Speed invariance of tactile texture perception

Abstract

The nervous system achieves stable perceptual representations of objects despite large variations in the activity patterns of sensory receptors. Here, we explore perceptual constancy in the sense of touch. Specifically, we investigate the invariance of tactile texture perception across changes in scanning speed. Texture signals in the nerve have been shown to be highly dependent on speed: temporal spiking patterns in nerve fibers that encode fine textural features contract or dilate systematically with increases or decreases in scanning speed, respectively, resulting in concomitant changes in response rate. Nevertheless, texture perception has been shown, albeit with restricted stimulus sets and limited perceptual assays, to be independent of scanning speed. Indeed, previous studies investigated the effect of scanning speed on perceived roughness, only one aspect of texture, often with impoverished stimuli, namely gratings and embossed dot patterns. To fill this gap, we probe the perceptual constancy of a wide range of textures using two different paradigms: one that probes texture perception along well-established sensory dimensions independently and one that probes texture perception as a whole. We find that texture perception is highly stable across scanning speeds, irrespective of the texture or the perceptual assay. Any speed-related effects are dwarfed by differences in percepts evoked by different textures. This remarkable speed invariance of texture perception stands in stark contrast to the strong dependence of the texture responses of nerve fibers on scanning speed. Our results imply neural mechanisms that compensate for scanning speed to achieve stable representations of surface texture. Our brain forms stable representations of objects regardless of viewpoint, a phenomenon known as invariance that has been described in several sensory modalities. Here, we explore invariance in the sense of touch and show that the tactile perception of texture does not depend on scanning speed. This perceptual constancy implies neural mechanisms that extract information about texture from the response of nerve fibers such that the resulting neural representation is stable across speeds.

Neural Basis of Touch and Proprioception in Primate Cortex

“…This ambiguity between speed and texture is also reflected in psychophysical judgments of speed, which are also influenced by texture (77). Interestingly, judgments of texture are largely independent of speed (24, 220, 242). …”

Emergence of an invariant representation of texture in primate somatosensory cortex

“…Indeed, psychophysical ratings along the three principal perceptual axes of textures -roughness, hardness, and stickiness -are identical across speeds (Boundy-Singer et al, 2017;Lederman, 1974;Meftah el-M et al, 2000). Furthermore, the perceived dissimilarity of a pair of textures -which probes texture perception across all of its dimensions and attributes -is very similar whether the two textures are scanned at the same speed or at different speeds (Boundy-Singer et al, 2017). What makes this tolerance so remarkable is that the response of tactile nerve fibers are highly speed dependent.…”

“…Next, we examined the extent to which neuronal responses could account for the well-documented speed-tolerance of texture perception (Boundy-Singer et al, 2017;Lederman, 1974;Meftah el-M et al, 2000). To this end, we tested the hypothesis that perceived roughness is determined by the population firing rate in somatosensory cortex (Burton and Sinclair, 1994;Lieber and Bensmaia, 2019) using a previously published set of roughness ratings from human subjects.…”

“…In touch, the best known instance of perceptual tolerance is for texture: tactile texture perception has been shown to be nearly independent of the force exerted on the surface (Lederman, 1981;Lederman and Taylor, 1972) or the speed at which it is scanned across the skin (Boundy-Singer et al, 2017;Lederman, 1974;Meftah el-M et al, 2000). Remarkably, this perceptual tolerance is achieved despite responses in the somatosensory nerves that are strongly modulated by exploratory parameters such as scanning speed (DiCarlo and Johnson, 1999;Goodwin and Morley, 1987a;Phillips et al, 1992) and, to a lesser degree, force (Goodwin and Morley, 1987b;Phillips et al, 1992;Saal et al, 2017).…”

Human first-order tactile neurons can resolve spatial details on the scale of single fingerprint ridges

“…Unlike with tactile stimuli based on stationary skin indentations, frictional forces can be expected to disrupt neurons' subfield layout by causing complex direction-dependent shear deformations of the skin within their receptive fields (Johansson and Flanagan, 2009;Delhaye et al, 2016). The receptive field of FA-1 and SA-1 neurons were scanned by a flat surface with small raised dots at speeds representing natural use of our hands in tactile pattern discrimination tasks (15, 30, and 60 mm/s) (Lederman, 1974;Vega-Bermudez et al, 1991;Boundy-Singer et al, 2017;Olczak et al, 2018). We quantified the spatial resolution of the receptive fields' subfield arrangement and examined how robustly a neuron's subfield layout spatially structures its response in the space domain across repeated scans and across scanning speeds.…”