A Continuum Mechanical Model of Mechanoreceptive Afferent Responses to Indented Spatial Patterns

Arun, S. P.; Bensmaı̈a, Sliman J.; Johnson, Kenneth O.

doi:10.1152/jn.01240.2005

Cited by 124 publications

(143 citation statements)

References 40 publications

(71 reference statements)

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“…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. from contact mechanics, such as edge enhancement and surround suppression (15,16). The dynamic component propagates through the skin surface as a wave and confers to afferents the ability to respond to vibration at a distance from the contact point (5).…”

Section: Resultsmentioning

confidence: 99%

Simulating tactile signals from the whole hand with millisecond precision

Saal

Delhaye

Rayhaun

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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223

251

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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...

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Section: Resultsmentioning

confidence: 99%

Simulating tactile signals from the whole hand with millisecond precision

Saal

Delhaye

Rayhaun

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

223

251

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“…The images show the indentation and strain profiles of the plaids. The strain profiles at the approximate depth of the receptor sheet (500 m under the surface of the skin) were estimated by using a continuum mechanical model (33). When one component was dominant, the perceived direction of the stimulus was determined by the direction of that component; when the intensities of the two gratings were similar, the stimulus was perceived as a plaid moving in the direction that bisected the two components' directions.…”

Section: Resultsmentioning

confidence: 99%

“…Third, skin mechanics enhance some features while making others intangible in a manner that has no direct analogue in vision (32,33). The perceived direction of the plaids could be predicted from their strain profiles (but not their indentation profiles): The strain profiles-computed at each time step-of patterns that evoked pattern motion were almost completely plaid-like whereas the strain profiles of patterns that evoked component motion fell within the continuum between plaid and grating ( Fig.…”

Section: Resultsmentioning

confidence: 99%

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The tactile integration of local motion cues is analogous to its visual counterpart

Pei

Hsiao

Bensmaı̈a

2008

Proc. Natl. Acad. Sci. U.S.A.

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The visual and somatosensory systems have been shown to process spatial information similarly. Here we investigate tactile motion processing using stimuli whose perceptual properties have been well established in vision research, namely superimposed gratings (plaids), barber poles, and bar fields. In both modalities, information about stimulus motion (speed and direction) conveyed by neurons at low levels of sensory processing is ambiguous, a conundrum known as the aperture problem. Our results suggest that the tactile perception of motion, analogous to its visual counterpart, operates in multiple stages: first, the perceived direction of motion is determined by a majority vote from local motion detectors, which are subject to the aperture problem. As in vision, the conflict between the cues from terminators and other local motion cues is gradually resolved over time so that the perceived direction approaches the veridical direction of motion.aperture problem ͉ psychophysics ͉ plaid ͉ barber pole ͉ somatosensory B oth vision and touch share the common problem of inferring stimulus form, texture, and motion from a spatiotemporal pattern of activation across a two-dimensional sensory sheet (i.e., the retina and skin). The two systems have been found to process information about two-dimensional spatial form in a similar fashion (1-3). In both systems, information about motion can be acquired by analyzing how stimulus contours change over time. Both the visual and somatosensory systems may therefore have evolved analogous mechanisms to process motion information as well. Then again, the analogy between the two systems is not absolute: for instance, depth ordering and transparency are problems that have no obvious analogue in the cutaneous sense (although palpation through gloves may involve a tactile equivalent of transparency). Furthermore, shear forces, which have no direct visual analogue, may contribute to the tactile perception of motion (4, 5). These differences between vision and touch may lead to differences in the way the two systems process motion.The study of motion processing provides an opportunity to address an important question in sensory neuroscience, namely: how is the environment represented at each stage of perceptual processing? Indeed, the speed and direction of motion of individual (one-dimensional) edges is ambiguous because information about the motion component parallel to their orientation is not available, a predicament known as the aperture problem (6) (Fig. 1). To acquire a veridical percept of an object's direction of motion, then, it is often necessary to integrate motion information across multiple stimulus contours that differ in orientation (7,8) or to rely on so-called terminators-such as end points, corners, and intersections-whose direction of motion is unambiguous (9, 10).The aperture problem is inherent to individual neurons at low levels of processing because these neurons have spatially restricted receptive fields and only ''see'' local contours of the stimulus. From the sta...

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“…In the simple ramp-and-hold mode, spatial patterns such as gratings, sinusoids, spheres, and letters can be generated, as long as the temporal profile of the stimulus simply consists of an initial on-ramp, a sustained phase, and an off-ramp. These types of stimuli were used in a study to generate a continuum mechanical model of mechanoreceptive afferent responses to arbitrary spatial patterns (Sripati et al, 2006a). Another application of this stimulus-generation mode is receptive field mapping.…”

Section: Applicationsmentioning

confidence: 99%

A dense array stimulator to generate arbitrary spatio-temporal tactile stimuli

Killebrew

Bensmaı̈a

Dammann

et al. 2007

Journal of Neuroscience Methods

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The generation and presentation of tactile stimuli presents a unique challenge. Unlike vision and audition, in which standard equipment such as monitors and audio systems can be used for most experiments, tactile stimuli and/or stimulators often have to be tailor-made for a given study. Here, we present a novel tactile stimulator designed to present arbitrary spatio-temporal stimuli to the skin. The stimulator consists of 400 pins, arrayed over a 1 cm 2 area, each under independent computer control. The dense array allows for an unprecedented number of stimuli to be presented within an experimental session (e.g., up to 1200 stimuli per minute) and for stimuli to be generated adaptively. The stimulator can be used in a variety of modes and can deliver indented and scanned patterns as well as stimuli defined by mathematical spatio-temporal functions (e.g., drifting sinusoids). We describe the hardware and software of the system, and discuss previous and prospective applications.

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A Continuum Mechanical Model of Mechanoreceptive Afferent Responses to Indented Spatial Patterns

Cited by 124 publications

References 40 publications

Simulating tactile signals from the whole hand with millisecond precision

Simulating tactile signals from the whole hand with millisecond precision

The tactile integration of local motion cues is analogous to its visual counterpart

A dense array stimulator to generate arbitrary spatio-temporal tactile stimuli

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