How Tactile Afferents in the Human Fingerpad Encode Tangential Torques Associated with Manipulation: Are Monkeys Better than Us?

Responses of individual afferents to torque with 2 N background normal force. A, Example torque stimuli from single trials of 7.5 mNm in clockwise (blue) and anticlockwise (red) directions and to normal force only (black trace). B–D, Responses from three individual SA-II afferents with various response profiles showing enhanced discharge rates in response to one torque direction and suppressed discharge rates to the opposite torque direction (B, C), or suppressed discharge rates to both torque directions (D). Instantaneous rate from an (E) SA-I afferent and (F) FA-I afferent that had an enhanced discharge rates in response to both torque directions. Three torque magnitudes of 3.5, 5.5, and 7.5 mNm were applied in each direction, but only responses to 7.5 mNm torque are included here, for clarity. Vertical gray dashed lines separate the torque phases: loading (L), plateau (P), and unloading (U). G, Histograms of the number of impulses per 100-ms bins in response to 7.5 mNm torque in either direction (example torque traces are shown above). Responses are represented as Z-scores of the difference in the number of impulses between torque trials and normal force only (0 mNm torque) trials. Each afferent tested in two directions is represented with anticlockwise and clockwise torque responses on the left and right sides respectively, one for each torque direction. Raster rows filled in with light gray indicate afferents in which one torque direction was not tested. L, loading phase; P, plateau phase; U, unloading phase.

Effect of torque on SA-II afferents in each torque phase. A, The receptive field center location (black dots) of each SA-II afferent and the direction in which its response was scaled by torque are plotted for each torque phase across a standard fingertip. Red and blue arrows indicate positive discharge rate change in anticlockwise and clockwise directions, respectively, and black arrows indicate negative change in discharge rate (suppression) in the respective direction. Black cross indicates torque stimulus rotational center and the gray circle indicates the approximate stimulus contact area. B, The proportion of SA-II afferents with scaled mean discharge rates in response to torque, with 2 N background normal force, is shown in darker columns. Red and blue bars represent afferents sensitive to anticlockwise and clockwise directions, respectively; gray bars represent afferents sensitive in at least one of the torque directions. The lighter colored stacked columns show the number of afferents that had nongraded responses to torque. Colored numbers above indicate the number of afferents with torque responses and in brackets the proportion of these that only showed nongraded responses.

The effect of background normal forces on SA-II afferent responses to torque. A, Responses to torque from the same single afferent are shown when the torques were applied with background normal forces increasing from 2 to 4 N (example torque at the top). The first SA-II afferent shows a typical response profile with decreasing torque sensitivity as background normal force increases. B, Torque responses from another afferent show sensitivity to clockwise torques that remained similar with increasing background normal forces but, in response to anticlockwise torques, responses transitioned from positive to negative change in discharge rate with increasing background normal force. See Figure 2 legend for detailed description.

Effect of normal force and receptive field center location on SA-II afferent's torque responses. A, The proportion of SA-II afferents that showed responses that were scaled by torque in at least one direction as measured by mean discharge rate, for each normal force. B–D, SA-II torque sensitivities with 2, 3, and 4 N background normal forces, separated by afferents that had significantly (B) increasing or (C) decreasing torque sensitivity with increasing background normal force, or were unaffected by background normal force (D). Red and blue semi-circles indicate that anticlockwise and clockwise torque sensitivity, respectively, was significantly increasing or decreasing with increasing background normal force. Black semi-circles indicate no influence in the respective direction. Only afferents that were tested with torque at each of the three normal forces are included. Values from individual afferents are connected by lines. The fingertip contours to the right of panels indicate only approximate receptive field center locations of these afferents as SA-II afferents have large receptive fields with diffuse borders.

Effect of torque on SA-I afferents in each torque phase. A, The receptive field center location (black dots) of each SA-I afferent and the direction in which its response was scaled by torque are plotted for each torque phase across a standard fingertip. B, C, The proportion of SA-I afferents that showed responses that were scaled by torque in at least one direction are shown in darker columns, as measured by (B) spike count and (C) first spike latency, with 2 N background normal force. Stacked columns in a lighter color in B, C show the number of afferents that had nongraded responses to torque. Colored numbers above indicate the number of afferents with torque responses and in brackets the proportion of these that only showed nongraded responses. See Figure 3 legend for detailed description.

Effect of normal force and receptive field center location on SA-I afferent's torque responses. A, B, The proportion of afferents that were scaled by torque in at least one direction as measured by (A) spike count and (B) first spike latency for each normal force. C–E, SA-I torque sensitivities with 2, 3, and 4 N background normal forces, separated by afferents that had significantly increasing (C) or decreasing (D) torque sensitivity with increasing background normal force, or were unaffected by background normal force (E). F, Sensitivity values from the torque loading phase are shown for SA-I afferents against their receptive field center distance from the stimulus rotational center. S_T was calculated from the maximum torque sensitivity value between either clockwise or anticlockwise torque directions. SA-I afferents showed increasing torque sensitivity with distance from the stimulus rotational center, up to 12 mm, and the most pronounced effect was from 6 to 12 mm. SA-I afferents with receptive field center >15 mm from the stimulus rotational center were unresponsive to torque. Vertical dashed line indicates the edge of the probe. Inset to the right shows a radar chart of the torque sensitivity in impulses mNm⁻¹ s⁻¹ (sensitivity increments shown at 0.325 and 0.75 impulses mNm⁻¹ s⁻¹) of afferents with receptive field centers in each quadrant of the fingertip, for each of the three background normal forces. Quadrants are labeled D, distal, P, proximal, U, ulnar, and R, radial. See Figure 5 legend for detailed description.

The effect of torque on FA-I afferent responses. A, The receptive field center location (black dots) of each FA-I afferent and the direction in which its response was scaled by torque are plotted for each torque phase across a standard fingertip. B, C, The proportion of FA-I afferents that showed responses scaled by torque are shown in darker colors based on (B) mean discharge rate and (C) first spike latency, with 2 N background normal force. Stacked columns in a lighter color in B, C show the number of afferents that had nongraded responses to torque. Colored numbers above indicate the number of afferents with torque responses and in brackets the proportion of these that only showed nongraded responses. See Figure 3 legend for detailed description.

The effect of normal force and receptive field center location on FA-I afferent's torque responses. A, B, The proportion of afferents that were scaled by torque in at least one direction as measured by (A) mean discharge rate and (B) first spike latency for each normal force. All three metrics were calculated in the loading and unloading phases, as FA-I afferents were unresponsive to torques in the plateau phase. C, D, FA-I torque sensitivities with 2, 3, and 4 N background normal forces, separated by afferents that had significantly decreasing torque sensitivity with increasing background normal force (C), or were unaffected by background normal force (D). E, Sensitivity values from the torque loading phase are shown for FA-I afferents against their receptive field center distance from the stimulus rotational center. FA-I afferents were mostly unresponsive to torque within 3 mm of the stimulus rotational center. With 2 N background normal force, FA-I afferents showed the highest torque sensitivity when their receptive field centers were between 3 and 9 mm from the stimulus rotational center. Vertical dashed line indicates the edge of the probe. Inset above shows a radar chart of the torque sensitivity in impulses mNm⁻¹ s⁻¹ (sensitivity increments shown at 0.5 and 1.0 impulses mNm⁻¹ s⁻¹) of afferents with receptive field centers in each quadrant of the fingertip, for each of the three background normal forces. Quadrants are labeled D, distal, P, proximal, U, ulnar, and R, radial. See Figure 5 legend for detailed description.