked by horizontal gratings (oriented perpendicular to the axis of the finger) vs. the mean modulation of responses evoked by vertical gratings (oriented parallel to the axis of the finger). RA modulation exhibited a strong anisotropy, whereas SA1 modulation did not. Bottom: mean firing rates evoked by vertical gratings vs. mean firing rates evoked by horizontal gratings at each vibratory frequency for all the fibers. For both types of fibers, firing rates exhibit a slight but significant tendency to lie below the diagonal, indicating an effect of grating orientation on the strength of the response (N_SA = 11, N_RA = 8).

FIG. 9

Population analysis. Top: the spatial profile of the summed responses of 11 SA1 and 8 RA fibers. Each trace corresponds to a vibratory frequency (see bottom for legend); different symbols denote different spatial periods. Spike rates at each frequency are normalized by the mean spike rate at that frequency to show the similarity of the spatial profiles across vibratory frequencies. The gray outline at the bottom of each plot shows the stimulus profile. Bottom: the spatial modulation as a function of spatial period, with vibratory frequency as a parameter. Spatial modulation increases monotonically with spatial period. Furthermore, vibratory frequency has no effect on spatial modulation, as is suggested by the spatial profiles shown (top).

FIG. 10

Population analysis of the effect of amplitude on spatial modulation. Gratings with a spatial period of 6 mm are presented at 3 intensities and 6 vibratory frequencies. The spatial profiles of the responses evoked by each stimulus are aligned and summed across fibers. To facilitate comparison of the spatial profiles across conditions, we divide the spike rates elicited by gratings at a given amplitude and frequency by the mean firing rate across offsets at that amplitude and frequency. Grating amplitude has no effect on SA1 modulation whereas RA modulation decreases slightly but significantly as amplitude increases. The reason for the high RA modulation at 40 Hz and −10dB is unclear. This data point is likely a statistical anomaly in the data as no single fiber is responsible for this large, seemingly stimulus-dependent modulation (N_SA = 9, N_RA = 5).

FIG. 11

Anisotropy in SA1 (left) and RA (right) population responses. There is a strong and significant anisotropy in SA1 and RA responses to static and vibrating gratings (compare regression line with unity slope). Specifically, the spatial modulation of the responses to vertical gratings is greater than the spatial modulation of the responses to horizontal gratings for both SA1 and RA fibers. The effect of grating orientation is much stronger at the population level than it is at the level of individual fibers for SA1 fibers (N_SA = 11, N_RA = 8)).

FIG. 12

Estimated amplitude of a sinusoid of amplitude 1 as a function of the sampling frequency f_s (expressed in samples per cycle). The modulation depth of afferent responses to the smallest gratings would be underestimated by an average of 35% given that only 2 samples are obtained per stimulus cycle.