Spatial and temporal codes mediate the tactile perception of natural textures

Top Cited Papers
Publisher Website
Google Scholar
Abstract
When we run our fingers over the surface of an object, we acquire information about its microgeometry and material properties. Texture information is widely believed to be conveyed in spatial patterns of activation evoked across one of three populations of cutaneous mechanoreceptive afferents that innervate the fingertips. Here, we record the responses evoked in individual cutaneous afferents in Rhesus macaques as we scan a diverse set of natural textures across their fingertips using a custom-made rotating drum stimulator. We show that a spatial mechanism can only account for the processing of coarse textures. Information about most natural textures, however, is conveyed through precise temporal spiking patterns in afferent responses, driven by high-frequency skin vibrations elicited during scanning. Furthermore, these texture-specific spiking patterns predictably dilate or contract in time with changes in scanning speed; the systematic effect of speed on neuronal activity suggests that it can be reversed to achieve perceptual constancy across speeds. The proposed temporal coding mechanism involves converting the fine spatial structure of the surface into a temporal spiking pattern, shaped in part by the mechanical properties of the skin, and ascribes an additional function to vibration-sensitive mechanoreceptive afferents. This temporal mechanism complements the spatial one and greatly extends the range of tangible textures. We show that a combination of spatial and temporal mechanisms, mediated by all three populations of afferents, accounts for perceptual judgments of texture. Significance Our exquisite tactile sensitivity to surface texture allows us to distinguish silk from satin or even good silk from cheap silk. We show that the tactile perception of natural textures relies on two neural mechanisms. Coarse textural features, for example, the individual elements of Braille, are represented in spatial patterns of activation across one population of mechanoreceptive afferents that densely innervate the fingertip skin. In contrast, our ability to discern fine textural features is mediated by the transduction and processing of vibrations produced in the skin during scanning. Indeed, two other populations of vibration-sensitive afferents produce temporally patterned responses to these vibrations, and spiking patterns in these afferent populations convey texture information and shape the way textures are perceived.