Fingerpads Of Monkeys Research Articles

Decoding tactile afferent activity to obtain an estimate of instantaneous force and torque applied to the fingerpad.

Dexterous manipulation is not possible without sensory information about object properties and manipulative forces. Fundamental neuroscience has been unable to demonstrate how information about multiple stimulus parameters may be continuously extracted, concurrently, from a population of tactile afferents. This is the first study to demonstrate this, using spike trains recorded from tactile afferents innervating the monkey fingerpad. A multiple-regression model, requiring no a priori knowledge of stimulus-onset times or stimulus combination, was developed to obtain continuous estimates of instantaneous force and torque. The stimuli consisted of a normal-force ramp (to a plateau of 1.8, 2.2, or 2.5 N), on top of which -3.5, -2.0, 0, +2.0, or +3.5 mNm torque was applied about the normal to the skin surface. The model inputs were sliding windows of binned spike counts recorded from each afferent. Models were trained and tested by 15-fold cross-validation to estimate instantaneous normal force and torque over the entire stimulation period. With the use of the spike trains from 58 slow-adapting type I and 25 fast-adapting type I afferents, the instantaneous normal force and torque could be estimated with small error. This study demonstrated that instantaneous force and torque parameters could be reliably extracted from a small number of tactile afferent responses in a real-time fashion with stimulus combinations that the model had not been exposed to during training. Analysis of the model weights may reveal how interactions between stimulus parameters could be disentangled for complex population responses and could be used to test neurophysiologically relevant hypotheses about encoding mechanisms.

Distribution and terminal arborizations of cutaneous mechanoreceptors in the glabrous finger pads of the monkey.

Recent electrophysiological studies demonstrated that neurons in the somatosensory cortex of monkeys respond to tangential forces applied to glabrous skin. To unravel the peripheral basis for this cortical response, we determined the distribution of presumptive low-threshold mechanoreceptors innervating the distal finger pads of monkeys. Endings were reconstructed in immunolabeled serial sections imaged by epifluorescence and confocal microscopy. Although classically implicated as cutaneous stretch receptors, no Ruffini corpuscles were found in the glabrous skin. Ruffini-like endings were only detected at the base of the finger nails. Pacinian corpuscles were sparsely distributed in the deep dermis. Meissner corpuscles (MCs) in dermal papillary ridges had a comparably high density in the thumb, index, and fifth fingers. Each MC was innervated by several large-caliber axons. Within the limits of our reconstructions, some of these axons terminated in only one MC, whereas others innervated several MCs. Merkel endings covered about 80% of the base of the intermediate epidermal ridges that form the pattern of fingerprints. In some cases, the distal tip of a Merkel-related axon gave rise to a several terminal branches that supplied endings to tightly circumscribed (30-70 microm) clusters of Merkel cells. In other cases, the nodes of axons gave rise to en passant branches that formed extended chains of endings among Merkel cells spread over territories up to 300 microm long. Based on their relatively diffuse distributions, the axons that innervate multiple MCs or the axons with en passant Merkel terminations seem most suited to transduce tangential forces.

Encoding of shape and orientation of objects indented into the monkey fingerpad by populations of slowly and rapidly adapting mechanoreceptors.

The peripheral neural representation of object shape and orientation was studied by recording the responses of a spatially distributed population of rapidly and slowly adapting type I mechanoreceptors (RAs and SAs, respectively) to objects of different shapes and orientations indented at a fixed location on the fingerpad of the anesthetized monkey. The toroidal objects had a radius of 5 mm on the major axis, and 1, 3, or 5 mm on the minor axis. Each object was indented into the fingerpad for 4 s at orientations of 0, 45, 90, and 135 degrees using a contact force of 15 gwt. Estimations of the population responses (PRs) were constructed by combining the responses of 91 SA and 97 RA single afferents at discrete times during the indentation. The PR was composed of the neural discharge rates (z coordinate) plotted at x and y coordinates of the most sensitive spot of the receptive field. The shapes of the PRs were related to the shapes of the objects by fitting the PRs with Gaussian surfaces. The orientations of the PRs were determined from weighted principal component analyses. The SA PR encoded both the orientation and shape of the objects, whereas the RA PR did neither. The SA PR orientation was biased toward the long axis of the finger. The RA PR encoded orientation only for the object with the highest curvature but did so ambiguously. Only the SA PR was well fit by a Gaussian surface. The shape of the object was discriminated by the SA PR within the first 500 ms of contact, and the form of the SA PR remained constant during the subsequent 3.5 s. This was manifested by constant widths of the PR along the major and minor axes despite a peak response that decreased from its maximum at 200 ms to an asymptotic value starting at 1 s. Thus the shape and orientation of each object were coded by the shape and orientation of the SA PR.

Neural encoding of shape: responses of cutaneous mechanoreceptors to a wavy surface stroked across the monkey fingerpad.

1. The role of cutaneous mechanoreceptors in the tactile perception of shape was investigated. Objects whose surfaces were shaped as a pattern of smooth, alternating convex and concave cylindrical surfaces of differing radii of curvature were constructed such that there were no discontinuities in the slope of the surface. These "wavy surfaces" were stroked across the fingerpad of the anesthetized monkey and electrophysiological responses of slowly adapting type I mechanoreceptive afferents (SAs) and rapidly adapting type I mechanoreceptive afferents (RAs) were recorded. 2. For both SAs and RAs, each convexity indenting the skin evoked a burst of impulses and each concavity of the same curvature that followed elicited a pause in response. "Spatial event plots" (SEPs) of the occurrence of action potentials as a function of the location of the object on the receptive field were obtained and interpreted as the responses of a spatially distributed population of fibers. With increasing magnitude of curvature (equivalently, decreasing radius of curvature) of convexity, the mean width of the burst in the SEPs for each fiber type (representing the width of a region of skin containing active fibers) decreased and the mean discharge rate during the burst increased. Over a range of velocities of stroking from 1 to 40 mm/s, the number of RAs activated increased with velocity, whereas SAs were active at all velocities. For both SAs and RAs, the burst rates increased with velocity, whereas the widths of the bursts and pauses remained approximately invariant. Thus the spatial measures of burst or pause width provide a robust representation of the size of a feature on the object surface. 3. For a given velocity of stroking, the spatially distributed pattern of averaged discharge rates (spatial rate profile, SRP) provided a representation of the shape of the wavy surface. The distance between neighboring peaks in the SRP for individual RAs and SAs was approximately the same as the distance between the peaks of the wavy surface. The averaged SRP for a population of SAs provided a better representation of shape than that for RAs. Whereas active regions in the SEP can be isomorphic to the two dimensional form of the stimulus "footprint" in contact with the skin surface, the SRP, which in addition encodes the features of the stimulus in the third dimension normal to the skin surface, is not isomorphic to the stimulus shape. 4. When the sizes as well as the shapes of objects are varied, it is hypothesized that a central processing mechanism extracts the invariant property of shape from the slopes of the rising and falling phases of an SRP that has been normalized for overall differences in discharge rates. These differences would be expected to occur with variations in the parameters of stimulation such as compressional force, stroke trajectory, and stroke velocity. It was shown that a common feature of the mean SRP for SAs evoked by each wavy surface convexity, regardless of its radius, was the constancy of the slope from the base to the peak and from the peak to the base. Thus a possible code for the constant curvature of a cylinder is the constancy of the slopes along the rising and declining phases of the triangular-shaped spatial response profile evoked in the SA population by the cylindrical convexity.

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.

Spatial and temporal factors determining afferent fiber responses to a grating moving sinusoidally over the monkey's fingerpad

Gratings of alternating grooves and ridges were moved sinusoidally across the fingerpads of anesthetized monkeys, while responses were recorded from individual slowly adapting afferents (SAs), rapidly adapting afferents (RAs), and Pacinian afferents (PCs) in the median nerve. The stimulus comprised 2 spatial variables, namely, groove width (G) and ridge width (W), and 2 temporal variables, namely, the peak speed of movement (S) and the peak temporal frequency (F) at which successive spatial cycles of the grating pass over a point in the receptive field. The responses of all 3 fiber types were determined by only 1 spatial variable, G, and only 1 temporal variable, F. Changes in W or S affected responses only if there was a concomitant change in either G or F. Responses were phase-locked to the occurrence of successive spatial cycles of the grating, and we have used the number of impulses elicited by a single spatial cycle as the fundamental measure of response. An equation of the form I = cGaexp(-b square root of F) describes the responses of all 3 fiber types. For SAs, the effect of groove width was greater (a = 2.64) than for RAs and PCs (a = 0.924 and 1.05, respectively). The reduction in response with frequency was most marked for SAs (b = 0.262), and greater for PCs (b = 0.167) than for RAs (b = 0.130). From the equation, the instantaneous response during the entire sinusoidal cycle was reconstructed as well as a second measure, the mean cyclic response. These 2 measures behaved differently with changes in the stimulus parameters. The temporal properties of the fibers, as revealed by gratings, may appear to be in conflict with those established by vibratory threshold studies; in fact, they are compatible with suprathreshold responses to vibrating probes.

Perceived roughness of a grating: correlation with responses of mechanoreceptive afferents innervating the monkey's fingerpad

Human subjects scaled gratings of alternating grooves and ridges for perceived roughness. Roughness increased with an increase in groove width and decreased with an increase in ridge width, but the effect of groove width was much greater than the effect of ridge width. In corresponding neurophysiological experiments, the gratings were moved sinusoidally across the receptive fields of single mechano-receptive afferents innervating the fingerpads of anesthetized monkeys. The measure of response used was the mean cyclic discharge rate (averaged over one cycle of the sinusoid). Slowly adapting afferents (SAs), rapidly adapting afferents (RAs), and Pacinian afferents (PCs) all showed a marked increase in response when groove width increased. An increase in ridge width had no consistent effect on the responses of SAs or RAs but resulted in a small decrease in the response of PCs. The response to a smooth surface differed significantly from the responses to the finer gratings only for the RAs. An alternative measure of response (the number of impulses elicited by each spatial cycle of the grating) increased with an increase in ridge width for all 3 fiber types. Thus, the large effect of groove width on perceived roughness can be accounted for by the mean cyclic discharge rate in the active afferent fibers. The smaller effect of ridge width can be accounted for by the number of impulses per spatial cycle of the grating.

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.

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.

Tactile discrimination of shape: responses of slowly adapting mechanoreceptor afferents to a step stroked across the monkey fingerpad

The representation of shape in the responses of slowly adapting mechanoreceptive afferent fibers (SAs) in monkeys was investigated. A series of flat plates was used, each having an increase in thickness (a step) in the middle so that one-half of the plate was thicker than the other. The cross-sectional shape of the step approximated that of a half-cycle of a sinusoid. The height of the step was fixed at 0.5 mm, while its width (half-cycle wavelength) was varied from 0 to 3.13 mm, resulting in step shapes that varied in steepness and curvature. The steps fell into 2 categories, characterized as “steep” and “gradual.” A servocontrolled mechanical stimulator stroked each step across the distal fingerpad from the high to the low side of the step and back, while maintaining the contact force at 20 gm wt. Evoked action potentials in single SAs innervating the fingerpads of anesthetized monkeys were recorded. Each SA's response to a step provided a spatial response profile (discharge rate as a function of step position) that reflected the distribution of curvature across the step shape. All the major features of the SA response could be consistently explained as being due to the sensitivity of the SA to the amount and rate of change in skin curvature. The response profile was altered by changes in stroke direction, step shape, and stroke velocity. Differences in stroke direction (back and forth) were indicated by differences in pattern of response: a “burst-pause-burst” for strokes from high to low, and a “pause-burst-pause” for strokes from low to high; a greater discharge rate in response to the step for low to high strokes, and for some SAs, the reduction or absence of basal discharge in one of the directions. The discharge rate during the burst for either direction of stroking was greater for steep than for gradual steps, and increased, for a given step shape, with increases in stroke velocity. Regardless of differences in stroke velocity, steep steps were distinguished from gradual steps by having narrower burst widths for low-to-high strokes and narrower pause widths for high-to-low strokes. The same stimuli were delivered to the human fingerpad, and the capacities of humans to discriminate between the steps were measured. It was concluded that the spatial features of SA responses, representing the widths of regions of active and inactive SA populations, as well as the intensive feature of discharge rate, accounted for the gross sensory discriminations of shape.(ABSTRACT TRUNCATED AT 400 WORDS)

Tactile discrimination of shape: responses of slowly and rapidly adapting mechanoreceptive afferents to a step indented into the monkey fingerpad

The representation of shape in the responses of monkey cutaneous mechanoreceptive afferents to steps of varying shape vertically indented into the fingerpad was studied. A series of flat plates was used, each with a step change in thickness in the middle so that one-half of the plate was thicker than the other. The cross-sectional shape of the step approximated that of a half-cycle sinusoid, 0.5 mm high, that was varied in half-cycle wavelength (step width) and hence in steepness and curvature. The steps fell into 2 categories, characterized as "steep" and "'gradual." Evoked action potentials were recorded from single, slowly adapting and from rapidly adapting Meissner corpuscle mechanoreceptive afferent fibers (SA and RA, respectively) innervating the fingerpad of the anesthetized monkey while each step was indented at a succession of lateral positions across the fiber's receptive field. The responses of each SA provided a spatial response profile (number of evoked impulses as a function of step position) that was directly related to the variation in curvature across the step. The rate of discharge was greatest under the sharpest (convex) portion of the step, least under the adjacent concave portion, and intermediate under the flat portions of the steps. The results indicated an exquisite sensitivity of the SA, even during the ramp phase of vertical indentation, to the changes in skin curvature. The spatial response profile remained relatively undistorted over time during the ensuing steady phase, while the contrast between the peak and the minimum response improved. RAs responded only during the ramp phase and with fewer responses, and gave rise to a poorly modulated spatial response profile, even though half of the RAs tested showed limited sensitivity to the amount or rate of change of skin curvature. It was hypothesized that RA responses are predominantly influenced by the vertical velocity of the most sensitive spot in the receptive field. When the same step stimuli were applied to the human fingerpad, the capacities of humans to discriminate differences in step shape were found to correlate with the discriminability of SAs, as opposed to the considerably poorer discriminability of RAs. It is concluded that information concerning the local curvature and hence the shape of objects indenting the skin is primarily coded by the SAs. In the 2 preceding papers (LaMotte and Srinivasan, 1987a, b), we investigated the responses of SAs and RAs to the same sinusoidal steps stroked back and forth across the fingerpad under constant compressional force.(ABSTRACT TRUNCATED AT 400 WORDS)

Tactile discrimination of shape: responses of rapidly adapting mechanoreceptive afferents to a step stroked across the monkey fingerpad

The representation of shape in the responses of slowly adapting mechanoreceptive afferent fibers (SAs) in monkeys was investigated. A series of flat plates was used, each having an increase in thickness (a step) in the middle so that one-half of the plate was thicker than the other. The cross-sectional shape of the step approximated that of a half-cycle of a sinusoid. The height of the step was fixed at 0.5 mm, while its width (half-cycle wavelength) was varied from 0 to 3.13 mm, resulting in step shapes that varied in steepness and curvature. The steps fell into 2 categories, characterized as "steep" and "gradual." A servocontrolled mechanical stimulator stroked each step across the distal fingerpad from the high to the low side of the step and back, while maintaining the contact force at 20 gm wt. Evoked action potentials in single SAs innervating the fingerpads of anesthetized monkeys were recorded. Each SA's response to a step provided a spatial response profile (discharge rate as a function of step position) that reflected the distribution of curvature across the step shape. All the major features of the SA response could be consistently explained as being due to the sensitivity of the SA to the amount and rate of change in skin curvature. The response profile was altered by changes in stroke direction, step shape, and stroke velocity. Differences in stroke direction (back and forth) were indicated by differences in pattern of response: a "burst-pause-burst" for strokes from high to low, and a "pause-burst-pause" for strokes from low to high; a greater discharge rate in response to the step for low to high strokes, and for some SAs, the reduction or absence of basal discharge in one of the directions. The discharge rate during the burst for either direction of stroking was greater for steep than for gradual steps, and increased, for a given step shape, with increases in stroke velocity. Regardless of differences in stroke velocity, steep steps were distinguished from gradual steps by having narrower burst widths for low-to-high strokes and narrower pause widths for high-to-low strokes. The same stimuli were delivered to the human fingerpad, and the capacities of humans to discriminate between the steps were measured. It was concluded that the spatial features of SA responses, representing the widths of regions of active and inactive SA populations, as well as the intensive feature of discharge rate, accounted for the gross sensory discriminations of shape.(ABSTRACT TRUNCATED AT 400 WORDS)

Tactile spatial resolution. II. Neural representation of Bars, edges, and gratings in monkey primary afferents.

Tactile spatial resolution. II. Neural representation of Bars, edges, and gratings in monkey primary afferents.

Peripheral neural representation of the spatial frequency of a grating moving across the monkey's finger pad.

1. Responses in mechanoreceptive afferent fibres innervating the monkey's finger pads were examined when a ridged surface ("grating') was moved across the fibre's receptive field with a specified velocity and applied force. 2. The stimulus feature represented in single fibre responses was the temporal frequency of the moving grating (stimulus temporal frequency = velocity of moving surface/spatial period); information about the spatial period of the grating was represented equivocally. 3. Peripheral neural representation of the grating's spatial period (or spatial frequency) depended on information signalled by the responding fibre population rather than by individual fibres. 4. The three mechanoreceptive fibre populations responded differentially to a grating moving across the finger pad. Slowly adapting fibres coded best those stimulus combinations with a stimulus temporal frequency in the range 20-60 Hz, rapidly adapting fibres coded best those with frequencies of 60-200 Hz, and Pacinian fibres best defined those stimuli with a high temporal frequency (100-300 Hz). 5. Applying the moving grating to the skin with varying radial forces in the range 20-60 g wt. did not greatly modify the pattern of discharge in the responding fibre populations.

Peripheral neural representation of spatial dimensions of a textured surface moving across the monkey's finger pad.

1. The responses of single cutaneous mechanoreceptive fibres evoked by a geometrically patterned surface sweeping across the skin were examined. The surfaces used were each a fine diamond-shaped array of "dots' in relief against a flat background. The fibres examined were rapidly adapting, slowly adapting and Pacinian fibres innervating the monkey's finger pad skin. 2. Each fibre's response to the two-dimensioned surface was assessed using a procedure in which the surface was swept across the fibre's receptive field many times, the position of the surface relative to the underlying receptive field being precisely known at any instant in time. Between each successive sweep the stimulus surface was shifted lateral to the direction of movement by a small increment. The response pattern generated by this scanning procedure specified the extent to which a single response of the fibre was dependent on the spatial and temporal dimensions of the stimulus. 3. The invariant spatial features of the moving surface were represented only in the responses of populations of fibres; responses of the constituent fibres always confounded the information relayed about the surface pattern and its rate of movement across the skin. 4. Factors determining the representation of the spatial and temporal characteristics of the moving surface in the responding mechanoreceptive fibre population were examined. These included the response characteristics of the constituent fibres, the innervation density, and the total number of fibres engaged by the moving surface.