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.

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.

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.

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.

A stimulator for moving textured surfaces sinusoidally across the skin.

The stimulator allows textured surfaces to be moved sinusoidally across the skin of the fingerpad. Sinusoidal motion is produced by a "scotch yolk" driven by a DC motor. The amplitude of movement is adjustable up to a maximum of 80 mm peak to peak and the frequency is continuously adjustable from 0.1 Hz to 2.0 Hz. Movement of the surface is monitored by an optical transducer and contact force between the finger and the surface is monitored by a strain gauge bridge. The stimulator is simple and robust and is suitable for both neurophysiological and psychophysical experiments in animals and humans.

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.

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.

The influence of stimulus velocity on the responses of single neurones in the striate cortex.

1. Using a multi-histogram technique forty-seven response-velocity curves were prepared for a variety of visual stimuli presented to twenty-one cells in the striate cortex of the anaesthetized, paralysed cat. 2. The character of each velocity-response curve varied according to the measurement used in assessing a response. Reasons are advanced for sampling the response over a single bin of short duration at the peak of the discharge in each average response histogram. 3. The sharpness of tuning varied markedly throughout the population of cells but it was not possible to establish any definitive class differences. 4. For simple and complex cell categories there was considerable overlap in both the range of effective stimulus velocities and the distribution of the optimal velocities. An observation not emphasized in the past was that some simple cells responded to very fast stimuli while a number of complex cells were driven by very slowly moving stimuli. 5. Generally changes in stimulus parameters such as the polarity of contrast of a moving edge, its orientation or direction of movement produced only slight modifications in the profile of the velocity-response curve. 6. The abolition of the response of simple cells that failed to be driven by rapidly moving stimuli was shown to be due to the entry of the stimulus into the inhibitory flank distal to the discharge region. When the movement of the stimulus was confined to the discharge region there was little evidence of velocity dependence in the response. The duration over which the inhibition from the distal flank remained effective was evaluated for representative simple cells.

Direction selectivity of complex cells in a comparison with simple cells.

Following our earlier study on direction selectivity in simple cells (5), the present findings on complex cells made it possible to compare the direction selectivity in the two types of striate cell. Common properties were found in the dimension of the smallest stimulus displacement giving a direction-selective response and in the role of inhibition in suppressing the response as the stimulus moved in the nonpreferred direction. However, the effectiveness of this inhibition varied in the two cell types since it suppressed both driven and spontaneous activity in the simple cell, but only driven firing in the complex cell. It is argued that direction selectivity must enter the response before the complex cell if the inhibition responsible for it's generation fails to influence the spontaneous activity of the cell. The consequences of this finding are considered in the terms of parallel or sequential processing of visual information in striate cortex.

Sinusoidal movement of a grating across the monkey's fingerpad: representation of grating and movement features in afferent fiber responses.

Gratings of alternating grooves and ridges were moved sinusoidally back and forth across the monkey's fingerpad. Each grating was completely specified by its spatial period and the movement by its peak speed: together these determined the peak temporal frequency at which grating ridges passed over the skin. Responses of cutaneous, mechanoreceptive afferents innervating the fingerpad were characterized in terms of these 3 parameters. Slowly adapting afferents (SAs), rapidly adapting afferents (RAs), and Pacinian afferents (PCs) had different characteristics. The responses (mean cyclic discharge rates) of the SAs increased when the spatial period of the grating increased (and peak speed of movement remained constant) but did not change with changes in the peak speed of the movement (while the spatial period of the grating remained constant). Conversely, the responses of the PCs increased when the peak speed of movement increased (and the spatial period remained constant) but were relatively insensitive to changes in the spatial period of the grating (while the peak speed remained constant). The responses of the RAs increased as the spatial period of the grating increased (and peak speed remained constant) and also increased as the peak speed of movement increased (and the grating spatial period remained constant). When the peak temporal frequency of the grating ridges was held constant, the responses of all 3 afferent groups changed with changes in the grating spatial period or in the peak speed of movement. Information about the spatial features of the grating, independent of the peak speed of movement, was present in the SA population response and in the ratios of the RA and PC population responses. Information about the peak speed of movement, independent of the spatial period of the grating, was present in the PC population response and could be extracted from the RA population response.

Sinusoidal movement of a grating across the monkey's fingerpad: temporal patterns of afferent fiber responses.

Responses were recorded from cutaneous afferents innervating mechanoreceptors in the monkey's fingerpad, while gratings of alternating grooves and ridges were moved sinusoidally across their receptive fields. The gratings were specified by their spatial period and the movement by its peak speed: together these determined the peak temporal frequency at which grating ridges passed over the receptive field. During the central 42 degrees of each half cycle of movement, the speed and thus the temporal frequency of the grating ridges remained constant to within 6.6% of their peak values. In this region the responses of all afferents were phase-locked to the temporal sequence of grating ridges. The number of impulses elicited by each grating ridge was a function of the stimulus variables. For all 3 afferent classes--namely, slowly adapting afferents (SAs), rapidly adapting afferents (RAs), and Pacinian afferents (PCs)--the number of impulses per grating ridge increased as the spatial period of the grating increased (while the peak speed of movement was held constant). Similarly, for all 3 classes, the number of impulses per ridge decreased as the peak speed of movement increased (while the spatial period of the grating remained constant). When the peak temporal frequency of the grating ridges was held constant, for SAs and RAs the number of impulses per ridge increased with an increase in the spatial period of the grating and thus with an increase in the peak speed. These phase-locked responses provided information about the peak temporal frequency of the grating ridges independent of the grating spatial period and of the peak speed of movement. The shape of the response profile during a half cycle of movement was different for different afferents. Many of the RA response profiles were close to sinusoidal. The SA and PC profiles tended to have reduced peaks or raised troughs, resulting in flatter profiles. Other departures from sinusoidal profiles were also seen.

Sinusoidal movement of a grating across the monkey's fingerpad: effect of contact angle and force of the grating on afferent fiber responses.

Responses were recorded from cutaneous afferents innervating mechanoreceptors in the monkey's fingerpad. When gratings of alternating grooves and ridges were moved sinusoidally back and forth across the receptive field, the responses of the afferent were often not equal for the 2 directions of movement. To investigate this phenomenon, the position of the center of the afferent's receptive field, relative to the contact area between the grating and the finger, was varied systematically. For some afferents, regardless of these relative positions, the response was always greater for a particular direction of movement. For other afferents, regardless of these relative positions, the responses for the 2 directions of movement were always equal. For a minority of afferents, the response was greater for movement in one particular direction for some relative positions and greater for movement in the opposite direction for other relative positions. Slowly adapting afferents (SAs), rapidly adapting afferents (RAs), and Pacinian afferents (PCs) exhibited all 3 types of response patterns. We could not relate these patterns to the afferent type or to the positions, in the fingerpad, of the receptive field center. The contact force between the grating and the finger was varied by varying the contact displacement (indentation). Two grating spatial periods were used. For SAs and PCs the response increased with increasing indentation for both gratings. For RAs the response to the finer grating increased with increasing indentation, but the response to the coarser grating did not.

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.

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.

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.