Search

This study compared the receptive field (RF) properties and firing rates of neurons in the cutaneous hand representation of primary somatosensory cortex (areas 3b, 1, and 2) of 9 awake, adult macaques that were intensively trained in a texture discrimination task using active touch (fingertips scanned over the surfaces using a single voluntary movement), passive touch (surfaces displaced under the immobile fingertips), or both active and passive touch. Two control monkeys received passive exposure to the same textures in the context of a visual discrimination task. Training and recording extended over 1–2 yr per animal. All neurons had a cutaneous receptive field (RF) that included the tips of the stimulated digits (D3 and/or D4). In area 3b, RFs were largest in monkeys trained with active touch, smallest in those trained with passive touch, and intermediate in those trained with both; i.e., the mode of touch differentially modified the cortical representation of the stimulated fingers. The same trends were seen in areas 1 and 2, but the changes were not significant, possibly because a second experience-driven influence was seen in areas 1 and 2, but not in area 3b: smaller RFs with passive exposure to irrelevant tactile inputs compared with recordings from one naive hemisphere. We suggest that added feedback during active touch and higher cortical firing rates were responsible for the larger RFs with behavioral training; this influence was tempered by periods of more restricted sensory feedback during passive touch training in the active + passive monkeys. NEW & NOTEWORTHY We studied experience-dependent sensory cortical plasticity in relation to tactile discrimination of texture using active and/or passive touch. We showed that neuronal receptive fields in primary somatosensory cortex, especially area 3b, are largest in monkeys trained with active touch, smallest in those trained with passive touch, and intermediate in those trained using both modes of touch. Prolonged, irrelevant tactile input had the opposite influence in areas 1 and 2, favoring smaller receptive fields.

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.

This study examined the extent to which haptic perception of two-dimensional (2-D) shape is modified by the design of the perceptual task (single-interval categorization vs. two-interval discrimination), the orientation of the angles in space (oblique vs. horizontal), and the exploration strategy (one or two passes over the angle). Subjects (n = 12) explored 2-D angles using the index finger of the outstretched arm. In the categorization task, subjects scanned individual angles, categorizing each as "large" or "small" (2 angles presented in each block of trials; range 80° vs. 100° to 89° vs. 91°; implicit standard 90°). In the discrimination task, a pair of angles was scanned (standard 90°; comparison 91-103°) and subjects identified the larger angle. The threshold for 2-D angle categorization was significantly lower than for 2-D angle discrimination, 4° versus 7.2°. Performance in the categorization task did not vary with either the orientation of the angles (horizontal vs. oblique, 3.9° vs. 4°) or the number of passes over the angle (1 vs. 2 passes, 3.9° vs. 4°). We suggest that the lower threshold with angle categorization likely reflects the reduced cognitive demands of this task. We found no evidence for a haptic oblique effect (higher threshold with oblique angles), likely reflecting the presence of an explicit external frame of reference formed by the intersection of the two bars forming the 2-D angles. Although one-interval haptic categorization is a more sensitive method for assessing 2-D haptic angle perception, perceptual invariances for exploratory strategy and angle orientation were, nevertheless, task-independent.

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.

The aim of this study was to define the relative contribution of self-generated cutaneous and proprioceptive feedback to haptic shape discrimination by systematically constraining the exploratory strategy. Subjects (n = 23) explored pairs of two-dimensional (2-D) angles (standard angle, 90 degrees; comparison angles, 91 degrees -103 degrees) placed at arm's length from the subject, and identified the larger angle of each pair. The exploratory strategies included a reference condition, dynamic scan of the index finger over the entire object [combined cutaneous and proprioceptive (shoulder) feedback], and modified conditions, static touch of the intersection of the two bars that formed the angle using the index finger (cutaneous feedback) and dynamic scans of the object using a hand-held tool (proprioceptive feedback, shoulder). Discrimination thresholds (75% correct) were very similar for dynamic and static touch with the index finger. Thresholds varied as a function of the static contact duration (1 s, 7.2 degrees +/- 0.6 degrees; approximately 3 s, 4.2 degrees +/- 0.5 degrees), but were not different from the reference condition (6.0 degrees +/- 0.9 degrees). The higher threshold with short static touch likely reflects movement-related gating of self-generated tactile inputs. Together, the results suggested that cutaneous feedback alone may be sufficient to explain 2-D angle discrimination, because the added proprioceptive feedback did not improve performance. Also, threshold did not vary with the number of dynamic scans (one or two), suggesting that the critical information was gathered on the first pass over the angle. In contrast, when the angles were explored with the tool, the threshold increased relative to the corresponding reference condition from the same session (tool, 9.6 degrees +/- 0.9 degrees; dynamic scan with the finger, 6.2 degrees +/- 1.0 degrees). Thus, performance was poorer with proprioceptive feedback alone, suggesting that cutaneous feedback was relatively more important for 2-D haptic angle discrimination in the present experiment.

In previous studies, we have shown that housing in enriched environment for about 3 months after weaning improved the topographic organization and decreased the size of the receptive fields (RFs) located on the glabrous skin surfaces in the forepaw maps of the primary somatosensory cortex (SI) in rats [Exp. Brain Res. 121 (1998) 191]. In contrast, housing in impoverished environment induced a degradation of the SI forepaw representation, characterized by topographic disruptions, a reduction of the cutaneous forepaw area and an enlargement of the glabrous RFs [Exp. Brain Res. 129 (1999) 518]. Based on these two studies, we postulated that these representational alterations could underlie changes in haptic perception. Therefore, the present study was aimed at determining the influence of housing conditions on the rat’s abilities in tactile texture discrimination. After a 2-month exposure to enriched or impoverished environments, rats were trained to perform a discrimination task during locomotion on floorboards of different roughness. At the end of every daily behavioral session, rats were replaced in their respective housing environment. Rats had to discriminate homogeneous (low roughness) from heterogeneous floorboards (combination of two different roughness levels). To determine the maximum performance in texture discrimination, the roughness contrast of the heterogeneous texture was gradually reduced, so that homogeneous and heterogeneous floorboards became harder to differentiate. We found that the enriched rats learned the first steps of the behavioral task faster than the impoverished rats, whereas both groups exhibited similar performances in texture discrimination. An individual “predilection” for either homogeneous or heterogeneous floorboards, presumably reflecting a behavioral strategy, seemed to account for the absence of differences in haptic discrimination between groups. The sensory experience depending on the rewarded texture discrimination task seems to have a greater influence on individual texture discrimination abilities than the sensorimotor experience related to housing conditions.

We combined behavioral assessment of texture discrimination and electrophysiological mapping of concomitant reorganization in the forepaw representation within the SI cortex. Rats were housed in enriched (EE) or impoverished (IE) environments which have been shown to remodel the forepaw map and possibly alter discriminative abilities. In addition, animals were trained to discriminate homogeneous floorboards of invariant roughness from heterogeneous floorboards of gradually decreasing roughness contrasts during locomotion. As reported recently, differences in perceptual abilities were not related to housing conditions, but to a predilection for a floorboard type [Bourgeon S, Xerri C, Coq JO. Abilities in tactile discrimination of textures in adult rats exposed to enriched or impoverished environments. Behav Brain Res 2004;153:217-231]. Consistently, the present study shows that cortical map remodeling resulting from short-duration daily experience can prevail over changes induced by housing conditions. The relative area of glabrous skin representation was related to the discrimination performance and learning abilities in the rats (H) with a predilection for heterogeneous floorboards, i.e. in the animals performing discrimination in the most challenging perceptual context. By contrast, this cortical area was influenced by the duration of sensory experience in rats (h) with a predilection for homogeneous floorboards. Both EE condition and training to discrimination selectively decreased the sizes of the SI neurons' receptive fields (RFs) located on glabrous skin. Smaller RFs and larger cortical areas serving glabrous skin were correlated with better perceptual performances and learning abilities in the H rats only. The present study shows that representational reorganization related to tactile discrimination performances depends upon the perceptual context.