Slowly Adapting Type I Afferents From the Sides and End of the Finger Respond to Stimuli on the Center of the Fingerpad

James W. Bisley, Antony W. Goodwin, and Heather E. Wheat

Department of Anatomy and Cell Biology, University of Melbourne, Parkville, Victoria 3052, Australia


    ABSTRACT
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Bisley, James W., Antony W. Goodwin, and Heather E. Wheat. Slowly Adapting Type I Afferents From the Sides and End of the Finger Respond to Stimuli on the Center of the Fingerpad. J. Neurophysiol. 84: 57-64, 2000. 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.


    INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

In most studies in which the properties of cutaneous afferents have been investigated, the stimuli were confined to the classical receptive field. Punctate probes indenting or vibrating into the skin of either humans or experimental animals were used to define the temporal or frequency characteristics of the afferents (Knibestol 1973; Talbot et al. 1968). The spatial characteristics of their receptive fields were delineated by varying the position of the stimuli on the skin (Johansson 1978; Phillips and Johnson 1981a; Pubols 1987; Vega-Bermudez and Johnson 1999a,b). These initial studies of the receptive field established the differences in properties between the four classes of afferents that innervate human glabrous skin: the slowly adapting type I and type II afferents (SAIs and SAIIs) and the fast adapting type I and type II afferents (FAIs and FAIIs); for review see Darian-Smith (1984) and Vallbo (1995). Both SAIs and FAIs are usually described as having "small" receptive fields with diameters on the order of a few millimeters.

In a second group of experiments, textured surfaces or fine patterned surfaces consisting of gratings, raised dots, or small letters were scanned across the receptive fields of primary afferent fibers (Darian-Smith and Oke 1980; Johnson and Lamb 1981; LaMotte and Whitehouse 1986). Although such surfaces extend beyond the classical receptive field, the emphasis in these studies was still on the properties of afferents innervating the area of contact. The features of these surfaces (small-scale properties) were represented in the responses of the populations of afferents from the skin, particularly in the responses of the SAI and FAI populations (Goodwin and Morley 1987; Phillips et al. 1990). Both of these populations convey information about the temporal and spatial parameters of surfaces scanned over the skin, with the SAI population appearing to play the major role in signaling spatial information (Blake et al. 1997a,b; Connor and Johnson 1992).

A third group of experiments addressed the issue of how the large-scale properties of objects contacting the fingerpads are represented in the responses of afferents innervating the fingerpads. LaMotte and colleagues used a variety of shaped objects either scanned across the finger or indented into the finger (LaMotte and Srinivasan 1987a,b, 1996; LaMotte et al. 1998; Srinivasan and LaMotte 1987). We have used spherical and cylindrical stimuli indented into the fingerpad (Dodson et al. 1998; Goodwin et al. 1995, 1997). Both SAIs and FAIs, which have a high innervation density on the fingerpad (Darian-Smith and Kenins 1980; Johansson and Vallbo 1979), convey information of importance during contact and manipulation of an object. Information about characteristics of the object such as its local shape, orientation, or position on the skin, are signaled primarily by the SAIs (Dodson et al. 1998; Khalsa et al. 1998; Wheat et al. 1995). The contact force between the finger and the object is also signaled by the SAI population in the region of contact, but this signal starts to saturate at higher forces (Goodwin et al. 1995). One aspect highlighted by these studies is that the multiple parameters of such stimuli can only be represented unambiguously in the responses of populations of afferents.

If the skin on the fingerpad formed an infinite flat surface, then it would be sufficient to characterize the responses of afferents terminating in the region of the stimulus. However, the finger is a closed viscoelastic body with a curved surface (Srinivasan and Dandekar 1996; Tubiana 1981). Thus objects contacting the fingerpad result in visible and obvious deformations on the sides and end of the finger remote from the contact point. The number of afferents innervating this region of skin is large (Darian-Smith and Kenins 1980; Johansson and Vallbo 1979), and it is likely that they will be activated and that they may signal significant information about a stimulus contacting the fingerpad. In the experiments reported here, we addressed this issue by extending our previous studies with spherical stimuli and asked three specific questions. First, when spheres are applied to the central, relatively flat portion of the fingerpad, what is the extent and nature of activity among SAIs innervating the sides and end of the finger? Second, could any activity convey significant information about the curvature of the stimulus? Third, is information about the contact force signaled by these afferents?


    METHODS
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Surgery

Responses were recorded from single primary afferent fibers isolated from the median nerves of six Macaca nemestrina monkeys weighing between 2.1 and 4.2 kg. All experimental procedures were approved by the University of Melbourne ethics committee and conformed to the National Health and Medical Research Council of Australia's Code of Practice for nonhuman primate research. The recording methods were standard (Goodwin et al. 1995; Talbot et al. 1968) and are only described briefly here. The monkeys were initially anesthetized with ketamine hydrochloride (15 mg/kg im) and given atropine sulfate (60 µg/kg im) to reduce salivation and bronchial secretion. Surgical anesthesia was induced with sodium pentobarbitone (15-20 mg/kg iv). Following pharyngeal anesthetization with 4% lignocaine hydrochloride spray, an endotracheal tube was inserted. Anesthesia was maintained throughout the experiment by regular doses of sodium pentobarbitone (diluted in saline to 15 mg/ml) delivered via an intraperitoneal catheter. Hydration was maintained by fluid replacement with isotonic saline through the same catheter at a rate of approximately 2 ml/(kg h). Body temperature was monitored by a rectal thermometer and kept at 37°C with the aid of insulating blankets and a pair of heating pads. Antibiotic cover was provided by amoxycillin (18 mg/kg im) every 6 h. Heart rate, blood pressure, respiration rate, oxygen saturation levels, and end tidal carbon dioxide levels were monitored continuously. In four successive experiments on a monkey, the median nerve was exposed at four sites and single fibers were isolated by microdissection; the first two dissections were in the upper arms and the last two were in the lower arms. At the end of each experiment, the dissection was sutured in layers and the animal was returned to a heated, padded recovery cage following an intramuscular dose of 50 mg/kg benzathine penicillin, 30 mg/kg procaine penicillin, and 19 mg/kg benzylpenicillin. Each experiment lasted a maximum of 18 h and there was a rest period of at least 2 wk between each experiment. During this rest period the monkeys were housed in large cages together with or adjacent to other monkeys and with access to an outdoor exercise area. They were observed closely and regularly by trained personnel and were in good health with no evident signs of pain or distress. Buprenorphine hydrochloride (8 µg/kg) was available for pain relief but was judged to be unnecessary. At the end of the series, the monkeys were in prime condition and showed no signs of sensory or motor deficits. They were returned to a breeding colony.

Receptive field location

Fifty-eight SAIs with receptive field centers on the curved region of the glabrous skin occupying the sides or end of the distal segment of the second, third, or fourth digit were selected for this study. Afferents were rejected if the receptive field center was 1) in close proximity to the nail, 2) close to the distal interphalangeal crease, or 3) on the central, relatively flat portion of the fingerpad where the stimulus was applied.

During the experiment, the location of each receptive field center was established using a series of graded von Frey hairs and was marked accurately on a plaster cast of the monkey's hand. After the experiment, the x, y, and z coordinates of the centers were measured by mounting the cast in a stereotaxic frame. The origin of the coordinate system was located on the dorsal surface of the finger at the junction of the midline and the distal interphalangeal joint (Fig. 1A). To allow pooling of data from both left and right hands, the x coordinates were taken as positive on the radial side and negative on the ulnar side. To pool results from different-sized fingers in different monkeys, the x, y, and z coordinates were normalized by dividing by the width, length, and depth of the distal segment of the finger, respectively. The length of the distal segment is the distance from the interphalangeal crease to the tip, the width is the distance from the ulnar to the radial edge at the interphalangeal crease, and the depth is the greatest distance from the dorsal to the ventral surface of the distal segment.



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Fig. 1. Location of receptive field centers of the 58 afferents. A: orientation of the Cartesian coordinate system used. The origin is located on the dorsal surface in the midline of the finger in line with the distal interphalangeal crease. The point of application of the stimulus (S1) is shown for an afferent with a receptive field center on the side of the finger (R1) and also for two centers on the end of the finger (S2, R2 and S3, R3). B and C: normalized x, y, and z coordinates of the centers shown in two planes viewed from the top of the finger (B) and from the end of the finger (C), respectively. The length, width, and height of the normalized distal phalanx are each one unit. D: a two-dimensional schematic representation of the unfolded glabrous skin. The boundary between the glabrous skin and the hairy skin and between the glabrous skin and the fingernail is shown by the outer solid line. The inner solid line represents the region within which the glabrous skin is relatively flat. The area between the inner solid line and the broken line represents glabrous skin that has some curvature but is still on the "upper face" of the finger. The area between the dotted line and the outer solid line represents glabrous skin that forms the sides or end of the finger. For this representation, the distal segment has a length, width, and depth of 10.5, 7.7, and 8.3 mm, respectively, which are the averages of the monkey fingers used in the present study. Crosses, diamonds, and open circles show centers for afferents with curvature indices (see RESULTS) <5, 5 to 15, and >15, respectively.

Stimulus

Delrin spheres were applied to the fingerpad via a stimulator that was described in detail previously (Goodwin et al. 1995). The monkey's finger was secured by imbedding the dorsal surface in a plasticine mold with the nail glued with cyanoacrylate to a metal insert. The stimulator consisted of a freely moving balanced beam with an adjustable counterweight to set the contact force, which was checked regularly with a laboratory balance (resolution 0.1 g). Spheres were mounted on an indexed rotatable hub on one end of the beam and were positioned 0.5 mm above the skin. When the beam was released by activating a relay, a damper ensured critically damped movement of the beam and the spheres contacted the skin with a velocity of approximately 20 mm/s-1. At contact, the line of action of the force was orthogonal to the plane tangential to the skin at the contact point. The stimulator was mounted on an adjustable x-y stage (0.01 mm resolution), which allowed accurate positioning of the stimulus on the skin. The spheres had curvatures of 0, 80.6, 172, 256, 340, 521, and 694 m-1, which correspond to radii of infinity , 12.4, 5.81, 3.90, 2.94, 1.92, and 1.44 mm, respectively. Contact force was set by the counterweight to 15, 20, 30, or 40 gf (0.147, 0.196, 0.294, or 0.392 N, respectively).

The stimulus was applied to the relatively flat central portion of the fingerpad at a point (of first contact between the sphere and the skin) determined for each afferent as follows. If the receptive field center was on the side of the finger, then the stimulus point was located in the midline of the finger such that a line between the stimulus point and the receptive field center was perpendicular to the longitudinal axis of the finger (S1-R1 in Fig. 1A). If the center of the receptive field was on the end of the finger, then the stimulus point was located in the midline of the finger at the distal end of the central region where the fingerpad was still relatively flat (S2-R2 and S3-R3 in Fig. 1A).

For each afferent, all seven spheres were applied to the fingerpad at three different forces. Depending on the sensitivity of the afferent, the forces used were 15, 20, and 30 gf for some afferents and 20, 30, and 40 gf for the others, to ensure that responses were adequate to classify the unit. The stimuli were presented in a block of 24 trials as follows: 1) at the lowest force, the flat surface was presented twice followed by the remaining six surfaces in order of increasing curvature; 2) the same curvature sequence was presented at the middle force; 3) the same curvature sequence at the highest force. The stimulus contacted the skin for 1.5 s and the interval between trials was 2.5 s. To provide some compensation for stimulus interaction, the response to the first presentation of the flat surface at each force was discarded so that, for all analyzed responses, the stimulus was preceded by a stimulus 2.5 s earlier at the same force. The block of 24 trials was repeated an additional five times and the mean and standard error (n = 6) for each stimulus combination was used in the analysis.

The times of occurrence of action potentials and of the pulse releasing the beam of the stimulator were recorded on a computer with a resolution of 0.1 ms.


    RESULTS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

In the present study, 58 SAIs with receptive field centers distributed over the curved region of glabrous skin on the sides and end of the distal phalanx of the finger were selected. The relative positions of the receptive field centers are shown in two ways. Their three-dimensional coordinates, normalized for finger size, are shown in Fig. 1, B and C. In Fig. 1D, the finger has been unfolded to produce a schematic two-dimensional representation. The locations of the receptive field centers were scattered widely over the sides and end of the finger. Receptive field "sizes" were consistent with those previously reported for the monkey finger; for example, areas of about 11 mm2 when mapped using von Frey hairs with forces at four times threshold (LaMotte and Whitehouse 1986).

The stimulus was applied to the central portion of the fingerpad (the area within the inner solid line in Fig. 1D) at a point on the midline closest to the afferent's receptive field center. The contact area measured with the flat surface at a contact force of 30 gf was <28 mm2 and was considerably smaller for the more curved stimuli. Thus the stimulus contact area was on the flat portion of the finger at a considerable distance from the receptive field center on the side or end of the finger and, for most afferents, was outside the area that would usually be considered as constituting the receptive field. Nevertheless, the afferents responded vigorously and the temporal characteristics of the response showed the same range of static and dynamic components seen in SAIs stimulated at the receptive field center. As a response measure, we used the number of impulses evoked in the first second of response. This is the measure that was used in our previous studies, where the stimulus was applied to receptive fields on the central region of the fingerpad, and that corresponds to our human psychophysics experiments, where the stimulus contacted the skin for 1 s. Twenty-eight of the 58 afferents were sufficiently sensitive so that forces of 15, 20, and 30 gf yielded responses in the range from about 5 to 70 impulses. For the remaining 30 afferents, forces of 20, 30, and 40 gf were used to yield responses in a similar range.

Effect of stimulus curvature on afferent responses

Even though the spheres were applied to the central region of the fingerpad, changing the curvature of the sphere affected the responses of most afferents with receptive fields on the sides or end of the finger. For a few afferents, such as that illustrated in Fig. 2A, responses were insensitive to changes in stimulus curvature at all three contact forces. At the other extreme, for some afferents the response increased with an increase in curvature over the complete range of curvatures (Fig. 2C). Most afferents exhibited some curvature sensitivity lying between these two extremes (Fig. 2B).



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Fig. 2. Effect of stimulus curvature on afferent responses. A-C: responses (mean ± SE, n = 6) of three afferents illustrating the range in curvature sensitivity. The curvature indices K and K2 include and exclude the flat surface, respectively. D and E: histograms showing distributions of the curvature indices among the 58 afferents. Arrows show corresponding values (K = 22 ± 1.8, K2 = 21 ± 2.8; mean ± SD) for afferents with receptive field centers located at the point of stimulus application (from the data of Goodwin et al. 1995). F: scatter plot of the two curvature indices in relation to the 45 degree line. Regression constants are r = 0.861, P < 0.001, slope = 0.952. In A, B, and C, the complete stimulus sequence was presented 6 times, allowing calculation of the mean and standard deviation of each index (n = 6) and thus a t-test of the significance of the difference of the mean from zero. The P values for K and K2, respectively, were 0.084 and 0.019 in A, 0.001 and 0.124 in B, and 0.001 for both in C.

To characterize the range of responses in our sample of afferents, we calculated an index of curvature sensitivity (K) that was independent of the responsiveness of the particular afferent as follows. For each of the three contact forces, the response at each curvature was subtracted from the response at the next highest curvature (i.e., response differences between 80.6 and 0, 172 and 80.6, 256 and 172, 340 and 256, 521 and 340, and 694 and 521 m-1). The mean of these 18 differences reflects curvature sensitivity but is scaled by the responsiveness of the particular afferent. This scaling was eliminated by dividing by the mean response to the 21 stimuli (7 curvatures × 3 contact forces) and the result was multiplied by 100 to obtain a convenient range of numbers.

The distribution of curvature indices is shown by the histogram in Fig. 2D. An index of 0 indicates that the afferent's response was invariant to changes in curvature. A positive index indicates that the response of the afferent increased as curvature increased; the higher the index, the greater the change in response (compare indices in Fig. 2, A-C). A negative curvature index indicates that as curvature increased the response of the afferent decreased.

For some of the intermediate units, the response increased from the flat surface to the sphere with curvature 80.6 m-1, but failed to continue increasing, or even decreased, as the curvature increased further (Fig. 2B). To quantify this effect, a second curvature index (K2) was calculated for the six curvatures from 80.6 to 694 m-1 (i.e., omitting the flat surface), analogous to the first index. Comparison of the distributions of the two indices and their scatter plot in Fig. 2 shows that for some afferents the curvature sensitivity with the flat surface included in the calculation was close to the sensitivity with the flat surface excluded, but for most afferents sensitivity was diminished for curvatures beyond 80.6 m-1 (K2 < K). As expected from the low standard errors in Fig. 2, indices were highly significant except when they were close to zero. For comparison, the two curvature indices were calculated for SAIs with receptive fields on the central portion of the fingerpad, when the spheres were applied to the receptive field center, using the data of Goodwin et al. (1995); these are shown by the arrows in Fig. 2, D and E.

These results show clearly that when a sphere was applied to the central part of the fingerpad, most of the afferents in our sample exhibited responses that increased with increasing curvature of the sphere. However, the range of curvature sensitivity was large and in all but a few cases the afferents were considerably less sensitive to curvature changes than afferents with receptive fields located on the central part of the fingerpad in the region of the stimulus.

The curvature sensitivity of an afferent was not related in any obvious way to the position of its receptive field center on the digit. To illustrate this, the 58 units were divided into three categories; those with small curvature indices (<5), intermediate indices (5-15), and large indices (>15). The location of receptive field centers for the three classes are shown with different symbols in Fig. 1D.

Effect of contact force on afferent responses

Increasing the contact force between the spheres and the fingerpad resulted in an increase in responses for all the SAIs, but there was a range of force sensitivities. Even though the afferent illustrated in Fig. 3A showed substantial increases in response when contact force increased, it is one of the less force-sensitive units in the sample. Most units showed a relatively greater force effect, like the unit shown in Fig. 3B. For each afferent, a force index (F) was calculated to quantify the degree to which a change in contact force changed the afferent's response, irrespective of the responsivity of the particular afferent, as follows. For each of the seven curvatures, the response at the lowest contact force (e.g., 20 gf) was subtracted from the response at the middle contact force (e.g., 30 gf), and the response at the middle contact force (e.g., 30 gf) was subtracted from the response at the highest contact force (e.g., 40 gf). The mean of the 14 differences was divided by the mean response for the 21 stimuli (7 curvatures × 3 contact forces) and multiplied by 100. An index of 0 indicates that there was no change in response when contact force changed. Even though the force range was 15, 20, and 30 gf for some units and 20, 30, and 40 gf for others, in either case the force index indicates the sensitivity of the response to changes in force.



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Fig. 3. Sensitivity of the afferents to changes in contact force. A and B: responses (mean ± SE, n = 6) of two representative units with force sensitivity indices at the lower end of the spectrum (A) and in the middle of the range (B). C: distribution of the index F among the 58 afferents. Arrow shows the corresponding index (F = 19.8 ± 3.5; mean ± SD) for afferents with receptive field centers at the point of stimulation (calculated from the data of Goodwin et al. 1995). In both A and B, a t-test showed that F was significantly different from zero with P 0.001.

The distribution of the force sensitivity index among the 58 afferents is shown by the histogram in Fig. 3C. For units where F > 100, the large index invariably resulted from a large force effect in combination with small responses at the lowest contact force. For comparison, the force sensitivity index for SAIs with receptive field centers at the point of stimulus contact on the central part of the fingerpad was calculated from the data of Goodwin et al. (1995) and is shown by the arrow in Fig. 3C.

These results show that when a sphere is applied to the central part of the fingerpad, the responses of SAIs with receptive fields located on the sides and end of the finger increase with an increase in contact force. Moreover, all the units in our sample were more sensitive to changes in contact force than units (Goodwin et al. 1995) located at the stimulus point.

A plot analogous to Fig. 1D showed that there was no obvious relationship between the location of an afferent's receptive field and its sensitivity to changes in the contact force of a sphere applied to the central portion of the pad.

Afferent sensitivity

For an individual afferent, the changes in response to changes in stimulus curvature or contact force were nonlinear. Thus the effect on the overall population response is complex and depends on the nature of the encoding mechanisms used by the CNS. For example, in some schemes more responsive afferents will contribute more to the population response while in other schemes afferent sensitivity will be compensated for (see DISCUSSION). The scatter plots in Fig. 4 show the relationships among variables in the pool of SAIs. There was no significant relationship between an afferent's curvature index and its sensitivity, measured here by the mean response to all the stimuli used. There was a significant, but minor (R2 = 0.367), trend for less responsive afferents to have a greater sensitivity to changes in contact force. The curvature and force indices of individual afferents showed only a minor dependence (R2 = 0.147).



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Fig. 4. Scatter plots for the 58 SAIs. A: relationship between the curvature index K of each afferent and its mean response to the 21 stimuli used (7 curvatures × 3 contact forces). Regression constants are r = -0.168, P = 0.207. B: relationship between mean response and the force index F. Regression constants are r = -0.606, P 0.001. C: relationship between the curvature index K and the force index F. Regression constants are r = 0.384, P = 0.003.


    DISCUSSION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Receptive fields of SAIs

A number of different methods have been used by investigators to measure the size of SAI receptive fields in primate glabrous skin. Using a glass probe to stimulate the monkey hand, Talbot et al. (1968) described "small, continuous, graded" fields that were smaller on the fingers (approximately 2 mm in diameter) than on the palm (approximately 4 mm in diameter). Their drawings show receptive fields on the sides and end of the finger that are comparable in size to those on the fingerpad. Pubols (1987) also reported that receptive fields on the monkey finger were smaller than those on the palm. In the human hand, Knibestol (1975) and Knibestol and Vallbo (1970) showed that SAIs had small receptive fields with sharp borders. In a rigorous quantitative study in humans, Johansson (1978) mapped the receptive fields of SAIs on the hand using an electromechanically driven probe (0.4 mm in diameter) and showed that they had a central region containing multiple zones of maximum sensitivity outside of which thresholds rose rapidly. A method of measuring receptive field areas using von Frey hairs and producing forces of 4-5 times threshold was introduced by Johansson and Vallbo (1980), who found that the median SAI receptive field size was 11.0 mm2. The receptive field sizes reported in the human studies appeared to be larger than those found in the monkey, but the measurement techniques used were different. LaMotte and Whitehouse (1986) used the same technique as Johansson and Vallbo (1980) and found that SAIs on the monkey distal phalanx had a median area (11.3 mm2) that was indistinguishable from the median value in the human. In a study using an array of closely spaced probes with accurately controlled indentations, Vega-Bermudez and Johnson (1999a,b) avoided the variability introduced by the hand-held stimuli used in most of the above studies and characterized the receptive fields on the monkey fingerpad precisely, reinforcing the above observations. In all of the above studies, the authors acknowledged that a receptive field is defined functionally and that its size varies with the stimulus parameters. However, the sharp rise in threshold at the borders ensures that the receptive field size does not vary much with the amplitude of an indenting probe (Johansson and Vallbo 1980; Vega-Bermudez and Johnson 1999a) and that SAIs are universally thought of as having confined receptive fields.

None of the studies of receptive fields foreshadowed our observation that the geometry of the finger results in a fundamental difference in the nature of receptive fields for skin on the fingers and for relatively flat pieces of skin, such as that on the palm. In our experiments, when the receptive fields of SAIs innervating the sides or end of the finger were plotted with von Frey hairs, they were typical of the small confined fields of SAIs innervating the fingerpad. However, when stimuli were applied to the central part of the fingerpad, the SAIs with remote receptive field centers responded vigorously. The apparent contradiction arises because stimuli on the fingerpad cause clearly visible distortions of the skin on the sides and end of the finger that are within the receptive fields of afferents from these regions. In a previous study, Pubols (1987) observed that when a probe indented a monkey's fingerpad, the skin on the side of the finger initially bulged outward, which he termed "negative indentation," but that the proceeding static component of indentation "became positive." He concluded that the curvature of the finger restricted the spread of positive indentation and thus the size of the receptive fields were smaller than those on the palm.

Although discussion of the definition of a receptive field is in some ways pedantic, it has an important bearing on the way population responses are viewed and on how information relayed by the primary afferent fibers is interpreted. In general, attention has been focused on subpopulations of fibers innervating skin in the region of the stimulus, and responses of afferents with remote receptive fields have not been considered even though, in many circumstances, their contribution may be significant. It is also important to take cognizance of these factors when describing the receptive field properties of classes of afferents or when using these properties to classify afferents. For example, one of the distinguishing characteristics of SAIIs is their sensitivity to remote skin stretch, a property not usually attributed to SAIs (Johansson and Vallbo 1980). Qualitative observation of the SAIs in the present study showed that they were sensitive to lateral movement of skin on the fingerpad (remote skin; see Biomechanics of the finger), which raises two issues. First, as a classification tool, remote skin stretch by itself may not readily distinguish between all SAIs and SAIIs on the sides or end of the finger; however, when combined with other criteria, such as regularity of discharge, response to von Frey hairs, etc., there is probably no ambiguity in the SAI/SAII classification. Second, when speculating on putative roles of SAIIs (Macefield et al. 1996; Westling and Johansson 1987), any hypothesis based on remote skin stretch should also allow for contribution from SAIs innervating regions of the finger remote from the stimulus. The same arguments apply to the other types of mechanoreceptive afferent fibers innervating the sides and end of the finger.

Representation of stimulus features

When an object contacts the fingerpad, the population of SAIs innervating the skin in the region of contact encodes information about the local shape of the stimulus, its position on the skin, and the contact force (Dodson et al. 1998; Goodwin et al. 1995, 1997; Khalsa et al. 1998; Srinivasan and LaMotte 1987; Wheat et al. 1995). A number of studies have shown that the SAIs (and the FAIs) innervating the fingerpad also signal details of the shape of an object stroked across the fingerpad (LaMotte and Srinivasan 1987a,b, 1996; LaMotte et al. 1998). In the experiments reported here, the stimuli consisted of spheres of different curvature contacting the fingerpad skin at different forces. The SAIs innervating the sides and end of the distal segment responded; they constitute a large population (Darian-Smith and Kenins 1980; Johansson and Vallbo 1979), but what features of the stimulus do they represent or encode?

There was a systematic change in the responses of most afferents when the curvature of the sphere changed, but the effect was small, much smaller than the changes occurring in the population of SAIs from the fingerpad in the vicinity of the stimulus. On these grounds it is unlikely that the afferents on the sides and end of the finger make a major contribution to encoding the local shape of objects contacting the fingerpad. In contrast, when contact force increased, the responses of all afferents increased and, for most, the changes were proportionally greater than those occurring in the population of SAIs from the fingerpad itself. Thus it is possible that the afferents from the sides and end of the finger provide the CNS with considerable information about contact force on the fingerpad. This hypothesis is particularly attractive because the SAIs from the fingerpad start showing some saturation at relatively low contact forces (Goodwin et al. 1995). At the higher contact forces common in many everyday manipulations, it is likely that the responses of afferents from the fingerpad would be saturated, but that the response of the population of SAIs from the sides and end of the fingers would continue to grow with increasing contact force. In the present experiments we did not quantify the effects of lateral forces applied to the fingerpad but observed, qualitatively, that the SAIs on the sides and end of the finger did respond to such stimuli. Thus these afferents may also play a role in determining load forces on the digits during manipulations (Westling and Johansson 1987).

The present study is only the first step in characterizing the response properties of afferents from the sides and end of the fingers and is insufficient to establish their role unequivocally. To reach more definite conclusions, it will be necessary to reconstruct realistic responses of the entire population of afferents from the sides and end of the fingers along the lines of reconstructions attempted for the populations on the fingerpad itself (Goodwin and Wheat 1999; Khalsa et al. 1998). In our data there was no obvious relationship between the position of the receptive field on the finger and its response characteristics; a larger sample is needed to clarify this issue. In addition, specific hypotheses need to be tested before the role of these afferents is clearly established. For example, it is not known whether neural codes are based directly on afferent responses, in which case they will be affected by the variation in sensitivity among fibers, or if central synaptic connection strengths are such that all fibers have the same efficacy (that is, their responses are effectively normalized), in which case their sensitivities are irrelevant. Ultimately, population reconstructions must include information from afferents all over the finger, particularly in more complex manipulations that are likely to engage many groups of afferents.

Biomechanics of the finger

The distal segment of the human finger is a complex structure (Tubiana 1981). The phalanx, a rigid bone at the center, is surrounded by viscoelastic material encased in skin. The fingerpad is soft and relatively mobile. During the everyday grasping and manipulating that constitute normal hand function, there is a complex sequence of events. When an object contacts the skin, the fingerpad is at first compliant, conforming to the shape of the object and changing the geometry of the distal segment. But with increasing contact force, the pad becomes increasingly incompressible (Pawluk and Howe 1999). There is also movement of the fingerpad with respect to the phalanx. The result is a widespread distribution of stresses and strains over the distal segment. To elucidate mechanotransduction in the finger, biomechanical models must take these factors into account.

Many models of skin mechanics have been concerned with events in the neighborhood of indenting edges, bars, or gratings, warranting the simplifying assumption of a flat, infinite, homogeneous, isotropic medium (Phillips and Johnson 1981b). In the waterbed model of Srinivasan (1989), the finger was of finite size with curved sides, but the sides were rigid walls. Other models, particularly for robot fingers, have been based on elastic cylinders with a rigid core, but here too the models are concerned with events in the region of the stimulus (Fearing 1990; Srinivasan and Dandekar 1996). While these models have provided invaluable insight into many aspects of skin mechanics, they obviously cannot be used with the present data. There is a need for realistic models of the finger that will explain the distribution of stresses and strains over the entire skin surface in response to tactile stimuli.


    ACKNOWLEDGMENTS

We thank H. Gehring for technical assistance in these experiments.

This work was supported by a grant from the National Health and Medical Research Council of Australia.

Present address of J. W. Bisley: Laboratory of Sensorimotor Research, National Eye Institute, 49 Convent Drive, Building 49, Bethesda, MD 20892-4435.


    FOOTNOTES

Address for reprint requests: A. W. Goodwin (E-mail: a.goodwin{at}anatomy.unimelb.edu.au).

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Received 10 January 2000; accepted in final form 21 March 2000.


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