The neural code for tactile roughness in the somatosensory nerves

Abstract

Roughness is the most salient perceptual dimension of surface texture but has no well-defined physical basis. We seek to determine the neural determinants of tactile roughness in the somatosensory nerves. Specifically, we record the patterns of activation evoked in tactile nerve fibers of anesthetized Rhesus macaques to a large and diverse set of natural textures and assess what aspect of these patterns of activation can account for psychophysical judgments of roughness, obtained from human observers. We show that perceived roughness is determined by the variation in the population response, weighted by fiber type. That is, a surface will feel rough to the extent that the activity varies across nerve fibers and varies across time within nerve fibers. We show that this variation-based neural code can account not only for magnitude estimates of roughness but also for roughness discrimination performance. Our sense of touch endows us with an exquisite sensitivity to the microstructure of surfaces, the most salient aspect of which is roughness. We analyze the responses evoked in tactile fibers of monkeys by natural textures and compare them to judgments of roughness obtained for the same textures from human observers. We then describe how texture signals from three populations of nerve fibers are integrated to culminate in a percept of roughness.

Emergence of an invariant representation of texture in primate somatosensory cortex

“…Human and macaque hands show very similar patterns of cutaneous innervation (Darian-Smith and Kenins, 1980;Johansson and Vallbo, 1979;Paré et al, 2003) and the tactile nerve fibers in the two species exhibit nearly identical response properties (Johansson et al, 1982;Phillips et al, 1992). Human texture perception can be successfully predicted by the responses of macaque nerve fibers (Blake et al, 1997;Connor and Johnson, 1992;Connor et al, 1990;Lieber et al, 2017;Weber et al, 2013) and cortical neurons (Bourgeon et al, 2016;Lieber and Bensmaia, 2019).…”

“…The methods for recording afferent responses to textured stimuli have been previously described in detail (Lieber et al, 2017;Weber et al, 2013). In brief, we recorded the responses of tactile fibers to 55 textured surfaces scanned over the fingertip, including everyday textures such as fabrics, sandpapers, as well as plastic gratings and embossed dots.…”

High-Dimensional Representation of Texture in the Somatosensory Cortex of Primates

“…At the periphery, texture-specific surface features are encoded through multiple mechanisms. Coarse surface features -measured in millimeters -are primarily encoded in the spatial pattern of activation across of SA1 fibers (Connor and Johnson, 1992) (and perhaps RA fibers as well (Lieber et al, 2017)). In contrast, fine surface features -typically measured in the tens or hundreds of microns -drive characteristic vibrations in the skin during texture scanning (Manfredi et al, 2014).…”

“…However, many tangible surface features are too small and too close together to be encoded spatially because the spatial code is limited by the innervation density of the skin (Darian-Smith and Kenins, 1980;Johansson and Vallbo, 1979). To perceive fine textural features requires movement between skin and surface, which leads to the elicitation of texture-specific skin vibrations, which in turn evoke precisely timed texture-specific spiking patterns in RA and Pacinian corpuscle-associated (PC) afferents (Bensmaïa and Hollins, 2005;Hollins and Risner, 2000;Hollins et al, 2001Hollins et al, , 2002Lieber et al, 2017;Weber et al, 2013). These spatial and temporal representations must be combined and synthesized to achieve a unified percept of texture, a process about which little is known.…”

“…While neurons in somatosensory cortex have been shown to encode information about texture, previous studies investigating cortical texture representations used surfaces with elements in the range of millimeters, such as Braille-like dot patterns (DiCarlo and Johnson, 2000;DiCarlo et al, 1998) and gratings (Darian-Smith et al, 1982;Sinclair and Burton, 1991;Tremblay et al, 1996), which span only a small fraction of the wide range of tangible textures. We have previously shown that responses to such textures -which only engage the spatial mechanism -provide an incomplete view of the neural mechanisms that mediate the perception of texture (Lieber et al, 2017;Weber et al, 2013).…”