Texture is encoded in precise temporal spiking patterns in primate somatosensory cortex

Abstract

Humans are exquisitely sensitive to the microstructure and material properties of surfaces. In the peripheral nerves, texture information is conveyed via two mechanisms: coarse textural features are encoded in spatial patterns of activation that reflect their spatial layout, and fine features are encoded in highly repeatable, texture-specific temporal spiking patterns evoked as the skin moves across the surface. Here, we examined whether this temporal code is preserved in the responses of neurons in somatosensory cortex. We scanned a diverse set of everyday textures across the fingertip of awake macaques while recording the responses evoked in individual cortical neurons. We found that temporal spiking patterns are highly repeatable across multiple presentations of the same texture, with millisecond precision. As a result, texture identity can be reliably decoded from the temporal patterns themselves, even after information carried in the spike rates is eliminated. However, the combination of rate and timing is more informative than either code in isolation. The temporal precision of the texture response is heterogenous across cortical neurons and depends on the submodality composition of their input and on their location along the somatosensory neuraxis. Furthermore, temporal spiking patterns in cortex dilate and contract with decreases and increases in scanning speed, respectively, and this systematic relationship between speed and patterning may contribute to the observed perceptual invariance to speed. Finally, we find that the quality of a texture percept can be better predicted when these temporal patterns are taken into consideration. We conclude that high-precision spike timing complements rate-based signals to encode texture in somatosensory cortex.