Touch Spanning Spatial Scales: Texture Coding along the Somatosensory Neuraxis

We are exquisitely sensitive to textures: our sense of touch provides us with a sensitivity that spans six orders in magnitude in spatial scale, from tens of nanometers to tens of millimeters. Here, we characterize neural representations of texture across the somatosensory neuraxis, from responses in the peripheral nerve and early stages of cortical processing, up through higher-order areas of cortex whose responses to natural texture have never before been evaluated. We monitor single-unit activity of peripheral afferents and cortical neurons in the macaque, and we relate these neural patterns of activity to perceptual features of texture evaluated by human subjects. This allows us to assess how the neural coding of texture is maintained and transformed across multiple stages of processing, as well as how it gives rise to our perceptual experience of texture.The first major focus of this work was to evaluate the role of precise temporal patterning of texture responses in somatosensory cortex. We find that finely timed patterns of activity, on the order of just a few milliseconds, are highly informative about texture. Individual cells vary in their temporal precision, and this heterogeneity can be explained, at least in part, by the inputs a cell receives: those cells that receive temporally precise inputs (from Pacinian-corpuscle associated peripheral afferents) are, themselves, temporally precise. Finally, while identifying a role for precise timing in perception had been elusive, we find that a combination of rate and timing is best for predicting the perceptual features of texture. The second focus of this work was to characterize natural texture representations in higher-order somatosensory cortex, including secondary somatosensory cortex (S2) and the parietal ventral area (PV). We find that cells in S2/PV convey information about texture, but this representation is sparser, higher-dimensional, and less driven by a shared response to low-level features. Furthermore, we find a portion of cells that are modulated by the behavioral task. Some cells are sensitive to trial type (same vs different), and other cells' activity correlates with the animal's decision, regardless of the actual trial type. Altogether, these findings provide for a more holistic view of texture coding and how it evolves across various stages of cortical processing in the somatosensory neuraxis.