Integration of vibrotactile frequency information beyond the mechanoreceptor channel and somatotopy

Abstract

A wide variety of tactile sensations arise from the activation of several types of mechanoreceptor-afferent channels scattered all over the body, and their projections create a somatotopic map in the somatosensory cortex. Recent findings challenge the traditional view that tactile signals from different mechanoreceptor-channels/locations are independently processed in the brain, though the contribution of signal integration to perception remains obscure. Here we show that vibrotactile frequency perception is functionally enriched by signal integration across different mechanoreceptor channels and separate skin locations. When participants touched two sinusoidal vibrations of far-different frequency, which dominantly activated separate channels with the neighboring fingers or the different hand and judged the frequency of one vibration, the perceived frequency shifted toward the other (assimilation effect). Furthermore, when the participants judged the frequency of the pair as a whole, they consistently reported an intensity-based interpolation of the two vibrations (averaging effect). Both effects were similar in magnitude between the same and different hand conditions and significantly diminished by asynchronous presentation of the vibration pair. These findings indicate that human tactile processing is global and flexible in that it can estimate the ensemble property of a large-scale tactile event sensed by various receptors distributed over the body.

Figure 1

Frequency interaction Across-finger. (A) Schematic views of the set up. (B) Trial sequences for each distractor conditions, when the target frequency was 30 Hz. When the target frequency was 240 Hz, the green waves representing 30-Hz vibrations and a blue wave representing 240 Hz vibration were interchanged. Participants were asked to make binary response (higher, lower) about the perceived vibration frequency of the second/comparison vibration compared to the first/target vibration on the target finger, and they received a feedback beep after each response. The frequency of the target and distractor vibration was 30 Hz or 240 Hz, while that of comparison was varied. The perceived intensity of all stimuli were kept at the same level. As for the distractor vibration, the same-frequency vibration was presented in the control condition, while the other was presented in the test condition. The onset and duration of target and distractor stimuli were the same. Note that participants were explicitly told which fingers were the target and distractor. The target finger was fixed during a block and counterbalanced across blocks. (C) Psychometric functions representing the proportion of trials where participants judged the frequency of the comparison vibration to be higher than that of the target, which was fixed at 30 Hz. Each data point represents the average across ten participants. Error bars indicate ±1 SEM. (D) PSEs of the target vibration of 30 Hz (top) and 240 Hz (bottom) for each distractor condition. N = 10. Error bars indicate ±1 SEM.

Figure 2

Frequency interaction Across-hand. (A) Schematic views of the set up. The distance between stimulators was the same to that in Across-finger conditions. (B) Psychometric functions of 30 Hz target condition. N = 10. Error bars indicate ±1 SEM. (C) Perceived frequency of the target vibration of 30 Hz (top) and 240 Hz (bottom). N = 10. Error bars indicate ±1 SEM.

Figure 3

Effect of onset timing in frequency interaction Across-finger. (A) Trial sequences for each distractor condition, when the target frequency was 30 Hz. The onset of the distractor vibration was 500 ms earlier than that of the target vibration, and offsets of these two vibrations were the same. (B) Psychometric functions of 30-Hz target condition. N = 10. Error bars indicate ±1 SEM. (C) Perceived frequency of the target vibration of 30 Hz (top) and 240 Hz (bottom). N = 10. Error bars indicate ±1 SEM.

Figure 4

Frequency interpolation between low- and high-frequency vibrations. (A) Trial sequence and typical example of the individual data. The target pair and the comparison pair were sequentially presented on two fingers. Participants were asked to make binary responses (higher, lower) about the perceived vibration frequency of the second pair compared to the first. In this experiment, participants were not informed of any possible differences between paired vibrations, and they did not receive any feedback signal after their response. For the target pair, the amplitude of the 30-Hz vibration was fixed, while that of 240-Hz vibration was varied (0.5, 1, or 2 relative to 30- Hz intensity, each called 30 Hz dominant, Equivalent, 240 Hz dominant) to evaluate the perceived frequency shift. The order of target and comparison pair was randomized in Across-finger and Physical-addition conditions. The finger on which the 30- or 240-Hz vibration was presented as a test pair was randomized in Across-finger and Across-finger-sequence conditions. (B) Experimental results and theoretical values. Green triangles with a dashed line represent averaged PSEs of the target pair of the Across-finger condition from 11 participants, blue circles with solid line represent that of Physical-addition condition from 11 participants, and red square with dotted line represent that of Across-finger-sequence condition from nine participants. Data are plotted against the weighted average of 30- and 240-Hz vibrations. The dot-dash line represents intensity-based linear interpolation of 30 and 240 Hz, while the two-dot chain line represents the geometric mean of 30 and 240 Hz. The black cross represents the predicted frequency of the sensor activity ratio of the two channels (equivalent to arrows in Fig. 6A). Error bars indicate ±1 SEM. (see the detail in main text).

Figure 5

Effects of somatotopic and environmental separations in interpolation experiments. (A) Schematic views of the setup. (B) Experimental results. Blue circles with a solid line represent averaged PSEs of the target pair of the Across-finger condition, green triangles with dashed line represent that of the Across-hand condition, and red squares with a dotted line represent that of the Across-hand-far condition, all averaged across ten participants. The dot-dash-line represents intensity-based linear interpolation of 30 and 240 Hz. N = 10. Error bars indicate ±1 SEM.

Figure 6

(A) Comparison between prediction of the ratio of channel activities and experimental results. Circles represent estimated channel activities for original stimuli in experiments based on sensitivity functions in previous research (1–5). Arrows represent predicted frequency from the ratio of RA and PC channel activities in the 30 Hz-dominant condition (blue arrow), Equivalent condition (green dashed arrow), and 240 Hz-dominant condition (red dotted arrow). These predicted frequencies are plotted as black crosses in Fig. 4B. Crosses represent matched/perceived frequencies in experiments, where each color represents each condition. (B) Similarity rating of the target pair and pair of sine-wave vibrations. Participants rated the similarity from 1 (dissimilar, easily-distinguishable) to 5 (very similar, indistinguishable). Note that 135 Hz (Red dotted line) is the weighted average of 30- and 240-Hz vibrations, though the rating distribution of this condition is far different from that of the target pair of Across-finger/hand or Physical-addition. N = 8. Error bars indicate ±1 SEM.