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.

The skin is our largest sensory organ and innervated by afferent fibers carrying tactile information to the spinal cord and onto the brain. The density with which different classes of tactile afferents innervate the skin is not constant but varies considerably across different body regions. However, precise estimates of innervation density are only available for some body parts, such as the hands, and estimates of the total number of tactile afferent fibers are inconsistent and incomplete. Here we reconcile different estimates and provide plausible ranges and best estimates for the number of different tactile fiber types innervating different regions of the skin, using evidence from dorsal root fiber counts, microneurography, histology, and psychophysics. We estimate that the skin across the whole body of young adults is innervated by ∼230,000 tactile afferent fibers (plausible range: 200,000–270,000), with a subsequent decrement of 5–8% every decade due to aging. Fifteen percent of fibers innervate the palmar skin of both hands and 19% the region surrounding the face and lips. Slowly and fast-adapting fibers are split roughly evenly, but this breakdown varies with skin region. Innervation density correlates well with psychophysical spatial acuity across different body regions, and, additionally, on hairy skin, with hair follicle density. Innervation density is also weakly correlated with the size of the cortical somatotopic representation but cannot fully account for the magnification of the hands and the face.

Significance: When we grasp an object, thousands of tactile nerve fibers become activated and inform us about its physical properties (e.g., shape, size, and texture). Although the properties of individual fibers have been described, our understanding of how object information is encoded in populations of fibers remains primitive. To fill this gap, we have developed a simulation of tactile fibers that incorporates much of what is known about skin mechanics and tactile nerve fibers. We show that simulated fibers match biological ones across a wide range of conditions sampled from the literature. We then show how this simulation can reveal previously unknown ways in which populations of nerve fibers cooperate to convey sensory information and discuss the implications for bionic hands.

Electrical connections between nerves and a prosthetic device enable amputees to discern precise, graded sensory intensity ranging from light touch to intense pressure.

Sensory systems are designed to extract behaviorally relevant information from the environment. In seeking to understand a sensory system, it is important to understand the environment within which it operates. In the present study, we seek to characterize the natural scenes of tactile texture perception. During tactile exploration complex high-frequency vibrations are elicited in the fingertip skin, and these vibrations are thought to carry information about the surface texture of manipulated objects. How these texture-elicited vibrations depend on surface microgeometry and on the biomechanical properties of the fingertip skin itself remains to be elucidated. Here we record skin vibrations, using a laser-Doppler vibrometer, as various textured surfaces are scanned across the finger. We find that the frequency composition of elicited vibrations is texture specific and highly repeatable. In fact, textures can be classified with high accuracy on the basis of the vibrations they elicit in the skin. As might be expected, some aspects of surface microgeometry are directly reflected in the skin vibrations. However, texture vibrations are also determined in part by fingerprint geometry. This mechanism enhances textural features that are too small to be resolved spatially, given the limited spatial resolution of the neural signal. We conclude that it is impossible to understand the neural basis of texture perception without first characterizing the skin vibrations that drive neural responses, given the complex dependence of skin vibrations on both surface microgeometry and fingertip biomechanics.