El-Mehdi Meftah

Tactile Speed Scaling: Contributions of Time and Space

A major challenge for the brain is to extract precise information about the attributes of tactile stimuli from signals that co-vary with multiple parameters, e.g., speed and texture in the case of scanning movements. We determined the ability of humans to estimate the tangential speed of surfaces moved under the stationary fingertip and the extent to which the physical characteristics of the surfaces modify speed perception. Scanning speed ranged from 33 to 110 mm/s (duration of motion constant). Subjects could scale tactile scanning speed, but surface structure was essential because the subjects were poor at scaling the speed of a moving smooth surface. For textured surfaces, subjective magnitude estimates increased linearly across the range of speeds tested. The spatial characteristics of the surfaces influenced speed perception, with the roughest surface (8 mm spatial period, SP) being perceived as moving 15% slower than the smoother, textured surfaces (2-3 mm SP). Neither dot disposition (periodic, non periodic) nor dot density contributed to the results, suggesting that the critical factor was dot spacing in the direction of the scan. A single monotonic relation between subjective speed and temporal frequency (speed/SP) was obtained when the ratings were normalized for SP. This provides clear predictions for identifying those cortical neurons that play a critical role in tactile motion perception and the underlying neuronal code. Finally, the results were consistent with observations in the visual system (decreased subjective speed with a decrease in spatial frequency, 1/SP), suggesting that stimulus motion is processed similarly in both sensory systems.

Central neural mechanisms contributing to the perception of tactile roughness.

This paper summarizes recent work showing that tactile roughness appreciation increases in a nearly linear fashion as tactile element spacing or spatial period (SP, distance centre-to-centre between raised dots in these experiments) is increased from 1.5 to 8.5 mm. Although a previous study had reported a U-shaped psychophysical function peaking at a nominal SP of 3.2 mm, differences in the surfaces (including changing SP in only one dimension as compared with two and higher dot heights that minimized contact with the smooth floor) likely contributed to the difference in the results. Roughness estimates were also unaffected by a 2-fold change in scanning speed (50 vs. 95 mm/s). Parallel recordings from neurones in primary somatosensory cortex (SI) during a texture discrimination task indicate that the discharge frequency of many SI cells shows a monotonic relation with SP (up to 5 mm tested). For some cells, the texture signals were ambiguous because discharge frequency co-varied with both texture and the scanning speed, as has also been reported for the peripheral mechanoreceptors that are activated by textured surfaces. Yet other SI cells showed a speed-invariant response to surface texture, consistent with perceptual constancy for roughness over a range of scanning speeds. We suggest that such a discharge pattern could be based on a simple intensive, or mean rate, code: an invariant central representation of surface texture could be obtained by subtracting a speed-varying signal from the ambiguous signals that co-vary with roughness and speed.

Instructed Delay Discharge in Primary and Secondary Somatosensory Cortex Within the Context of a Selective Attention Task

The neuronal mechanisms that contribute to tactile perception were studied using single-unit recordings from the cutaneous hand representation of primate primary (S1) and secondary (S2) somatosensory cortex. This study followed up on our recent observation that S1 and S2 neurons developed a sustained change in discharge during the instruction period of a directed-attention task. We determined the extent to which the symbolic light cues, which signaled the modality (tactile, visual) to attend and discriminate, elicited changes in discharge rate during the instructed delay (ID) period of the attention task and the functional importance of this discharge. ID responses, consisting of a sustained increase or decrease in discharge during the 2-s instruction period, were present in about 40% of the neurons in S1 and S2. ID responses in both cortical regions were very similar in most respects (frequency, sign, latency, amplitude), suggesting a common source. A major difference, however, was related to attentional modulation during the ID period: attentional influences were almost entirely restricted to S2 and these effects were always superimposed on the ID response (additive effect). These findings suggest that the underlying mechanisms for ID discharge and attention are independent. ID discharge significantly modified the initial response to the standard stimuli (competing texture and visual stimuli), usually enhancing responsiveness. We also showed that tactile detection in humans is enhanced during the ID period. Together, the results suggest that ID discharge represents a priming mechanism that prepares cortical areas to receive and process sensory inputs.

Neuronal correlates of tactile speed in primary somatosensory cortex

Moving stimuli activate all of the mechanoreceptive afferents involved in discriminative touch, but their signals covary with several parameters, including texture. Despite this, the brain extracts precise information about tactile speed, and humans can scale the tangential speed of moving surfaces as long as they have some surface texture. Speed estimates, however, vary with texture: lower estimates for rougher surfaces (increased spatial period, SP). We hypothesized that the discharge of cortical neurons playing a role in scaling tactile speed should covary with speed and SP in the same manner. Single-cell recordings (n = 119) were made in the hand region of primary somatosensory cortex (S1) of awake monkeys while raised-dot surfaces (longitudinal SPs, 2-8 mm; periodic or nonperiodic) were displaced under their fingertips at speeds of 40-105 mm/s. Speed sensitivity was widely distributed (area 3b, 13/25; area 1, 32/51; area 2, 31/43) and almost invariably combined with texture sensitivity (82% of cells). A subset of cells (27/64 fully tested speed-sensitive cells) showed a graded increase in discharge with increasing speed for testing with both sets of surfaces (periodic, nonperiodic), consistent with a role in tactile speed scaling. These cells were almost entirely confined to caudal S1 (areas 1 and 2). None of the speed-sensitive cells, however, showed a pattern of decreased discharge with increased SP, as found for subjective speed estimates in humans. Thus further processing of tactile motion signals, presumably in higher-order areas, is required to explain human tactile speed scaling.

Physical determinants of the shape of the psychophysical curve relating tactile roughness to raised-dot spacing: implications for neuronal coding of roughness

There are conflicting reports as to whether the shape of the psychometric relation between perceived roughness and tactile element spacing [spatial period (SP)] follows an inverted U-shape or a monotonic linear increase. This is a critical issue because the former result has been used to assess neuronal codes for roughness. We tested the hypothesis that the relations shape is critically dependent on tactile element height (raised dots). Subjects rated the roughness of low (0.36 mm)- and high (1.8 mm)-raised-dot surfaces displaced under their fingertip. Inverted U-shaped curves were obtained as the SP of low-dot surfaces was increased (1.3-6.2 mm, tetragonal arrays); a monotonic increase was observed for high-dot surfaces. We hypothesized that roughness is not a single sensory continuum across the tested SPs of low-dot surfaces, predicting that roughness discrimination would show deviations from the invariant relation between threshold (ΔS) and the value of the standard (S) surface (Weber fraction, ΔS/S) expected for a single continuum. The results showed that Weber fractions were increased for SPs on the descending limb of the inverted U-shaped curve. There was also an increase in the Weber fraction for high-dot surfaces but only at the peak (3 mm), corresponding to the SP at which the slope of the psychometric function showed a modest decline. Together the results indicate that tactile roughness is not a continuum across low-dot SPs of 1.3-6.2 mm. These findings suggest that correlating the inverted U-shaped function with neuronal codes is of questionable validity. A simple intensive code may well contribute to tactile roughness.

Tactile texture signals in primate primary somatosensory cortex and their relation to subjective roughness intensity

This study investigated the hypothesis that a simple intensive code, based on mean firing rate, could explain the cortical representation of subjective roughness intensity and its invariance with scanning speed. We examined the sensitivity of neurons in the cutaneous, finger representation of primary somatosensory cortex (S1) to a wide range of textures [1 mm high, raised-dot surfaces; spatial periods (SPs), 1.5-8.5 mm], scanned under the digit tips at different speeds (40-115 mm/s). Since subjective roughness estimates show a monotonic increase over this range and are independent of speed, we predicted that the mean firing rate of a subgroup of S1 neurons would share these properties. Single-unit recordings were made in four alert macaques (areas 3b, 1 and 2). Cells whose discharge rate showed a monotonic increase with SP, independent of speed, were particularly concentrated in area 3b. Area 2 was characterized by a high proportion of cells sensitive to speed, with or without texture sensitivity. Area 1 had intermediate properties. We suggest that area 3b and most likely area 1 play a key role in signaling roughness intensity, and that a mean rate code, signaled by both slowly and rapidly adapting neurons, is present at the level of area 3b. Finally, the substantial proportion of neurons that showed a monotonic change in discharge limited to a small range of SPs (often independent of response saturation) could play a role in discriminating smaller changes in SP.

Effects of transcranial direct current stimulation of primary somatosensory cortex on vibrotactile detection and discrimination

Anodal transcranial direct current stimulation (a-tDCS) of primary somatosensory cortex (S1) has been shown to enhance tactile spatial acuity, but there is little information as to the underlying neuronal mechanisms. We examined vibrotactile perception on the distal phalanx of the middle finger before, during, and after contralateral S1 tDCS [a-, cathodal (c)-, and sham (s)-tDCS]. The experiments tested our shift-gain hypothesis, which predicted that a-tDCS would decrease vibrotactile detection and discrimination thresholds (leftward shift of the stimulus-response function with increased gain/slope) relative to s-tDCS, whereas c-tDCS would have the opposite effects (relative to s-tDCS). The results showed that weak a-tDCS (1 mA, 20 min) led to a reduction in both vibrotactile detection and discrimination thresholds to 73-76% of baseline during the application of the stimulation in subjects categorized as responders. These effects persisted after the end of a-tDCS but were absent 30 min later. Most, but not all, subjects showed a decrease in threshold (8/12 for detection; 9/12 for discrimination). Intersubject variability was explained by a ceiling effect in the discrimination task. c-tDCS had no significant effect on either detection or discrimination threshold. Taken together, our results supported our shift-gain hypothesis for a-tDCS but not c-tDCS.