Feeling fooled: Texture contaminates the neural code for tactile speed.

Benoit P Delhaye,Kristine R Mclellan,Molly K O'Donnell,Sliman J Bensmaia,Justin D Lieber,Adam Kohn

doi:10.1371/journal.pbio.3000431

Benoit P Delhaye, Kristine R Mclellan + Show 4 more

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https://doi.org/10.1371/journal.pbio.3000431

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Abstract

Motion is an essential component of everyday tactile experience: most manual interactions involve relative movement between the skin and objects. Much of the research on the neural basis of tactile motion perception has focused on how direction is encoded, but less is known about how speed is. Perceived speed has been shown to be dependent on surface texture, but previous studies used only coarse textures, which span a restricted range of tangible spatial scales and provide a limited window into tactile coding. To fill this gap, we measured the ability of human observers to report the speed of natural textures—which span the range of tactile experience and engage all the known mechanisms of texture coding—scanned across the skin. In parallel experiments, we recorded the responses of single units in the nerve and in the somatosensory cortex of primates to the same textures scanned at different speeds. We found that the perception of speed is heavily influenced by texture: some textures are systematically perceived as moving faster than are others, and some textures provide a more informative signal about speed than do others. Similarly, the responses of neurons in the nerve and in cortex are strongly dependent on texture. In the nerve, although all fibers exhibit speed-dependent responses, the responses of Pacinian corpuscle–associated (PC) fibers are most strongly modulated by speed and can best account for human judgments. In cortex, approximately half of the neurons exhibit speed-dependent responses, and this subpopulation receives strong input from PC fibers. However, speed judgments seem to reflect an integration of speed-dependent and speed-independent responses such that the latter help to partially compensate for the strong texture dependence of the former.

Highlights

When we manipulate objects, we acquire information about their properties—their shape and texture, e.g.—through the sense of touch
To elucidate the neural mechanisms of tactile speed processing, we obtained from blindfolded human subjects perceptual judgments of speed as a variety of textured surfaces were scanned across their stationary fingertips using a circular drum
Feeling fooled: Texture contaminates the neural code for tactile speed assessed how speed affected the neuronal responses in the nerve and in the brain, the degree to which speed-related responses could be disentangled from texture-related ones, and the extent to which neuronal responses could account for perceptual judgments of speed

Summary

Introduction

We acquire information about their properties—their shape and texture, e.g.—through the sense of touch. Most interactions involve movement between skin and object, and tactile signals tend to be enhanced by movement, leading, for example, to increased sensitivity to surface texture [1,2,3] and to local object contours [4]. Aware of the motion-induced sensitization of touch, as evidenced by the fact that we spontaneously deploy exploratory procedures that involve motion to acquire object-specific information [5]. Touch conveys information about the motion itself, as evidenced by the fact that (blindfolded) subjects can distinguish the direction [6,7,8] and speed at which objects move across the skin [9,10]. The firing rate of nerve fibers tends to increase as stimuli move faster across the skin [12,13,14], but surface texture modulates afferent firing rates. How speed- and texture-dependent components are disentangled remains to be elucidated

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