Cutaneous afferents from the monkeys fingers: responses to tangential and normal forces.

Control of tangential force plays a key role in everyday manipulations. In anesthetized monkeys, forces tangential to the skin were applied at a range of magnitudes comparable to those used in routine manipulations and in eight different directions. The paradigm used enabled separation of responses to tangential force from responses to the background normal force. For slowly adapting type I (SAI) afferents, tangential force responses ranged from excitatory through no response to suppression, with both a static and dynamic component. For fast adapting type I (FAI) afferents, responses were dynamic and excitatory only. Responses of both afferent types were scaled by tangential force magnitude, elucidating the neural basis for previous human psychophysical scaling data. Most afferents were direction selective with a range of preferred directions and a range in sharpness of tuning. Both the preferred direction and the degree of tuning were independent of the background normal force. Preferred directions were distributed uniformly over 360 degrees for SAI afferents, but for FAI afferents they were biased toward the proximo-ulnar direction. Afferents from all over the glabrous skin of the distal segment of the finger responded; there was no evident relationship between the position of an afferent's receptive field on the finger and its preferred direction or its degree of tuning. Nor were preferred directions biased either toward or away from the receptive field center. In response to the relatively large normal forces, some afferents saturated and others did not, regardless of the positions of their receptive fields. Total afferent response matched human psychophysical scaling functions for normal force.

The AsTex: clinimetric properties of a new tool for evaluating hand sensation following stroke.

OBJECTIVES: To investigate the clinimetric properties and clinical utility of the AsTex((R)), a new clinical tool for evaluation of hand sensation following stroke. DESIGN: The AsTex((R)) was administered on two occasions separated by a week to appraise test-retest reliability, and by three assessors on single occasion to establish inter-rater reliability. Pilot normative values were collected in an age-stratified sample. Clinical utility was evaluated based on ease of administration, ceiling and floor effects, and responsiveness to sensory recovery. PARTICIPANTS: Test-retest (n = 31) and inter-rater (n = 31) reliability and normative values (n = 95) for the AsTex((R)) were established in neurologically normal participants aged 18-85 years. Test-retest reliability was investigated in 22 individuals a mean of 46 months (range 12-125) post stroke and clinical utility was evaluated in an additional 24 subacute stroke participants a mean of 29.4 days (range 12-41) post stroke. MAIN MEASURE: The AsTex((R)). RESULTS: The AsTex((R)) demonstrated excellent test-retest (intraclass correlation coefficient (ICC) = 0.98, 95% confidence interval (95% CI) = 0.97-0.99) and inter-rater reliability (ICC = 0.81, 95% CI = 0.73-0.87) in neurologically normal participants. Test-retest reliability of the AsTex((R)) in individuals following stroke was excellent (ICC = 0.86, 95% CI = 0.68-0.94). The AsTex((R)) was simple to administer, demonstrated small standard error of measurement (0.14 mm), minimal floor and ceiling effects (12.5% and 8.3%) and excellent responsiveness (standardized response mean = 0.57) in subacute stroke participants. CONCLUSION: The AsTex((R)) is a reliable, clinically useful and responsive tool for evaluating hand sensation following stroke.

How is tactile information affected by parameters of the population such as non-uniform fiber sensitivity, innervation geometry and response variability?

Analysis of population responses in the tactile system requires a step beyond the isomorphic representations that are commonly presented. Using a simple model based on our data for spheres contacting the fingerpad, we illustrate how the parameters of the population itself have a profound effect on the fidelity of neural representations or codes. The effects of these parameters, such as innervation density, variability of sensitivity, type and covariance of noise are not apparent from single unit responses and, at least at present, require a theoretical or modeling approach of some sort.

Encoding of direction of fingertip forces by human tactile afferents.

In most manipulations, we use our fingertips to apply time-varying forces to the target object in controlled directions. Here we used microneurography to assess how single tactile afferents encode the direction of fingertip forces at magnitudes, rates, and directions comparable to those arising in everyday manipulations. Using a flat stimulus surface, we applied forces to a standard site on the fingertip while recording impulse activity in 196 tactile afferents with receptive fields distributed over the entire terminal phalanx. Forces were applied in one of five directions: normal force and forces at a 20 degrees angle from the normal in the radial, distal, ulnar, or proximal directions. Nearly all afferents responded, and the responses in most slowly adapting (SA)-I, SA-II, and fast adapting (FA)-I afferents were broadly tuned to a preferred direction of force. Among afferents of each type, the preferred directions were distributed in all angular directions with reference to the stimulation site, but not uniformly. The SA-I population was biased for tangential force components in the distal direction, the SA-II population was biased in the proximal direction, and the FA-I population was biased in the proximal and radial directions. Anisotropic mechanical properties of the fingertip and the spatial relationship between the receptive field center of the afferent and the stimulus site appeared to influence the preferred direction in a manner dependent on afferent type. We conclude that tactile afferents from the whole terminal phalanx potentially contribute to the encoding of direction of fingertip forces similar to those that occur when subjects manipulate objects under natural conditions.

Tactile discrimination of edge shape: limits on spatial resolution imposed by parameters of the peripheral neural population.

When the flat faces of a coin are grasped between thumb and index finger, a "curved edge" is felt. Analogous curved edges were generated by our stimuli, which comprised the flat face of segments of annuli applied passively to immobilized fingers. Humans could scale the curvature of the annulus and could discriminate changes in curvature of approximately 20 m(-1). The responses of single slowly adapting type I afferents (SAIs) recorded in anesthetized monkeys could be quantified by the product of two factors: their sensitivity and a spatial profile dependent only on the radius of the annulus. This allowed us to reconstruct realistic SAI population responses that included noise, variation in fiber sensitivity, and varying innervation patterns. The critical question was how relatively small populations ( approximately 70 active fibers) can encode edge curvature with such precision. A template-matching approach was used to establish the accuracy of edge representation in the population. The known large interfiber variability in sensitivity had no effect on curvature resolution. Neural resolution was superior to human performance until large levels of central noise were present showing that, unlike simple detection, spatial processing is limited centrally. In contrast to the behavior of mean response codes, neural resolution improved with increasing covariance in noise. Surprisingly, resolution for any single population varied considerably with small changes in the position of the stimulus relative to the SAI matrix. Overall innervation density was not as critical as the spacing of receptive fields at right angles to the edge.

Tactile discrimination of gaps by slowly adapting afferents: effects of population parameters and anisotropy in the fingerpad.

The aim of this study was to determine the acuity of the peripheral tactile system for gaps and to determine how stimulus orientation may impact on this. We quantified the ability of humans to discriminate small differences in gap width using a forced-choice task. Stimuli were presented passively to the distal fingerpad in a region where the skin ridges all run approximately in the same direction. Two standard gap widths were used (2 and 2.9 mm), and the comparison gap widths were larger than the standard gaps. With the gap axis parallel to the skin ridges, the average difference limen was approximately 0.2 mm for both standards. We examined the effect of stimulus orientation by asking subjects to discriminate between a smooth surface and a grating (ridge width, 1.5 mm; groove width, 0. 75 mm). They were able to discriminate the two surfaces when the axis of the grooves was parallel to the skin ridges, but performance was below threshold in the orthogonal orientation. The underlying neural mechanisms were investigated using the gap stimuli to activate single slowly adapting type I mechanoreceptive afferents (SAIs) innervating the fingerpads of anesthetized monkeys. The edges of the gap produced response peaks, and the gap resulted in a trough in the receptive field profiles. The response magnitude at the peaks was greater, and at the troughs was smaller, for larger gap widths and also when the axis of the gap was parallel to the skin ridges as compared with the orthogonal orientation. Simulated SAI population responses showed that response profiles were distorted by variation in afferent sensitivity and by neural noise. Using signal detection theory, based on a neural measure of the gaps computed over the active population, the acuity of the SAIs under realistic population conditions was compared with human performance. These analyses showed how parameters like afferent sensitivity, the pattern and density of innervation, and noise impact on performance and why their impact is different for the two stimulus orientations investigated. The greatest limitation was imposed by noise that is independent of response magnitude, and this effect was greater for stimuli oriented orthogonal to the skin ridges than for the parallel orientation.

Slowly adapting type I afferents from the sides and end of the finger respond to stimuli on the center of the fingerpad.

The central part of the fingerpad in anesthetized monkeys was stimulated by spheres varying in curvature indented into the skin. Responses were recorded from single slowly adapting type I primary afferent fibers (SAIs) innervating the sides and end of the distal segment of the stimulated finger. Although these afferents had receptive field centers that were remote from the stimulus, their responses were substantial. Increasing the curvature of the stimulus resulted in an increased response for most afferents. In general, responses increased most between stimuli with curvatures of 0 (flat) and 80.6 m(-1), with further increases in curvature having progressively smaller effects on the response. We calculated an index of sensitivity to changes in curvature; this index varied widely among the afferents but for most it was less than the index calculated for afferents innervating the fingerpad in the vicinity of the stimulus. Responses of all the SAIs increased when the contact force of the stimulus increased. An index of sensitivity to changes in contact force varied widely among the afferents but in all cases was greater than the index calculated for SAIs from the fingerpad itself. Neither the curvature sensitivity nor the force sensitivity of an afferent was related in any obvious way to the location of its receptive field center on the digit. There was only a minor correspondence between an afferent's sensitivity to force and its sensitivity to curvature. The large number of afferents innervating the border regions of the digit do respond to stimuli contacting the central fingerpad; they convey some information about the curvature of the stimulus and substantial information about contact force.

Effects of nonuniform fiber sensitivity, innervation geometry, and noise on information relayed by a population of slowly adapting type I primary afferents from the fingerpad.

The capacity of a population of primary afferent fibers to signal information about a sphere indenting the fingerpad is limited by factors such as the inhomogeneity of sensitivity among the afferents, the pattern and density of innervation, and the effects of noise (response variability). Using experimental data recorded from single slowly adapting type I afferents (SAIs), we simulated the response of the SAI population to such a stimulus. The human ability to discriminate stimulus curvature, location, and force has been quantified previously. We devised three neural measures, treating them as surrogates for the real neural measures underlying human performance, and explored how population parameters usually overlooked in neural coding studies affect such measures. Variation in sensitivity among SAIs is large; this distorts population response profiles markedly but has no significant impact on the neural measures. Two classes of noise were introduced, one dependent on and the other independent of the level of neural activity. Resolution of the model was compared with discrimination in humans. Correlation of noise among neurons had different effects for the different measures. An increase in correlation decreased resolution in the measure for force but improved resolution in the measure for position. Increasing innervation density (1) always increased resolution for position and (2) increased resolution for force if noise was uncorrelated but had diminishing effects as correlation increased. Correlation and innervation density had complex effects on the measure for curvature, depending on the class of noise. Nonuniformity in the pattern of innervation had negligible effects on resolution.

Control of grip force when tilting objects: effect of curvature of grasped surfaces and applied tangential torque.

When we manipulate objects in everyday tasks, there are variations in the shape of the grasped surfaces, and the loads that potentially destabilize the grasp include time-varying linear forces and torques tangential to the grasped surfaces. Previous studies of the control of fingertip forces for grasp stability have dealt principally with flat grip surfaces and linear force loads. Here, we studied the regulation of grip force with changes in curvature of grasped surfaces and changes in tangential torque applied by the index finger and thumb when humans lifted an object and rotated it about the horizontal grip axis through an angle of 65 degrees. The curvatures of the matched pair of spherical surfaces varied from -50 m-1 (concave with radius 20 mm) to 200 m-1 (convex with radius 5 mm). The applied tangential torque at the orientation of 65 degrees was varied sixfold. Regardless of the values of curvature and end torque, grip force and tangential torque were coordinated, increasing in parallel throughout the tilt with an approximately linear relationship; the slope of the line increased progressively with increasing surface curvature. This parametric scaling of grip force was directly related to the minimum grip force required to prevent rotational slip, resulting in an adequate safety margin against slip in all cases. We conclude that surface curvature parametrically influences grip force regulation when the digits are exposed to torsional loads. Furthermore, the sensorimotor programs that control the grip force apparently predict the effect of the total load comprising linear forces and tangential torques.

Control of grasp stability when humans lift objects with different surface curvatures.

In previous investigations of the control of grasp stability, humans manipulated test objects with flat grasp surfaces. The surfaces of most objects that we handle in everyday activities, however, are curved. In the present study, we examined the influence of surface curvature on the fingertip forces used when humans lifted and held objects of various weights. Subjects grasped the test object between the thumb and the index finger. The matching pair of grasped surfaces were spherically curved with one of six different curvatures (concave with radius 20 or 40 mm; flat; convex with radius 20, 10, or 5 mm) and the object had one of five different weights ranging from 168 to 705 g. The grip force used by subjects (force along the axis between the 2 grasped surfaces) increased with increasing weight of the object but was modified inconsistently and incompletely by surface curvature. Similarly, the duration and rate of force generation, when the grip and load forces increased isometrically in the load phase before object lift-off, were not influenced by surface curvature. In contrast, surface curvature did affect the minimum grip forces required to prevent frictional slips (the slip force). The slip force was smaller for larger curvatures (both concave and convex) than for flatter surfaces. Therefore the force safety margin against slips (difference between the employed grip force and the slip force) was higher for the higher curvatures. We conclude that surface curvature has little influence on grip force regulation during this type of manipulation; the moderate changes in slip force resulting from changes in curvature are not fully compensated for by changes in grip force.

Peripheral neural mechanisms determining the orientation of cylinders grasped by the digits.

When a human grasps a cylindrical object, feedback on the orientation of the cylinder with respect to the axes of the digits is crucial for successful manipulation of the object. We measured the ability of humans to discriminate the orientations of cylinders passively contacting the fingerpad. For a cylinder of curvature of 521 m-1 (radius, 1.92 mm) subjects were able to discriminate, at the 75% level, orientation differences of 5.4 degrees; for a less curved cylinder (curvature, 172 m-1; radius, 5.81 mm) the difference limen decreased to 4.2 degrees. The neural mechanisms underlying the determination of tactile orientation were investigated by recording the responses of single slowly adapting type I afferents (SAIs) innervating the fingerpads of anesthetized monkeys. When cylinders were stepped across the receptive field of an SAI, the resulting response profiles were Gaussian in shape; the shape corresponded to the shape of the cylinder, increasing in height and decreasing in width for more curved cylinders. All SAIs had the same underlying profile shape except for a multiplicative constant determined by the sensitivity of the individual afferent. Thus it was possible to reconstruct the response of the population of active SAIs in the fingerpad. Changing the orientation of the cylinder resulted in a rotation of the population response, but the change in angle of the population response was greater than the change in orientation of the cylinder. This discrepancy increased as the orientation of the cylinder moved closer to the orientation of the axis of the finger and was more pronounced for the less curved cylinder. Measured contact areas between the cylinders and the skin were elliptical, with orientations exceeding those of the cylinder; again the differences were greater for the less curved cylinder and for orientations closer to that of the finger axis. The human discrimination performance could be explained in terms of the SAI population responses.

Encoding of object curvature by tactile afferents from human fingers.

Isolated responses were recorded from fibers in the median nerves of human subjects by using microneurography. Mechanoreceptive afferent fibers with receptive fields on the fingerpads were selected. The fingers were immobilized and spherical stimuli were applied passively to the receptive field with a contact force of 40-, 60-, or 80-g weight. The radii of the spheres were 1.92, 2.94, 5.81, or 12.4 mm or infinity (flat); the corresponding curvatures, given by the reciprocal of the radii, were 694, 340, 172, 80.6, or 0 m-1, respectively. When the spheres were applied to the receptive field center of slowly adapting type I afferents (SAIs), the response increased as the curvature of the sphere increased and also increased as the contact force increased. All SAIs behaved in the same way except for a scaling factor proportional to the sensitivity of the afferent. When a sphere was located at different positions in the receptive field, the shape of the resulting response profile reflected the shape of the sphere; for more curved spheres the profile was higher and narrower (increased peak and decreased width). Slowly adapting type II afferents (SAIIs) showed different response characteristics from the SAIs when spheres were applied to their receptive field centers. As the curvature of the stimulus increased from 80.6 to 172 m-1, the response increased. However, further increases in curvature did not result in further increases in response. An increase in contact force resulted in an increase in the response of SAIIs; this increase was proportionately greater than it was for SAIs. For SAIIs, the shape of the receptive field profile did not change when the curvature of the stimulus changed. For fast-adapting type I afferents (FAIs), the responses were small and did not change systematically with changes in curvature or contact force. Fast-adapting type II afferents (FAIIs) did not respond to our stimuli. Human SAIs, FAIs, and FAIIs behaved like monkey SAIs, FAIs, and FAIIs, respectively. The response of the SAI population contains accurate information about the shape of the sphere and its position of contact on the finger and also indicates contact force. Conversely, whereas SAIIs possess a greater capacity to encode changes in contact force, they provide only coarse information on local shape.

Tactile resolution: peripheral neural mechanisms underlying the human capacity to determine positions of objects contacting the fingerpad.

We measured the ability of humans to discriminate the positions of spherical objects passively contacting the fingerpad. The discrimination threshold averaged 0.55 mm for a moderately curved sphere (radius 5.80 mm) and decreased to 0.38 mm for a more curved sphere (radius 1.92 mm); since the receptor density is about 1 per mm2, these values are substantially smaller than those predicted by the sampling theorem (referred to as hyperacuity). To elucidate the underlying neural mechanisms, responses to the same spheres and random sequences of stimuli were recorded from single Merkel afferents (SAIs) and Meissner afferents (RAs) in anesthetized monkeys. For multiple applications of identical stimuli, coefficients of variation of responses were around 3%. Profiles of responses across the SAI population were "hill-shaped." A change in position of the stimulus on the skin resulted in a matching shift of the profile, evident over the whole profile for the more curved sphere but ony at the skirts for the less curved sphere. The shift in response profiles, relative to the standard deviations, increased as the change in position increased, and was more reliable for the more curved sphere. Responses were measured over four time frames: 0.2, 0.3, 0.5, and 1.0 sec. Although responses increased with an increase in integration time, so, too, did their standard deviations, so that signal-to-noise ratios or the resolution in the SAI population was bout the same at 0.2 sec as at 1.0 sec. Only half the RAs responded; responses were small, but signalled reliable information about the position of the stimulus.

Representation of curved surfaces in responses of mechanoreceptive afferent fibers innervating the monkey's fingerpad.

The aim was to elucidate how the population of digital nerve afferents signals information about the shape of objects in contact with the fingerpads during fine manipulations. Responses were recorded from single mechanoreceptive afferent fibers in median nerves of anesthetized monkeys. Seven spherical surfaces were used, varying from a highly curved surface (radius, 1.44 mm; curvature, 694 m-1) to a flat surface (radius, infinity; curvature, 0 m-1). These were applied to the fibers' receptive fields, which were located on the central portion of a fingerpad. When the objects were located at the centers of the receptive fields, the responses of the slowly adapting fibers (SAIs) increased as the curvature of the surface increased and as the contact force increased. All SAIs behaved in the same way, differing only by a scaling factor (the sensitivity of the individual afferent). Responses of the rapidly adapting afferents were small and did not vary systematically with the stimulus parameters, and most Pacinians did not respond at all. Stimuli were applied at different positions in the receptive fields of SAIs to define the response profiles of the afferents (response as a function of position on the fingerpad). All SAIs had similarly shaped profiles for the same surface curvature and the shape differed for different curvatures. These profiles reflected the shape of the stimulus. An increase in contact force scaled these profiles upward. Thus, the population of digital nerve fibers signals unambiguous information about the shape and contact force of curved surfaces contacting the fingerpad.

Human tactile discrimination of curvature when contact area with the skin remains constant.

A forced choice paradigm was used to measure the capacity of human subjects to discriminate the curvature of stimuli applied passively to the skin of an immobilized finger. The stimuli consisted of spherically curved segments with a base radius of 2.5 mm; thus the area of contact with the fingerpad skin was approximately 19.6 mm2 for all stimuli. There were 2 series of experiments. In series 1, the standard surface had a curvature of 286 m-1 (radius of curvature 3.5 mm); subjects were able to discriminate an increase in curvature of about 13%. In series 2, the standard had a curvature of 154 m-1 (radius 6.5 mm); subjects were able to discriminate an increase in curvature of about 18%. Thus, even when the contact area between the surface and the skin was invariant, humans were able to discriminate small changes in curvature using only information from the cutaneous receptors.

Magnitude estimation of contact force when objects with different shapes are applied passively to the fingerpad.

Stimuli with spherically curved surfaces were presented passively to the fingerpads of human subjects. There were 28 stimuli, consisting of all combinations of 4 different curvatures and 7 different contact forces; these were presented in random order. Subjects scaled their perceived magnitude of the contact force using magnitude estimation. Perceived force increased markedly with an increase in experimentally applied contact force. An increase in curvature resulted in a slight increase in perceived contact force. Thus, when humans are passively presented with objects changing in both shape and contact force, they are able to extract information about the force. Because of the passive nature of the task, all such information must be conveyed to the brain by the cutaneous mechanoreceptors.

Tactile discrimination of curvature by humans using only cutaneous information from the fingerpads.

Spherically curved surfaces were applied, with controlled force, to the fingerpads of human subjects; their fingers were immobilized. The curvature of the surfaces was characterised by the reciprocal of the radius of curvature. In scaling experiments, the subjects' perceived magnitude of curvature increased markedly with an increase in the curvature of the stimulus. An increase in contact force resulted in a slight decrease in perceived curvature. Four discrimination experiments were performed using a forced choice paradigm. Subjects could discriminate, at the 75% level, a flat surface (zero curvature) from a convex curvature of 4.9 m-1 (radius of curvature 204 mm) and from a concave curvature of 5.4 m-1 (radius 185 mm). When discriminating 2 convex spherical surfaces, subjects could discriminate a curvature of 144 m-1 from a curvature of 158 m-1 (radii 6.95 and 6.33 mm respectively), and could discriminate a curvature of 287 m-1 from one of 319 m-1 (radii 3.48 and 3.13 mm respectively); the Weber fraction is about 0.1. Contact areas between the curved surfaces and the fingerpad skin were estimated. There was approximate correspondence between contact areas and the scaling functions.