When we grasp and manipulate an object, populations of tactile nerve fibers become activated and convey information about the shape, size, and texture of the object and its motion across the skin. The response properties of tactile fibers have been extensively characterized in single-unit recordings, yielding important insights into how individual fibers encode tactile information. A recurring finding in this extensive body of work is that stimulus information is distributed over many fibers. However, our understanding of population-level representations remains primitive. To fill this gap, we have developed a model to simulate the responses of all tactile fibers innervating the glabrous skin of the hand to any spatiotemporal stimulus applied to the skin. The model first reconstructs the stresses experienced by mechanoreceptors when the skin is deformed and then simulates the spiking response that would be produced in the nerve fiber innervating that receptor. By simulating skin deformations across the palmar surface of the hand and tiling it with receptors at their known densities, we reconstruct the responses of entire populations of nerve fibers. We show that the simulated responses closely match their measured counterparts, down to the precise timing of the evoked spikes, across a wide variety of experimental conditions sampled from the literature. We then conduct three virtual experiments to illustrate how the simulation can provide powerful insights into population coding in touch. Finally, we discuss how the model provides a means to establish naturalistic artificial touch in bionic hands.mechanoreceptor | tactile afferent | somatosensory periphery | skin mechanics | computational model T he human hand is endowed with thousands of mechanoreceptors of different types distributed across the skin, each innervated by one or more large myelinated nerve fibers (1). These fibers convey detailed information about contact events and provide us with an exquisite sensitivity to the form and surface properties of grasped objects (2, 3). During object manipulation and tactile exploration, the glabrous skin of the hand undergoes complex spatiotemporal mechanical deformations, which in turn, drive very precise spiking responses in individual afferents. Coarse object features, such as edges and corners, are reflected in spatial patterns of activation in slowly adapting type I (SA1) and rapidly adapting (RA) fibers, which are densely packed in the fingertip (3, 4). At the same time, interactions with objects and surfaces elicit high-frequency, low-amplitude surface waves that propagate across the skin of the finger and palm and excite vibration-sensitive Pacinian (PC) afferents all over the hand (5-8).Recording the activity of tactile nerve fibers in monkeys or humans is technically difficult, is slow, and generally yields responses from a single unit at a time (9, 10). Although such recordings have yielded powerful insights into the neural basis of touch, they provide a limited window into the information that the hand c...
Electrical stimulation of sensory nerves is a powerful tool for studying neural coding because it can activate neural populations in ways that natural stimulation cannot. Electrical stimulation of the nerve has also been used to restore sensation to patients who have suffered the loss of a limb. We have used long-term implanted electrical interfaces to elucidate the neural basis of perceived intensity in the sense of touch. To this end, we assessed the sensory correlates of neural firing rate and neuronal population recruitment independently by varying two parameters of nerve stimulation: pulse frequency and pulse width. Specifically, two amputees, chronically implanted with peripheral nerve electrodes, performed each of three psychophysical tasks—intensity discrimination, magnitude scaling, and intensity matching—in response to electrical stimulation of their somatosensory nerves. We found that stimulation pulse width and pulse frequency had systematic, cooperative effects on perceived tactile intensity and that the artificial tactile sensations could be reliably matched to skin indentations on the intact limb. We identified a quantity we termed the activation charge rate (ACR), derived from stimulation parameters, that predicted the magnitude of artificial tactile percepts across all testing conditions. On the basis of principles of nerve fiber recruitment, the ACR represents the total population spike count in the activated neural population. Our findings support the hypothesis that population spike count drives the magnitude of tactile percepts and indicate that sensory magnitude can be manipulated systematically by varying a single stimulation quantity.
The sense of proprioception allows us to keep track of our limb posture and movements and the sense of touch provides us with information about objects with which we come into contact. In both senses, mechanoreceptors convert the deformation of tissues-skin, muscles, tendons, ligaments, or joints-into neural signals. Tactile and proprioceptive signals are then relayed by the peripheral nerves to the central nervous system, where they are processed to give rise to percepts of objects and of the state of our body. In this review, we first examine briefly the receptors that mediate touch and proprioception, their associated nerve fibers, and pathways they follow to the cerebral cortex. We then provide an overview of the different cortical areas that process tactile and proprioceptive information. Next, we discuss how various features of objects-their shape, motion, and texture, for example-are encoded in the various cortical fields, and the susceptibility of these neural codes to attention and other forms of higher-order modulation. Finally, we summarize recent efforts to restore the senses of touch and proprioception by electrically stimulating somatosensory cortex. © 2018 American Physiological Society. Compr Physiol 8:1575-1602, 2018.
Through highly precise perceptual and sensorimotor activities, the human tactile system continuously acquires information about the environment. Mechanical interactions between the skin at the point of contact and a touched surface serve as the source of this tactile information. Using a dedicated custom robotic platform, we imaged skin deformation at the contact area between the finger and a flat surface during the onset of tangential sliding movements in four different directions (proximal, distal, radial and ulnar) and with varying normal force and tangential speeds. This simple tactile event evidenced complex mechanics. We observed a reduction of the contact area while increasing the tangential force and proposed to explain this phenomenon by nonlinear stiffening of the skin. The deformation's shape and amplitude were highly dependent on stimulation direction. We conclude that the complex, but highly patterned and reproducible, deformations measured in this study are a potential source of information for the central nervous system and that further mechanical measurement are needed to better understand tactile perceptual and motor performances.
The temporal evolution of surface strain, resulting from a combination of normal and tangential loading forces on the fingerpad, was calculated from high-resolution images. A customized robotic device loaded the fingertip with varying normal force, tangential direction and tangential speed. We observed strain waves that propagated from the periphery to the centre of the contact area. Consequently, different regions of the contact area were subject to varying degrees of compression, stretch and shear. The spatial distribution of both the strains and the strain energy densities depended on the stimulus direction. Additionally, the strains varied with the normal force level and were substantial, e.g. peak strains of 50% with a normal force of 5 N, i.e. at force levels well within the range of common dexterous manipulation tasks. While these observations were consistent with some theoretical predictions from contact mechanics, we also observed substantial deviations as expected given the complex geometry and mechanics of fingertips. Specifically, from in-depth analyses, we conclude that some of these deviations depend on local fingerprint patterns. Our data provide useful information for models of tactile afferent responses and background for the design of novel haptic interfaces.
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