Feeling fooled: Texture contaminates the neural code for tactile speed

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.

Abstract

Our ability to sense the speed at which a surface moves across our skin is highly unreliable and depends on the texture of the surface. This study shows that speed illusions can be predicted from the responses of a specific population of nerve fibers and of their downstream targets; because the skin is too sparsely innervated to compute tactile speed accurately, the nervous system relies on a heuristic to estimate it.