Temporal coherency of mechanical stimuli modulates tactile form perception

Abstract

The human hand can detect both form and texture information of a contact surface. The detection of skin displacement (sustained stimulus) and changes in skin displacement (transient stimulus) are thought to be mediated in different tactile channels; however, tactile form perception may use both types of information. Here, we studied whether both the temporal frequency and the temporal coherency information of tactile stimuli encoded in sensory neurons could be used to recognize the form of contact surfaces. We used the fishbone tactile illusion (FTI), a known tactile phenomenon, as a probe for tactile form perception in humans. This illusion typically occurs with a surface geometry that has a smooth bar and coarse textures in its adjacent areas. When stroking the central bar back and forth with a fingertip, a human observer perceives a hollow surface geometry even though the bar is physically flat. We used a passive high-density pin matrix to extract only the vertical information of the contact surface, suppressing tangential displacement from surface rubbing. Participants in the psychological experiment reported indented surface geometry by tracing over the FTI textures with pin matrices of the different spatial densities (1.0 and 2.0 mm pin intervals). Human participants reported that the relative magnitude of perceived surface indentation steeply decreased when pins in the adjacent areas vibrated in synchrony. To address possible mechanisms for tactile form perception in the FTI, we developed a computational model of sensory neurons to estimate temporal patterns of action potentials from tactile receptive fields. Our computational data suggest that (1) the temporal asynchrony of sensory neuron responses is correlated with the relative magnitude of perceived surface indentation and (2) the spatiotemporal change of displacements in tactile stimuli are correlated with the asynchrony of simulated sensory neuron responses for the fishbone surface patterns. Based on these results, we propose that both the frequency and the asynchrony of temporal activity in sensory neurons could produce tactile form perception.

Figure 1

Geometric profile of tactile stimuli used in psychological experiments. (a) Geometric configuration of the fishbone tactile illusion (FTI) pattern. This geometry comprises a central strip (the spine of the fishbone) and ribs (adjacent areas). In the experiment, the central strip width was constant, but the interval between ribs was varied to change the perceived stimulus temporal frequency in the adjacent rib areas. (b) Schematic of the passive pin matrix. This instrument comprises pins of 0.8 or 1.8 mm in diameter, with a pin spacing of 1.0 or 2.0 mm. The pins can follow the surface geometry beneath the pin matrix in the vertical direction and suppress the horizontal displacement. (c) We prepared three pin matrices with multiple pin configurations; $d_1$ indicates the diameter of the contact area to the fingertip, and $d_2$ indicates the diameter of the contact area to the surface geometry.

Figure 2

The touch condition affects the mean probability of perceiving a more indented (hollower) surface geometry. Participants examined a pair of different fishbone patterns (36 combinations in total), and they indicated which pattern was more indented in each trial under a certain touch condition (bare finger or utilizing pin matrix (PM) 1, 2, or 3. Psychological data showed different probabilities of answering “more indented” than other rib intervals ($N=12$). The horizontal axis represents the rib interval in the fishbone surface pattern. Under bare-finger conditions, the probability increased between 0.2 and 0.4 mm and gradually decreased when the rib interval exceeded 1.4 mm. The probability trace was exaggerated under pin matrix conditions. Specifically, the probability steeply increased between 0.2 and 0.4 mm and decreased as the rib interval increased under touch conditions with PM1, except for the steep dips at rib intervals of 1.0 and 2.0 mm. This trend was more enhanced under touch conditions with PM2 and PM3. In particular, the probability of more indented was abruptly decreased at the 1.0 mm rib interval. Mean estimates of probability are plotted, and error bars indicate $95\%$ confidence intervals.

Figure 3

Mathematical model. (a) A pin of the pin matrix produces skin deformation that leads to (b) opening a mechanosensitive ion channel in a mechanoreceptor. (c) Change in receptor potential due to the mechanoreceptor’s physiological response is conveyed electrically to a spike initiation site (d) where four mechanoreceptors are connected. This mechanoreceptor-sensory neuron system works as (e) a responsive receptive field distributed uniformly in the fingertip. After calculating the responses of multiple receptive fields, both the firing rate of each receptive field and the firing timing synchronicity (the Shannon entropy) over multiple receptive fields are calculated. The concept of the process of mechanoreception is developed based on proposals in the existing literature^,,.

Figure 4

Numerical results of receptive fields at different time points. (a) Initial setup. (b–e) Four successive time moments [$t=$518 (b), 519 (c), 520 (d), and 521 ms (e)], where typical responses of mechanoreceptors to mechanical input signals are shown. Large circles represent receptive fields, whose action potential activities v(t) are indicated by the color bar; red and blue represent the excited and the resting state, respectively. Each receptive field has a neuron that integrates signals from mechanoreceptors, which are represented by small circles. The activities of the mechanoreceptors and the conductance g(t) are represented by the grayscale color. Connections between a receptive field and mechanoreceptors are indicated by lines. After calculating the responses of multiple receptive fields, both the firing rate of each receptive field and the firing timing synchronicity (the Shannon entropy) over multiple receptive fields are calculated. Supplementary Videos 1–3 demonstrate the time-lapse results of how 72 receptive fields responded to the fishbone pattern of 1.0 mm and 0.4 mm intervals under PM1 and PM2 conditions.

Figure 5

Detailed analysis of numerical results. (a) In our model, the sensory neuron responds vigorously to the fishbone patterns when the rib interval is 0.4 mm for all pin matrix conditions. (b) Calculated temporal asynchrony of action potentials. There are sudden dips in the calculated values at rib intervals of 1.0, 2.0 and 3.0 mm.

Figure 6

Calculated incoherency of mechanical displacements through pin matrices. The temporal incoherency of (a) height and (b) height change was indexed by the Shannon entropy. (c) Relationship between incoherency of tactile stimuli through pin matrices and temporal asynchrony of action potentials for different pin matrix conditions.

Figure 7

A model of tactile form perception in fingertips. Both the frequency and the temporal asynchrony of action potentials may contribute to tactile form perception. If the temporal asynchrony of action potentials were to decrease, a perceiver would report attenuated depth of perceived surface indentation at the backbone of fishbone patterns.