Millisecond Precision Spike Timing Shapes Tactile Perception

In primates, the sense of touch has traditionally been considered to be a spatial modality, drawing an analogy to the visual system. In this view, stimuli are encoded in spatial patterns of activity over the sheet of receptors embedded in the skin. We propose that the spatial processing mode is complemented by a temporal one. Indeed, the transduction and processing of complex, high-frequency skin vibrations have been shown to play an important role in tactile texture perception, and the frequency composition of vibrations shapes the evoked percept. Mechanoreceptive afferents innervating the glabrous skin exhibit temporal patterning in their responses, but the importance and behavioral relevance of spike timing, particularly for naturalistic stimuli, remains to be elucidated. Based on neurophysiological recordings from Rhesus macaques, we show that spike timing conveys information about the frequency composition of skin vibrations, both for individual afferents and for afferent populations, and that the temporal fidelity varies across afferent class. Furthermore, the perception of skin vibrations, measured in human subjects, is better predicted when spike timing is taken into account, and the resolution that predicts perception best matches the optimal resolution of the respective afferent classes. In light of these results, the peripheral representation of complex skin vibrations draws a powerful analogy with the auditory and vibrissal systems.