C. Elaine Chapman

Haptic discrimination of object shape in humans : contribution of cutaneous and proprioceptive inputs

Using two-dimensional (2D) angles composed of two straight, 8-cm-long arms that formed an angle, we investigated the importance of cutaneous feedback from the exploring index finger, and proprioceptive feedback from the shoulder (scanning movements made with the outstretched arm), to the human ability to discriminate small differences in the angles. Using a two-alternative forced-choice paradigm, subjects identified the larger angle in each pair explored (standard angle, 90°; comparison angles, 91° to 103°). Subjects were tested under four experimental conditions: (1) active touch (reference condition); (2) active touch with digital anaesthesia; (3) passive touch (a computer-controlled device displaced the angle under the subject’s immobile digit); and (4) passive touch with digital anaesthesia. When only proprioceptive feedback from the shoulder was available (condition 2), there was a significant increase in discrimination threshold, from 4.0° in the reference condition (condition 1) to 7.2°, indicating that cutaneous feedback from the exploring digit contributed to task performance. When only cutaneous feedback from the finger was available (condition 3), there was also a significant increase in threshold from 4.2° in the active condition to 8.7°. This suggested that proprioceptive feedback from the shoulder, potentially from a variety of deep (muscle and joint) but also cutaneous receptors, contributed to the ability to discriminate small changes in 2D angles. When both sources of feedback were eliminated (condition 4), subjects were unable to discriminate even the largest difference presented (13°). The results suggest that this sensory task is truly an integrative task drawing on sensory information from two different submodalities and so, following the definition of Gibson, is haptic in nature. The results are discussed in relation to the potential neural mechanisms that might underlie a task that requires integration across two anatomically separate body parts and two distinct modalities.

Tactile acuity in the blind: A closer look reveals superiority over the sighted in some but not all cutaneous tasks

Previous studies have shown that blind subjects may outperform the sighted on certain tactile discrimination tasks. We recently showed that blind subjects outperformed the sighted in a haptic 2D-angle discrimination task. The purpose of this study was to compare the performance of the same blind (n=16) and sighted (n=17, G1) subjects in three tactile discrimination tasks dependent solely on cutaneous inputs from the fingertip of the index finger, D2. A second group of sighted subjects (n=30, G2) were also tested. Texture discrimination thresholds were 0.62 (G1)-0.80 mm (G2) for the sighted subjects, and 0.64 mm for the blind (standard, 2mm spatial period). Grating orientation thresholds were 0.99 (G1)-1.12 mm (G2) for the sighted subjects, and 0.96 mm for the blind. Finally, vibrotactile frequency discrimination thresholds (100 Hz standard) were 19.5 (G2) and 20.0 Hz (G1) for the sighted, and 16.5 Hz for the blind subjects. There were no significant differences in performance between the blind and the sighted subjects for the grating orientation or vibrotactile frequency discrimination tasks. In contrast, blind subjects outperformed the sighted for the texture discrimination task (G2 only), possibly reflecting the fact that the raised dot surfaces were similar to the dots forming Braille characters (all were fluent Braille readers).

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.

Haptic discrimination of object shape in humans: two-dimensional angle discrimination.

The human ability to recognize objects on the basis of their shape, as defined by active exploratory movements, is dependent on sensory feedback from mechanoreceptors located both in the skin and in deep structures (haptic feedback). Surprisingly, we have little information about the mechanisms for integrating these different signals into a single sensory percept. With the eventual aim of studying the underlying central neural mechanisms, we developed a shape discrimination test that required active exploration of objects, but was restricted to one component of shape, two-dimensional (2D) angles. The angles were machined from 1-cm-thick Plexiglas, and consisted of two 8-cm-long arms that met to form an angle of 90° (standard) or 91° to 103° (comparison angles). Subjects scanned pairs of angles with the index finger of the outstretched arm and identified the larger angle of each pair explored. Discrimination threshold (75% correct) was 4.7° (range 0.7° to 12.1°), giving a precision of 5.2% (0.8–13.4%: difference/standard). Repeated blocks of trials, either in the same session or on different days, had no effect on discrimination threshold. In contrast, the motor strategy was partly modified: scanning speed increased but dwell-time at the intersection did not change. Finally, 2D angle discrimination was not significantly modified by rotating the orientation of one of the angles in the pair (0°, 4° or 8° rotation towards the midline, in the vertical plane), providing evidence that subjects evaluated each angle independently in each trial. Subject reports indicated that they relied on cutaneous feedback from the exploring digit (amount of compression of the finger at the angle) and mental images of the angles, most likely arising from proprioceptive information (from the shoulder) generated during the to-and-fro scans over the angle. In terms of shoulder angles, the mean discrimination threshold here was 0.54° (range 0.08° to 1.36°). These values are lower than previous estimates of position sense at the shoulder. In light of the subjects’ strategies, it therefore seems likely that both cutaneous and proprioceptive (including both dynamic and static position-related signals) feedback contributed to the haptic discrimination of 2D angles.

Perception of simulated local shapes using active and passive touch

This study reexamined the perceptual equivalence of active and passive touch using a computer-controlled force-feedback device. Nine subjects explored a 6 x 10-cm workspace, with the index finger resting on a mobile flat plate, and experienced simulated Gaussian ridges and troughs (width, 15 mm; amplitude, 0.5 to 4.5 mm). The device simulated shapes by modulating either lateral resistance with no vertical movement or by vertical movement with no lateral forces, as a function of the digit position in the horizontal workspace. The force profiles and displacements recorded during active touch were played back to the stationary finger in the passive condition, ensuring that stimulation conditions were identical. For the passive condition, shapes simulated by vertical displacements of the finger had lower categorization thresholds and higher magnitude estimates compared with those of active touch. In contrast, the results with the lateral force fields showed that with passive touch, subjects recognized that a stimulus was present but were unable to correctly categorize its shape as convex or concave. This result suggests that feedback from the motor command can play an important role in processing sensory inputs during tactile exploration. Finally, subjects were administered a ring-block anesthesia of the digital nerves of the index finger and subsequently retested. Removing skin sensation significantly increased the categorization threshold for the perception of shapes generated by lateral force fields, but not for those generated by displacement fields.

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.

Role of Primary Somatosensory Cortex in Active and Passive Touch

Publisher Summary The sensory and motor capabilities of the hand in humans and other nonhuman primates are highly developed and together confer a special evolutionary advantage to primates. When the hand is used as a sensory organ, specifically for discriminative touch and stereognosis, then the movements become subsidiary to the goal of obtaining somesthetic feedback. It is argued that the functional role of primary somatosensory (S1) cortex can be fully appreciated only when studied in relation to the various behavioral factors that modify the access of sensory information to the central processing centers, including movement, attention, motivation, motor set, and arousal. Movement is used as an example of one such behavioral factor. The importance of movement to touch is underlined by the observation that tactile perception is better when there is movement between the stimulus and the skin, as compared to when the same stimulus is applied statically. The existence of movement-related gating controls over behaviorally relevant cutaneous inputs to S1 cortex may appear to be paradoxical and difficult to reconcile with the highly refined tactile abilities associated with active touch.

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.

Factors influencing the perception of tactile stimuli during movement

This chapter provides an overview of the factors that influence the perception of cutaneous stimuli during the course of movement. The inhibitory influences responsible for movement-related reductions in the ability to detect near-threshold stimli and to appreciate the intensity of suprathreshold stimuli are characterized as showing a spatial gradient and sensitivity to the movement kinematics and kinetics. Different models of the signals responsible for the gating effects are considered. The closest approximation to the experimental data was obtained with a model including a nonlinear inhibitory surround. Two other models, masking and a linearly augmenting inhibitory surround, failed to produce results consistent with all experimental observations.

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.