SA1 and RA Receptive Fields, Response Variability, and Population Responses Mapped with a Probe Array

F. Vega-Bermudez and K. O. Johnson

Department of Neuroscience and Krieger Mind/Brain Institute, Johns Hopkins University, Baltimore, Maryland 21218


    ABSTRACT
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Vega-Bermudez, F. and K. O. Johnson. SA1 and RA receptive fields, response variability, and population responses mapped with a probe array. Twenty-four slowly adapting type 1 (SA1) and 26 rapidly adapting (RA) cutaneous mechanoreceptive afferents in the rhesus monkey were studied with an array of independently controlled, punctate probes that covered an entire fingerpad. Each afferent had a receptive field (RF) on a single fingerpad and was studied at 73 skin sites (50 mm2). The entire array was lowered to 1.6 mm below the point of initial skin contact (the background indentation) before delivering single-probe indentations. SA1 and RA responses differed in several ways. 1) SA1 RF boundaries were affected much less by indentation depth than were RA boundaries, and the SA1 RF areas were much more uniform in size. The mean SA1 RF area grew from 5.1 to 8.8 mm2 as the indentation depth increased from 50 to 500 µm; the mean RA RF area grew from 5.5 to 22.4 mm2 over the same intensity range. 2) SA1 RFs were more elongated than RA RFs. Elongated RFs were oriented in all directions relative to the skin ridges and the finger axis. 3) SA1 impulse rates were linear functions of indentation depth at all probe locations in the RF; RA responses tended toward saturation beginning at 100 µm indentation depth when the probe was over the HS. Similarities between SA1 and RA responses were that 1) both were extremely repeatable with SDs < 1 impulse per trial and 2) both had population responses (number of impulses) that were nearly linear functions of indentation depth. However, SA1s represented increasing indentation depth by increasing impulse rates in a small, relatively constant group of afferents, whereas the RAs represented increasing indentation depth predominantly by the recruitment of new afferents at a distance.


    INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

This paper and a companion paper (Vega-Bermudez and Johnson 1999) report the results of a study of the responses of SA1 (slowly adapting type 1) and RA (rapidly adapting) cutaneous mechanoreceptive afferents to simple and complex spatial patterns of indentation delivered with an array of independently controlled probes that cover the entire fingerpad. The stimulus conditions before indentation simulate placement of a finger on a flat surface with sufficient pressure to flatten the skin surface. This simplifies the relationship between the probes and the skin by creating uniform conditions of preindentation around each probe. In this paper we report the results of indentations with single probes at many locations within each afferent fiber's receptive field (RF), which provide a detailed characterization of the intensive and spatial response properties of SA1 and RA afferent fibers. In the second paper we report the results of stimulation with multiple probes and the effect of background indentation depth on the responses to indentation with single and multiple probes.

SA1 and RA afferent fibers have been studied extensively with single punctate probes (Burgess et al. 1983; Cohen and Vierck 1993; Goodwin et al. 1995; Harrington and Merzenich 1970; Jänig et al. 1968; Knibestöl and Vallbo 1980; Poulos et al. 1984; Pubols and Benkich 1986; Werner and Mountcastle 1965), but with few exceptions (Cohen and Vierck 1993; LaMotte and Whitehouse 1986) studies with carefully controlled indentation have been confined to the hot spot (HS, point of maximum sensitivity). In this paper we report SA1 and RA responses to indentation depths ranging from 50 to 500 µm at 73 points within a large area around the HS. This detailed examination of RF structure allows us to address three important issues.

The first issue concerns the relative sizes of SA1 and RA RFs. The inference that SA1 afferents are primarily responsible for tactile form perception (Johnson and Hsiao 1992) is based partly on their smaller RF areas. However, the literature is not clear on this point. Some studies in both human and monkey have reported that the SA1 RFs are smaller than RA RFs (Blake et al. 1997; Johansson 1979; Johnson and Lamb 1981; Knibestöl 1973, 1975), whereas other studies in both species have reported that they are approximately the same size (Johansson and Vallbo 1980; LaMotte and Whitehouse 1986; Talbot et al. 1968). The second issue concerns the effects of stimulus intensity on the two-dimensional structure of SA1 and RA RFs. Two previous studies have examined RF structure (Cohen and Vierck 1993; Johansson 1978), but neither study addressed the effects of stimulus intensity on the two-dimensional structure of SA1 and RA RFs. The third issue concerns the SA1 and RA population responses to punctate indentation. There is widespread agreement that the subjective intensity produced by punctate indentation is described by a power function with an exponent near one (Greenspan et al. 1984; Harrington and Merzenich 1970; Knibestöl and Vallbo 1980; Mountcastle 1967). However, comparison of psychophysical data with the responses of single primary afferent responses to indentation has produced conflicting results (Knibestöl and Vallbo 1980; Kruger and Kenton 1973; Mountcastle 1967). In this study, we estimate the SA1 and RA population responses to punctate indentation taking into account recruitment at a distance, the variability in sensitivity between afferents, and the variability in response properties between afferents.

In this paper we describe the responses of 24 SA1 and 26 RA afferent fibers to stimuli at 73 locations spread over a 50-mm2 skin region containing each fiber's RF. The data convey the spatial and intensive response properties of SA1 and RA afferents at indentation depths ranging from 50 to 500 µm. We show that SA1 and RA afferent RF areas are approximately equal at threshold and that RA RF areas grow much more rapidly with increasing indentation amplitude than do SA1 RF areas. This accounts for differences between previous reports. We also show that both afferent populations signal indentation depth reliably with a population discharge rate that is approximately proportional to indentation depth. In the SA1 population this results from limited growth in the spread of activity but near-linear growth in the impulse rates of all individual afferents. In the RA population, this results predominantly from growth in the number of active fibers (because of growth in RF area). Both afferent types signal indentation depth with extremely low variability.


    METHODS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Neurophysiological methods

Experiments were performed on anesthetized monkeys (Macaca mulata) weighing between 3.0 and 5.0 kg. Single mechanoreceptive fibers were dissected from the median or ulnar nerves with methods described earlier (Mountcastle et al. 1972). After isolating a fiber suitable for study, its RF was explored manually with von Frey hairs, and a spot at its apparent point of maximum sensitivity was marked with ink. This was not necessarily the true HS, but it was sufficiently close that the entire RF was always well within the area studied. Peripheral afferent fibers were classified as follows: SA1 when its RF had a local region of high sensitivity, and it responded to steady indentation with a sustained response; RA when it responded transiently to sustained indentation and its entrainment threshold at 100 Hz was higher than at 40 Hz; PC (Pacinian) when it responded transiently to sustained indentation and its entrainment threshold at 100 Hz was lower than at 40 Hz. Only fibers with RFs near the centers of the fingerpads were studied.

Stimuli

The stimulator array, developed by the Johns Hopkins Applied Physics Laboratory as a prototype for an array with 400 independently controlled probes, was a hexagonal probe array (see Fig. 1) whose overall diameter was 13 mm. Individual probes were 0.5 mm in diameter and spaced at 1-mm intervals, center to center. All 155 probes were stationary except the central seven probes, which were driven by independent, servo-controlled linear motors (Schneider 1988). Each motor had a rise time of 2 ms, a half-amplitude band-pass of 150 Hz, and was capable of 1,000-µm indentation. The feedback displacement sensor provided a precision of 2 µm. The stationary probes were truncated cones with sides sloped at 60° and tops raised 0.85 mm above the background plate to ensure that the skin did not contact the plate.



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Fig. 1. Stimulus array. Seven active probes driven by linear motors occupy the central, 7 locations of a larger hexagonal array of static probes spaced at 1.0-mm intervals (center to center). Active probes are cylindrical rods, 0.5-mm diam. The passive probes are truncated cones raised 0.85 mm above the background with sides sloped at 60° relative to the base. Active and passive probes are both 0.5 mm in diameter where they contact the skin. The array illustrated here is smaller than the actual array (13 mm diam.).

The array was centered over the RF with a three-axis translation stage with 5-µm resolution in all directions and was oriented so it was tangential to the skin at the HS. It was then lowered onto the skin until the skin was flattened and all probes within 4 mm of the HS (8-mm diam) contacted the skin. The approximate background condition before indentation with individual probes can be visualized by looking through plate glass while pressing a fingerpad onto the opposite side of the glass until the contact region is 8 mm in diameter. The point at which the entire array contacted the skin and the subsequent indentation required to flatten the skin were determined visually with a dissecting microscope. The indentation required to flatten the skin ranged from 1.6 to 2.0 mm for most fibers (n = 42); a few required more (4 required 2.4 mm) or less (4 required 1.2 mm) indentation to flatten the skin. The discharge in SA1 afferents produced by this indentation was (although negligible) subtracted from the response evoked by probe indentation. Whenever the array was moved, testing was delayed for >= 15 s to allow the mechanical response to reach steady state. The array was larger than any fingerpad, and no array placement resulted in contact with the edge of the array.

Each stimulus consisted of indentation with one probe for 200 ms followed by withdrawal for 200 ms, yielding a repetition period of 400 ms. Stimulus events and action potential times were recorded with a resolution of 0.1 ms. The RF of each fiber was mapped at 73 skin sites on a hexagonal grid, 8 mm in diameter, centered on the fiber's HS. The total area covered was 50 mm2. At each of 19 array placements, 175 stimuli were delivered in quasirandom order; these comprised five repetitions of five indentation depths (50, 100, 200, 350, and 500 µm) at each of the seven active probe sites. When applied to human skin, those amplitudes produced sensations that ranged from being barely perceptible to strong. Stimuli were presented in increasing order of amplitude at each array placement to minimize the effects of prior stimuli. The placements were 1) central probe over the HS, 2) central probe over all 6 locations previously occupied by active probes 1 mm from the HS, and 3) central probe over all 12 locations previously occupied by inactive probes 1.7 or 2 mm from the HS. Field maps derived in this way were based on 3,325 stimuli (7 probes × 5 indentation depths × 5 trials per depth × 19 array placements).

Analysis

RF area was computed with a 10% rule for consistency with previous studies of RF area (Blake et al. 1997; Johnson and Lamb 1981; Phillips et al. 1992): RF area at each indentation amplitude was defined as the number of probe positions where the response exceeded 10% of the response at the most sensitive location (the HS) at that same indentation amplitude divided by the probe density (1.15 probes/mm2). All statistical analyses were done with SPSS for Windows 8.0 (Chicago).


    RESULTS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

RF maps were obtained from 24 SA1 and 26 RA afferents with RFs on the distal fingerpads. All were studied at 73 RF locations with at least two indentation depths at 200 and 500 µm. Twelve SA1 and 13 RA afferents were studied more extensively with five indentation depths ranging from 50 to 500 µm. Background indentation with the entire array produced a small ongoing impulse rate in some SA1 afferents that exceeded 1 impulse/s in only 6 of 24 afferents (mean 0.81 impulses/s, maximum 3.05 impulses/s).

RFs obtained with 500-µm pulses are shown in Figs. 2 and 3. The HS was often not at the RF center, and the loss of responsiveness away from the HS was often abrupt, particularly in SA1 afferents. At the sampling resolution used in this study, 1 mm, the RFs were, with few exceptions, unimodal. SA1 fields with more than one response peak are SA10 and SA12 (Fig. 2). RA fields with more than one response peak are RA06, RA11, RA14, RA16, RA17, and RA23 (Fig. 3). Rarely, the fields were neither circular nor ellipsoidal (e.g., SA10 in Fig. 2 and RA17 in Fig. 3).



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Fig. 2. Receptive fields (RFs) of 24 slowly adapting type 1 (SA1) fibers mapped with 500-µm stimulus pulses. The large open circles represent the skin areas sampled at 73 points on a hexagonal grid (8-mm diam, 50 mm2). Points in the grid were separated by 1 mm. Area of each  represents impulse rate evoked at that point normalized by impulse rate evoked at the hot spot (HS). In monkeys, unlike humans, skin ridges run parallel to the proximal-distal axis of the finger. All maps are displayed with the skin ridges oriented from left to right. Lower right: photograph of a monkey distal phalanx in the same orientation as the RF maps.



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Fig. 3. RFs of 26 rapidly adapting (RA) fibers mapped with 500-µm stimulus pulses. Details are the same as in Fig. 2.

All the RFs were analyzed for elongation and orientation by fitting a two-dimensional Gaussian function to each RF map and extracting the ellipse corresponding to 1 SD. The SA1 RFs were significantly more elongated than the RA RFs as measured by the ratios of the major to minor axes of the best fitting ellipses (Kolmogorov-Smirnov, P = 0.017). Most SA1 RFs (71%, 17/24) had aspect ratios >1.5, and 17% (4/24) had aspect ratios >2.0 (SA01, SA05, SA14, and SA20 in Fig. 2). RA RFs, in contrast, were more uniformly circular; 73% (19/26) had aspect ratios <1.5, and all had aspect ratios <2.0. RFs with aspect ratios large enough to make a meaningful measure of orientation (aspect ratio >1.5) were oriented in all directions relative to the finger axis and displayed no statistically significant difference from a uniform distribution of orientations (P > 0.05). Because the skin ridges in the rhesus monkey run in a proximal-to-distal direction there was also no relationship between RF orientation and ridge orientation.

Effects of indentation depth

SA1 and RA afferents responded to stimuli with increasing amplitude differently. Typical examples of RF maps produced by 100- and 500-µm indentations are shown in Fig. 4. These examples illustrate the general finding that, although the RF areas of both SA1 and RA fiber types were affected by indentation depth, the growth of RF area was much greater in RA than in SA1 afferents (P < 0.0001, 2-way ANOVA). The growth of RF area for 13 RA and 12 SA1 afferents studied at five amplitudes is shown in Fig. 5. Mean SA1 RF area grew from 5.1 to 8.8 mm2 as the indentation depth increased from 50 to 500 µm, whereas the mean RA RF area quadrupled from 5.5 to 22.4 mm2. Variation in RF size also differed significantly between afferent types. The RA RF SD grew from 3.60 to 8.17 mm2 as the indentation depth increased from 50 to 500 µm. The SA1 RF SD, in contrast, dropped from 2.02 to 1.26 mm2. Close inspection of the SA1 data in Fig. 5 shows that this drop in RF variability occurred because the growth in mean receptive area was mainly caused by growth in the smaller RFs.



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Fig. 4. RF maps of 3 typical SA1 and 3 typical RA afferents at 2 indentation depths. Top panel: 3 typical SA1 RFs. Bottom panel: 3 typical RA RFs. Top row in each panel: RF maps obtained with indentation depths of 500 µm; bottom row in each panel: with 100 µm. Area of each  is proportional to the mean impulse rate evoked by the stimulus at that location relative to the rate evoked by the 500-µm stimulus at the HS (displayed above each pair of RFs). RA impulse rates are lower because the RA afferents responded only during the transient phase of the 200-ms indentation period.



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Fig. 5. RF area vs. indentation depth. RF area at each indentation depth was determined by counting the number of RF sites yielding a response >= 10% of the peak response at that indentation depth (Johnson and Lamb 1981) and dividing by the RF sampling density (1.15 sample points/mm2). The indentation depth was the probe depth below the background depth for the entire stimulus array. A: RF areas for 13 RA (---) and 12 SA1 fibers (- - - ). B: average RF areas for RA () and SA1 () afferents. Error bar represents 1 SE.

The relationships between impulse rate and indentation depth at all 73 sites in the RFs of 8 typical SA1 and RA afferents are displayed in Figs. 6 and 7. SA1 intensity functions at all RF locations were quite linear. The small number of intensity functions in each panel of Fig. 6 (9-13 out of a possible 73 intensity functions) reflects the small number of sites where any response was elicited in SA1 RFs. RA intensity functions (Fig. 7), in contrast, were predominantly nonlinear when stimulated at or near the HS. The large number of intensity functions in each panel of Fig. 7 (20-36) reflects the large number of RF sites that responded to 500-µm indentation.



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Fig. 6. Intensity functions for 8 SA1 fibers at all RF locations. Ordinate of each graph represents the response (mean impulse rate during 200-ms indentation period) normalized with respect to the response to the 500-µm indentation at the HS. Average impulse rate evoked by the 500-µm indentation at the HS is displayed at the top left-hand corner of each graph. Full range of stimuli (50- to 500-µm indentation depth) was delivered at 73 skin sites around the HS. Intensity function at each site was included if the response at any amplitude was >= 10% of the response to the 500-µm indentation at the HS. All lines other than the line ending at 1.0 at 500 µm represent intensity functions with the indenting probe >= 1.0 mm from the HS. The small number of SA1 intensity functions with intercepts >100 µm illustrates the relative lack of SA1 RF growth when the indentation depth is >100 µm. Eight typical SA afferents are shown for symmetry with Fig. 7, where 8 RA afferents are shown.



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Fig. 7. Intensity function for 8 RA fibers at all RF locations. Details as in Fig. 6. The large number of RA intensity functions with intercepts >100 µm illustrates the progressive growth RA RF area when the indentation depth is >100 µm. Eight RA afferents are shown because their RF properties were quite variable; the 8 shown in this figure are representative of the entire sample of RA afferents.

Average SA1 and RA intensity functions at different distances from the HS are plotted in Fig. 8, which shows that the slope of the intensity function decreases with increasing distance. The tendency toward linearity among SA1 afferents and saturation (negative curvature) in the responses of individual RA afferent intensity functions is evident in the mean intensity functions illustrated in Fig. 8. The slope of the mean RA intensity function at the HS declines more than 2:1 (from 88 to 37 impulses s-1 mm-1) in the interval from 100-200 µm compared with the slope in the interval from 50-100 µm; in contrast, the comparable SA1 slopes are unchanged (318 and 316 impulses s-1 mm-1, respectively). The same pattern of RA saturation is evident in the individual RA afferents illustrated in Fig. 7.



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Fig. 8. Impulse rate vs. indentation depth at varying distances from the HS. Top graph: averages for 12 SA1 afferents at the HS and at distances of 1.0, 2.0, and 3.0 mm from the HS. Error bars show the SE at each point. Bottom graph: averages for 13 RAS. The large difference in mean firing rates between SA1 and RA afferents is explained partially by the transient nature of the RA response, which falls silent before the end of the 200-ms stimulus period used to calculate mean rate. Differences in peak rates were smaller than the differences in mean rates illustrated in Fig. 8. Average SA1 peak discharge rate evoked by the 500-µm indentation at the HS was 191 impulses/s; the comparable mean RA peak rate was 72 impulses/s.

It is evident in Fig. 8 that the effective stimulus intensity declines rapidly as the stimulus point moves away from the HS. The data in Fig. 8 are replotted in Fig. 9 to show the mean attenuation in stimulus strength with distance. If the lines between the points are used to estimate the responses at probe placements at nonintegral distances from the HS, it can be estimated that the SA1 and RA responses fall to approximately one-half their peak values when the HSs are 0.75 and 1.30 mm the probe. From this, it can be seen that the RA population response exceeding one-half its peak value spreads over an area approximately three times [(1.3/0.75)2] the comparable SA1 area. The relative spread of the two population responses depends, of course, on the indentation depth because the SA1 and RA RF areas grow at different rates with increasing depth.



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Fig. 9. Mean response vs. distance from the HS. Mean responses at 1.0, 2.0, 3.0 and 4.0 mm from the HS were obtained from the contour plots in Fig. 10. Indentation depth is shown above each curve.

Population response

The responses of individual afferents to stimuli at and away from the HS were used to infer the properties of the population response evoked by single stimuli. Average RF maps are illustrated in Fig. 10, with contours set at increments of 12 impulses/s for the SA1 maps and 2 impulses/s for the RA maps. By using Mountcastle and Powell's (1959) reciprocal interpretation of RF maps, these average spatial maps serve as estimates of the population responses to single stimuli at 50-, 100-, 200-, 350-, and 500-µm indentation. An interesting aspect of these population response maps is that they are nearly circular, although many afferents, particularly SA1s, have eccentric RFs (i.e., elongated RFs with the HS displaced from the center). This is because the elongated RFs have orientations in all directions.



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Fig. 10. Average RF maps at indentation depths ranging from 50 to 500 µm. Horizontal axis in the figure corresponds to the proximal-distal axis of the finger. Average maps were obtained by aligning the (12 SA1 and 13 RA) individual RFs at their points of maximum sensitivity. Mean peak discharge rate at the HS is shown above and to the right of each contour plot. SA1 contours are at increments of 12 impulses/s; RA contours at 2 impulses/s.

The number of active fibers, mean impulse rate per fiber, and the total population firing rates are displayed in Fig. 11. The total SA1 and RA impulse rates were both fitted by power functions with exponents slightly less than 1.0, but neither was significantly different from 1.0 (P > 0.05, nonlinear regression, R2 = 0.998 for both SA1 and RA data; the SA1 exponent was 0.87, and the RA exponent was 0.81). However, this occurred in distinctly different ways in the two populations. In the SA1 population, proportionality between population impulse rate and indentation depth was due almost entirely to near-linear growth in impulse rates in individual afferents (Figs. 6 and 8). In the RA population, proportionality between population impulse rate and indentation depth was due mainly to growth in the number of active fibers.



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Fig. 11. Estimated SA1 and RA number of active fibers, mean impulse rate, and population firing rates vs. probe indentation depth. The numbers of active SA1 and RA fibers at each stimulus intensity (bottom graph) were estimated with the reciprocal interpretation of the RF studies (Mountcastle and Powell 1959). If RF properties were uniform across each population the RF areas of individual SA1s or RAS at each indentation depth would also be the skin areas over which afferents are activated. Then the total number of afferents activated would equal this area times the local innervation density (1.55 RA afferents and 1.17 SA1 afferents/mm2 at the rhesus fingerpad) (Darian-Smith and Kenins 1980). Because the RF properties are not uniform (Fig. 5) we use the mean SA1 and RA RF areas at each indentation depth to estimate the number of active fibers. Mean impulse rate (middle graph) over all active fibers (fibers with rates >= 10% of HS rate) at each indentation depth was estimated in a similar way. First, the mean rate that would have resulted if the RF properties were uniform was calculated for each afferent as the mean rate at all stimulus sites within its RF where the impulse rate exceeded 10% of the rate at the HS. The mean over all active fibers was estimated as the mean across all afferents of a single type (SA1 or RA). The total population impulse rate (top graph) was estimated as the product of the number of active fibers (bottom graph) times the mean impulse rate over all active fibers (middle graph).

Response variability

A remarkable quality of SA1 and RA responses to indentation, first reported by Werner and Mountcastle (1965, 1968), is their extreme repeatability. The SDs of the responses of 12 SA1 and 13 RA afferents to stimuli at all amplitudes and distances from the HS are illustrated in Fig. 12. Multiple regression analysis showed that there was no statistically significant dependence on stimulus amplitude or distance from the HS when impulse rate was controlled (included as an explanatory variable). The relationship between impulse count variability and mean impulse count was significant for both SA1 and RA afferents (log-log linear regression, P < 0.001), but the trend was slight.



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Fig. 12. Response variability in 12 SA1 and 13 RA afferents. Each datum (343 SA1 data, 363 RA data) represents the mean impulse count and its SD at 1 stimulus amplitude and 1 location within a RF. Stimuli at 1 amplitude and 1 location were presented in blocks of 5; the first response was discarded to eliminate effects, if any, of prior stimuli at a different intensity. Data points are drawn from responses to 50-, 100-, 200-, 350-, and 500 µm indentations at locations including the HS and sites 1, 2, and 3 mm from the HS. In many cases, but particularly in the RA responses, all responses at 1 RF location and indentation depth yielded the same impulse count, and the SD was 0 (whose log value is undefined); those values are displayed in the zone between 0.1 and 0.13.


    DISCUSSION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

The main result reported here is that SA1 and RA afferents respond very differently to indentation with a punctate probe. SA1 afferents have RFs with stiff boundaries that change much less as indentation depth increases than do RA RF boundaries. A tenfold increase in indentation depth from 50 to 500 µm produced a 70% increase in SA1 RF area, which corresponds to a 30% increase in the linear RF dimensions. Also, SA1 RF areas became more uniform as indentation depth increased; the areal SD dropped from 2.0 to 1.3 mm2, and the coefficient of variation dropped from 0.4 to 0.14. The RA afferents responded very differently to increasing indentation depth. The same tenfold increase in indentation depth produced a 300% increase in the mean RA receptive area, which corresponds to a doubling of the linear dimensions, and the areal SD increased from 3.6 to 8.2 mm2. Also, RA afferent responses begin to saturate at small indentation depths, whereas the SA1 responses are linear. At indentation depths of around 100 µm the RA intensity function slope declines by more than 2:1 when the probe is on the HS and the indentation depth doubles.

Despite the differences in RF properties, both afferent populations signaled indentation depth reliably with a population discharge rate that was approximately proportional to indentation depth. In the SA1 population this resulted from limited growth in the spread of activity (number of active fibers) but near-linear growth in the impulse rates of individual afferents. In the RA population this resulted from limited growth in the impulse rates of individual afferents but near-linear growth in the number of active fibers (i.e., growth in RF area).

In the remainder of the paper we discuss three things. First, we take this opportunity to review and resolve the differences in reported RF areas between studies. We conclude that the variation is entirely determined by differences in the stimuli used and that the results reported here are consistent with the literature. We then discuss an old controversy concerning the linkage between primary afferent responses and subjective magnitude estimates. Finally, we comment on the remarkably small SA1 and RA response variability.

RF area

The literature on RF areas in primate glabrous skin contains results that are highly variable, with reported RF areas on the fingerpads ranging from <4 mm2 for both SA1 and RA afferents (Talbot et al. 1968) to means of 20 (SA1) and 40 (RA) mm2 (Knibestöl 1973, 1975). The differences between studies result from the sensitivity of these afferents (Johansson and Vallbo 1980; Talbot et al. 1968), the dependence of RF area on stimulus intensity (Cohen and Vierck 1993; Johansson 1979; LaMotte and Whitehouse 1986), stimulus velocity (Cohen and Vierck 1993; Pubols 1987), the nature of the stimulus (Johansson and Vallbo 1980; Johnson 1974; Johnson and Lamb 1981; Knibestöl 1973; Phillips et al. 1992; Talbot et al. 1968), and the criteria for defining RF boundaries. When these factors are taken into account, the data are consistent with the data from the present study (Fig. 5); that is, the data are uniform in suggesting that SA1 and RA RF areas are similar at threshold, that RA RF areas grow more rapidly than SA1 areas, and that suprathreshold RA RF areas are more variable. The data also suggest that there is no substantial difference between human and monkey RF areas at the fingerpad.

The most variable areal data are those related to hand-held stimuli. Studies that appear to have taken the greatest care to map RFs at amplitudes close to threshold (Johansson 1978; Talbot et al. 1968) report small RF areas of 3-5 mm2. However, when suprathreshold, hand-held stimuli are used, results differ greatly between studies. Johansson and Vallbo (1980) used von Frey hairs and reported that SA1 and RA RFs areas (11.0 and 12.6 mm2, respectively) in humans are nearly identical at forces that are four to five times threshold, but the SA1 stimuli in their study were more than twice as intense as the RA stimuli because the SA1 von Frey thresholds were more than twice as high as the RA thresholds. LaMotte and Whitehouse (1986) obtained a nearly identical result in the monkey with stimuli at 4.5 times threshold. Knibestöl (1973, 1975) reported RF areas severalfold larger with hand-held probes, as noted previously.

No matter how carefully hand-held stimuli are applied, there is a fundamental problem related to differences in velocity sensitivity between SA1 and RA afferents. Both afferent types are sensitive to velocity, but studies employing ramp indentation (Pubols and Pubols 1976) and vibratory stimuli (Freeman and Johnson 1982; Talbot et al. 1968) show that RA afferents are more sensitive to motion than are SA1 afferents and that RA receptors are close to being pure velocity sensors (Freeman and Johnson 1982). Consequently, their RF areas are determined primarily, if not wholly, by the velocity with which a probe is applied (Cohen and Vierck 1993). However, to apply a probe at a precise location manually, it needs to be applied slowly, and the slower the application the smaller is the RA field compared with the SA1 field. Factors such as this probably account for the large variation between studies when hand-held probes are used.

When controlled suprathreshold stimuli are used, RA areas are invariably larger and more variable than SA1 RF areas when compared at the same indentation depths. The study most like the one reported here is by Johansson (1978, 1979), who mapped human SA1 and RA RFs carefully with a linear motor mounted on a translation stage. Johansson's (1979) curves of RF area versus indentation depth are similar to the data plotted in Fig. 5; the suprathreshold RA RF areas grow approximately two times faster than SA1 areas, the areas are approximately two times larger, and they are approximately twice as variable.

Although Johansson's (1979) curves of RF area versus indentation depth are similar in form to those plotted in Fig. 5, the areas are approximately twice as large at similar indentation depths, with median SA1 and RA RFs of ~16 and 40 mm2 at an indentation of 500 µm (vs. 9 and 22 mm2 in this study). A difference in stimulus conditions that may account for this difference in areas is that the skin around Johansson's probe was unconstrained, whereas the skin in the present study was constrained by the entire array of probes, which can make a difference to the deformation patterns in the surrounding skin. A study of monkey afferent responses to a punctate probe where the skin was unconstrained (Cohen and Vierck 1993) reported SA1 and RA RFs areas averaging 38 and 64 mm2 when a 0.04 N stimulus was applied at 1 N/s. The corresponding indentation depth is uncertain.

Stimulus conditions similar to those in this study are provided by studies in humans and monkeys with scanned, raised dots on a flat surface (Blake et al. 1997; Johnson and Lamb 1981; Phillips et al. 1992). The RF areas reported in those studies are similar to each other and to the results presented here. All three studies used identical scanning velocities and methods of measuring RF area. Dot heights were identical in two studies at 0.5 mm (Blake et al. 1997; Phillips et al. 1992), and the dot diameters were small (<= 0.7-mm diam) compared with the RF areas they were probing. The mean human SA1 and RA RF areas averaged 4.8 and 6.1 mm2 (Phillips et al. 1992). The mean monkey SA1 and RA RF areas averaged 4.5 and 11.6 mm2 in one study (Johnson and Lamb 1981) and 5.9 and 10.7 mm2 in the other (Blake et al. 1997). The discrepancy in these studies, if any, is that the human RA RF areas were smaller than the monkey RA areas.

The available data suggest that there is no substantial difference between RF areas in monkeys and humans and that SA1 RF boundaries are more rigid than RA boundaries. Data from both species show that SA1 and RA RF areas are similar at threshold and that RA RF areas grow more rapidly with increasing indentation and are more variable than SA1 areas. The differences between studies are, we believe, accounted for by differences in SA1 and RA response properties and differences in methods, stimuli, and criteria for defining RF area.

Population response

There is universal agreement that, when a punctate probe indents the skin rapidly, the subjective magnitude is linearly related to the indentation depth (Greenspan et al. 1984; Harrington and Merzenich 1970; Knibestöl and Vallbo 1980; Mountcastle 1967). However, reports of the relationship between single afferent responses and indentation depth have varied between laboratories (Knibestöl and Vallbo 1980; Mountcastle et al. 1966; Pubols and Pubols 1976), and therefore the assertion of linearity between the responses of primary afferent responses and magnitude estimation (Mountcastle 1967) has been disputed. The data presented in this paper are uniform in showing that the responses of single SA1 afferents on the fingerpad are linearly related to probe indentation depth. However, it is clear that magnitude estimates must depend on the population response to indentation, not on the responses of any single neuron. The population response need not correspond to the responses of individual afferents as is made clear by comparing the responses of individual RA afferents and the RA population response (Figs. 7 and 11). The estimates of SA1 and RA population impulse rates and total numbers of active units presented in this paper are linear or near-linear functions of indentation depth. If we presume that subjective magnitude depends on either the total impulse rate or the total number of active fibers (in either the SA1 or RA populations) then the hypothesis of linearity between subjective magnitude and the neural code on which it is based is supported (Johnson et al. 1996; Mountcastle 1967).

Response variability

The trial-to-trial variability in the SA1 and RA neural responses was very low (cf. Wheat et al. 1995), was independent of stimulus location and indentation depth, and depended only on the response magnitude. Werner and Mountcastle (1965) reported similar results for SA afferent responses in the hairy skin of the cat and monkey; they attributed the low variability to the fact that they used long sequences of identical stimuli (30-50 stimuli) at intervals of 3-5 s, thus avoiding interactions between successive responses. In the present study stimuli were delivered rapidly at many different RF locations and many different amplitudes (50-500 µm) in quasirandom order. Werner and Mountcastle also showed that the interspike interval variability was proportional to the mean interval (with a coefficient of variation of 0.14). If the response was a renewal process (spike intervals are independent) (Cox 1962), the variability of the impulse count would have risen as the square root of the number of impulses (slope of 0.5 in the log-log plot shown in Fig. 9). In fact, it rose at a lower rate, implying that the response variability was lower than would be predicted by the low interspike interval variability reported by Werner and Mountcastle. Levine (1980) has reported the same discrepancy in the firing statistics of retinal ganglion cells.


    ACKNOWLEDGMENTS

We thank S. Hsiao, H. Dong, and W. Schneider for assistance.

This work was supported by National Institute of Neurological Disorders and Stroke Grant NS-18787 and by the W. M. Keck Foundation.


    FOOTNOTES

Address for reprint requests: K. Johnson, 338 Krieger Hall, Johns Hopkins University, 3400 N. Charles St., Baltimore, MD 21218.

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 25 June 1998; accepted in final form 22 February 1999.


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