Experimental setup.

A. Receptive field center locations shown on a standardized fingertip for all first-order tactile neurons included in the study, divided by neuron type. B. The flat stimulus surface was centered at the standard site of stimulation and oriented such that its tangential plane was parallel to the flat portion of skin on the fingertip. The surface maintained contact with the skin at a force of 0.2 N in intertrial periods. Force stimuli were superimposed on this background contact force and were delivered in the normal direction (N), and at an angle of 20 degrees to the normal with tangential components in the distal (D), radial (R), proximal (P) and ulnar (U) directions, as indicated by the five arrows in the lower panel.

Stimulation sequence exposes fingertip viscoelasticity.

A. Trial order for the entire regular sequence, which repeats fingertip loadings in five different force directions in a fixed order, implying that loadings in each direction received the same stimulation history. Force (red lines) and contactor position (black lines) are shown along the normal (z), distal/proximal (y), and ulnar-radial (x) axes, while recording action potentials from a single exemplary SA-1 neuron (bottom trace). B. Average contactor position in the tangential plane for all trials in the regular sequence across all recorded neurons (and thus fingertips). The colored segments of the curves indicate the protraction phase for each of the five force directions, while other phases of the fingertip loading (plateau, retraction) and the inter-stimulus period are shown in grey. Dashed lines show the directions in which the tangential force components were applied. C. Trial order for the entire irregular sequence, where force directions are varied such that trials in each stimulation direction were preceded by loading in each of the five directions once. Same neuron (and fingertip) as in A. D. Average contactor position in the tangential plane for the irregular sequence. Same format as in B. E. Contactor position in the tangential plane at the start of (filles circles) and during the force protraction phase (colored lines) per force direction, referenced to the fingertip position at rest (gray marker). Same trials as in D, but different force directions are shown in separate panels for better visibility.

Influence of preceding loading direction on fingertip deformation and neural responses.

A. Contact position along the x, y, and z axes (see Fig. 1B) as a function of time super-imposed for all five trials with loading in the distal direction (‘test trial’) as well as the respective previous loading (‘preceding trial’) in the regular (left column) and the irregular (right column) sequence. Vertical dashed lines mark transitions between loading phases (Pr: protraction, Pl: plateau, Re: retraction phase, Int: intertrial period). The yellow shaded area indicates the protraction phase of the test trials. Each trace is colored according to the force direction of the previous loading. Data was recorded from a neuron whose response is shown in B. B. Dots (top) represent action potentials recorded from an FA-1 neuron for each trial, whose contactor movements are shown in A. The superimposed traces below represent the corresponding firing rate profiles, defined as the recip-rocal of the interval between subsequent action potentials. Color coding as in A. C,D. Exemplary responses of one SA-1 (C) and two SA-2 neurons (D) to force loadings corresponding to those in A. All neurons show higher variability in their firing rate profiles during test trials in the irregular compared to the regular sequence.

Increased variability in neural responses and fingertip deformations in the irregular sequence.

A. Standard deviation of neuronal instantaneous firing rates as a function of time during test trials in each loading direction in the regular (dashed lines) and irregular (solid lines) sequences. Data averaged across neurons of each type and all loading directions. Shaded areas indicate SEM. Vertical dashed lines mark transitions between loading phases as in Fig. 3A and stars indicate phases where there was a significant difference between regular and irregular sequences at p < 0.05. B. Average instantaneous firing rates for the regular and irregular sequence as a function of time. Dashed black lines indicate the force profile of the fingertip loading. Note that the average firing rates are almost identical in the regular and irregular sequence. C. Standard deviation of tangential (2D) contactor position for the regular and irregular sequences. D. Standard deviation of contactor velocities (black lines) and average contactor velocity (purple lines) for the regular and irregular sequences.

Information about current and previous force direction during the force protraction phase.

A. Average mutual information about force direction for FA-1 (left), SA-1 (middle), and SA-2 (right) neurons as a function of time during the protraction phase in the irregular sequence. Information is shown for the current trial (solid orange line) or the preceding trial (solid yellow line) and is compared to the regular sequence (dotted black line). Grey dashed lines denote the stimulus force profile. B. Examples of mutual information curves (top) and spike trains (bottom) for three individual neurons with different response behaviors. Information curves as in A. Spike trains are split by current force direction with spikes colored by previous force direction. Examples are of a neuron with mixed tuning (left), a neuron that predominantly signals information about the previous stimulus (middle), and a neuron that primarily signals information about the current force direction (right). C. Proportion of FA-1 (blue), SA-1 (green), and SA-2 (purple) neurons showing different response behaviors during the protraction phase. Most neurons of either class signaled predominantly the current force direction, but around 35% of neurons either signaled the previous force direction or showed mixed response behavior. D. Information transmitted about force direction for neurons tuned to the current force direction for the regular and the irregular sequence. Information decreases considerably for the irregular sequence, even in neurons responding strongly to the current direction.

SA-2 neurons signal information about previous forces in the absence of loading.

A. Spike raster plots for three SA-2 neurons recorded during the interstimulus periods of the irregular sequence. Each dot represents an action potential, and the colors indicate the preceding force direction. Note that the responses differ systematically based on the previous force direction. Bottom panel: To illustrate the effect of previous force direction on the deformation state of the fingertip during the interstimulus period, the average contactor position in the ulnar-radial (U-R) direction during the corresponding irregular stimulation sequences is shown (on the same time scale as upper panels). Colors indicate the force direction in the preceding trial corresponding to the color coding in A. B. Average mutual information about force direction in the test trial (orange line) or the preceding trial (yellow line) during the interstimulus period and during the subsequent protraction phase for the same three neurons shown in panel A. C. Average mutual information across all SA-2 neurons active in the absence of load during the interstimulus period.

Continuous representation of fingertip viscoelastic state in the SA-2 population.

A. Colored dots indicate tangential contactor positions (top) and their representation in the SA-2 population signal (bottom) at three different times: the middle of the interstimulus period (−0.125 s), the end of the interstimulus period (0 s) and the end of the subsequent protraction phase (0.125 s). The colors of the markers denote the force direction in the directly preceding trial. Contactor position is the two-dimensional position in the tangential plane. SA-2 representations are derived from average spike trains distances across the different trials, visualized in a two-dimensional space using multidimensional scaling and aligned with the contactor positions using Procrustes analysis (see Methods for details). B. Averaged total variance and within-direction variance for contactor position and SA-2 population signal representations at the same three time points as in A. As illustrated by the dashed ellipses in A, total variance denotes the two-dimensional variance across all trials, while within-direction variance denotes the variance for trials belonging to the same preceding force direction. Higher total than within-direction variance indicates that data for trials in the same preceding direction are more clustered than data for trials in all preceding directions, which is required for discrimination of preceding force direction.