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

Abstract

Bourgeon S, Dépeault A, Meftah EM, Chapman CE. Tactile texture signals in primate primary somatosensory cortex and their relation to subjective roughness intensity. J Neurophysiol 115: 1767-1785, 2016. First published February 10, 2016 doi:10.1152/jn.00303.2015.-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. tactile roughness; neuronal coding; passive touch; hierarchical processing WHEN WE TOUCH A SURFACE, THE tactile impression of smoothness/roughness is influenced by the physical structure of the surface. A number of factors contribute, including the number of projections (or tactile elements) that make up the surface, their spacing, density, size, form, degree of unevenness and the material from which they are constructed. Any tactile exploration of a surface necessarily activates all of the largediameter cutaneous mechanoreceptive afferents that are involved in discriminative touch, including (in the monkey) slowly adapting type I (SA), rapidly adapting (RA) and Pacinian (PC) afferents. The discharge evoked by textured surfaces is complex, reflecting not only the surface structure, but also factors intrinsic to the exploration process, including scanning speed and contact force.Although the nature of the relationship between subjective roughness and texture remains controversial, the bulk of the evidence suggests that, if the tactile elements are sufficiently high (Ն1 mm), then there is a linear relation between subjective roughness and tactile element spacing [spatial period (SP), distance center-to-center between adjacent elements] for sur-

Neural Basis of Touch and Proprioception in Primate Cortex

“…With this caveat, the responses of APC neurons to gratings and dot patterns have been shown to be modulated by the spatial period of the stimuli. However, a subset of these neurons seems to track the perceived roughness of such textures (25, 53), consistent with the hypothesis that they are causally implicated in texture perception. Furthermore, lesions of area 1 result in pronounced deficits in texture dis- crimination (296, 333, 334), so this area may be part of a pathway specialized for texture processing.…”

Emergence of an invariant representation of texture in primate somatosensory cortex

“…While we did observe significant differences in speed-sensitivity across different afferent classes (Delhaye et al, 2019), every submodality trended towards more speed-sensitivity than that was observed in cortex (RA: 29.3%±3.3% and PC: 35.0%±5.4%, p < 0.05, SA1: 23.8%±6.2%, p=0.18, see Supplementary Figure 2A -B). The speed-sensitivity of responses in area 3b trended towards smaller values than responses from areas 1 and 2 (area 3b: 12.9%±9.8% < area 1: 23.1%±7.5% at p<0.05 and area 2: 24.4%±24.9%, p=0.33, see Supplementary Figure 2A-B), consistent with previous reports (Bourgeon et al, 2016;Dépeault et al, 2013). Figure 1.…”

“…As signals ascend the somatosensory hierarchy, the tuning of individual neurons becomes increasingly heterogeneous . We might thus expect subpopulations of cortical neurons to show specialization for speed or texture coding (Bourgeon et al, 2016;Dépeault et al, 2013). Indeed, we found a significant proportion of cortical cells exhibited speed ratios weaker than any observed in peripheral afferents ( Figure 1E) (12/49 with ratio < 0.12, p<0.05, permutation test, see Methods), an effect that was present in all three cortical areas (Supplementary Figure 2D).…”

“…It thus stands to reason that these same mechanisms could extract a speed-tolerant representation of texture that was not present in the peripheral response. Indeed, previous work suggests that a subpopulation of neurons in somatosensory cortex may exhibit speed-tolerant responses to texture (Bourgeon et al, 2016;Dépeault et al, 2013;DiCarlo and Johnson, 1999;Sinclair and Burton, 1991). However, these studies only characterized cortical responses to parametrically defined dot patterns and gratings that span a narrow range of tangible textures (Weber et al, 2013).…”

Brain networks underlying conscious tactile perception of textures as revealed using the velvet hand illusion

“…However, it remains unknown whether this area is also critical for the conscious tactile perception of object properties such as textures. Previous electrophysiological studies involving monkeys have demonstrated that neurons in S1 are involved in the perception of texture (Bourgeon, Depeault, Meftah el, & Chapman, 2016;Chapman, Tremblay, Jiang, Belingard, & Meftah el, 2002;Sinclair & Burton, 1991) and vibrational frequency (Romo, Lemus, & de Lafuente, 2012). However, such studies have been unable to clarify the extent to which such activity is associated with conscious texture perception.…”