The Representation of Stimulus Orientation in the Early Stages of Somatosensory Processing

Bensmaı̈a, Sliman J.; Denchev, Peter V.; Dammann, J. Francis; Craig, James C.; Hsiao, Steven S.

doi:10.1523/jneurosci.4162-07.2008

Cited by 163 publications

(226 citation statements)

References 30 publications

Supporting

Mentioning

212

Contrasting

Order By: Relevance

“…This match in timing further corroborates the claim that the temporal precision of the models, this time measured at the population level, is similar to that of measured afferent populations. Interestingly, SA1 and RA populations carry signals that are equally informative about orientation, contrary to what might be expected based on their single-unit responses (33,39). Indeed, individual SA1 fibers tend to convey more precise information about spatial form, but this advantage at the single-cell level seems to be compensated for by the greater number of RA fibers.…”

Section: B-d)mentioning

confidence: 84%

Simulating tactile signals from the whole hand with millisecond precision

Saal

Delhaye

Rayhaun

et al. 2017

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

223

251

View full text Add to dashboard Cite

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...

show abstract

Section: B-d)mentioning

confidence: 84%

Simulating tactile signals from the whole hand with millisecond precision

Saal

Delhaye

Rayhaun

et al. 2017

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

223

251

View full text Add to dashboard Cite

show abstract

“…However, our sense of touch conveys much more elaborate information about objects: information about their size and shape, about their material properties and surface microstructure (texture), and about how they move across the skin [38]. In somatosensory cortex, different populations of neurons encode these different properties: some S1 neurons respond to the shape of objects by encoding the orientation of their edges [39]; others are sensitive to the curvature of object contours [40]; others are tuned for the direction in which the objects move across the skin [41]; others seem to encode coarse [42] and fine [43] surface microstructure. Higherlevel object features seem to be encoded more explicitly at higher levels of cortical processing, with relatively nonselective responses in area 3b and stronger selectivity in areas 1 and 2.…”

Section: Expanding the Sensory Repertoirementioning

confidence: 99%

Biological and bionic hands: Natural neural coding and artificial perception

Bensmaı̈a

2015

2015 IEEE World Haptics Conference (WHC)

View full text Add to dashboard Cite

One contribution of 15 to a theme issue 'Controlling brain activity to alter perception, behaviour and society'. The first decade and a half of the twenty-first century brought about two major innovations in neuroprosthetics: the development of anthropomorphic robotic limbs that replicate much of the function of a native human arm and the refinement of algorithms that decode intended movements from brain activity. However, skilled manipulation of objects requires somatosensory feedback, for which vision is a poor substitute. For upper-limb neuroprostheses to be clinically viable, they must therefore provide for the restoration of touch and proprioception. In this review, I discuss efforts to elicit meaningful tactile sensations through stimulation of neurons in somatosensory cortex. I focus on biomimetic approaches to sensory restoration, which leverage our current understanding about how information about grasped objects is encoded in the brain of intact individuals. I argue that not only can sensory neuroscience inform the development of sensory neuroprostheses, but also that the converse is true: stimulating the brain offers an exceptional opportunity to causally interrogate neural circuits and test hypotheses about natural neural coding.

show abstract

“…The two systems have been found to process information about two-dimensional spatial form in a similar fashion (1)(2)(3). In both systems, information about motion can be acquired by analyzing how stimulus contours change over time.…”

mentioning

confidence: 99%

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

Pei

Hsiao

Bensmaı̈a

2008

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

Self Cite

View full text Add to dashboard Cite

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...

show abstract

The Representation of Stimulus Orientation in the Early Stages of Somatosensory Processing

Cited by 163 publications

References 30 publications

Simulating tactile signals from the whole hand with millisecond precision

Simulating tactile signals from the whole hand with millisecond precision

Biological and bionic hands: Natural neural coding and artificial perception

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

Contact Info

Product

Resources

About