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
Vega-Bermudez, F. and K. O. Johnson. SA1 and RA receptive
fields, response variability, and population responses mapped with a
probe array. J. Neurophysiol. 81: 27012710, 1999. 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 mm; 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 mm
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

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 fibers 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 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.

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; Janig et al. 1968; Knibestol 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 mm
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;
Knibestol 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; Knibestol and Vallbo 1980;
Mountcastle 1967). However, comparison of psychophysical
data with the responses of single primary afferent responses to
indentation has produced conflicting results (Knibestol 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 fibers RF. The data convey the
spatial and intensive response properties of SA1 and RA af-

0022-3077/99 $5.00 Copyright 1999 The American Physiological Society

2701

2702

F. VEGA-BERMUDEZ AND K. O. JOHNSON

ferents at indentation depths ranging from 50 to 500 mm. 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

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-mm indentation. The feedback

displacement sensor provided a precision of 2 mm. 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.
The array was centered over the RF with a three-axis translation
stage with 5-mm 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 5 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 fibers 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 mm)
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 3 5
indentation depths 3 5 trials per depth 3 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

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.).

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
mm. Twelve SA1 and 13 RA afferents were studied more
extensively with five indentation depths ranging from 50 to 500
mm. 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-mm pulses are shown in Figs. 2 and
3. The HS was often not at the RF center, and the loss of

SA1 AND RA RECEPTIVE FIELDS MAPPED WITH A PROBE ARRAY

2703

FIG. 2. Receptive fields (RFs) of 24

slowly adapting type 1 (SA1) fibers mapped
with 500-mm 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 F 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.

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).
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 5 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-mm indentations are shown in Fig. 4. These
examples illustrate the general finding that, although the RF

FIG. 3. RFs of 26 rapidly adapting (RA) fibers

mapped with 500-mm stimulus pulses. Details are
the same as in Fig. 2.

2704

F. VEGA-BERMUDEZ AND K. O. JOHNSON

intensity functions in each panel of Fig. 7 (20 36) reflects the

large number of RF sites that responded to 500-mm indentation.
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 s21 mm21) in the interval from 100 200 mm
compared with the slope in the interval from 50 100 mm; in
contrast, the comparable SA1 slopes are unchanged (318
and 316 impulses s21 mm21, respectively). The same pattern of RA saturation is evident in the individual RA afferents illustrated in Fig. 7.
It is evident in Fig. 8 that the effective stimulus intensity

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 mm;
bottom row in each panel: with 100 mm. Area of each F is proportional to the
mean impulse rate evoked by the stimulus at that location relative to the rate
evoked by the 500-mm 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.

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 mm, 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 mm.
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.
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

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 (F) and SA1 (M) afferents. Error bar represents 1 SE.

SA1 AND RA RECEPTIVE FIELDS MAPPED WITH A PROBE ARRAY

2705

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-mm indentation at the HS. Average
impulse rate evoked by the 500-mm indentation at the HS is displayed at the top left-hand corner of each graph. Full range of stimuli
(50- to 500-mm 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-mm indentation at the HS. All lines other than the line ending at
1.0 at 500 mm represent intensity functions with the indenting probe $1.0 mm from the HS. The small number of SA1 intensity
functions with intercepts .100 mm illustrates the relative lack of SA1 RF growth when the indentation depth is .100 mm. Eight
typical SA afferents are shown for symmetry with Fig. 7, where 8 RA afferents are shown.

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.

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 mm illustrates the progressive growth RA RF area when the indentation depth is .100 mm. 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.

2706

F. VEGA-BERMUDEZ AND K. O. JOHNSON

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 5 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.
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 sig-

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-mm indentation at the HS was 191 impulses/s; the comparable mean RA peak rate was 72 impulses/s.

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 Powells (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-mm 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.
The number of active fibers, mean impulse rate per fiber, and

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.

SA1 AND RA RECEPTIVE FIELDS MAPPED WITH A PROBE ARRAY

2707

FIG. 10. Average RF maps at indentation depths ranging from 50 to 500 mm. 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.

nificant 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 (loglog linear regression, P , 0.001), but
the trend was slight.
DISCUSSION

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 mm
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 mm 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 (Knibestol 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;
Knibestol 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 35 mm2. However, when suprathreshold, hand-held stimuli are used, results

2708

F. VEGA-BERMUDEZ AND K. O. JOHNSON

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. Knibestol (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. Johanssons (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 Johanssons (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 mm (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 Johanssons 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
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).

SA1 AND RA RECEPTIVE FIELDS MAPPED WITH A PROBE ARRAY

2709

ference 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

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 mm 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.

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 dif-

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; Knibestol and Vallbo 1980;
Mountcastle 1967). However, reports of the relationship between single afferent responses and indentation depth have
varied between laboratories (Knibestol 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 35 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 mm) 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 loglog 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

2710

F. VEGA-BERMUDEZ AND K. O. JOHNSON

Mountcastle. Levine (1980) has reported the same discrepancy

in the firing statistics of retinal ganglion cells.
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.
Address for reprint requests: K. Johnson, 338 Krieger Hall, Johns Hopkins
University, 3400 N. Charles St., Baltimore, MD 21218.
Received 25 June 1998; accepted in final form 22 February 1999.
REFERENCES
BLAKE, D. T., HSIAO, S. S., AND JOHNSON, K. O. Monkey cutaneous SAI and
RA responses to raised and depressed scanned patterns: effects of width,
height, orientation, and a raised surround. J. Neurophysiol. 78: 25032517,
1997.
BURGESS, P. R., MEI, J., TUCKETT, R. P., HORCH, K. W., BALLINGER, C. M., AND
POULOS, D. A. The neural signal for skin indentation depth. I. Changing
indentations. J. Neurosci. 3: 15721585, 1983.
COHEN, R. H. AND VIERCK, C. J. Population estimates for responses of cutaneous mechanoreceptors to a vertically indenting probe on the glabrous skin
of monkeys. Exp. Brain Res. 94: 105119, 1993.
COX, D. R. Renewal Theory. London: Methuen, 1962.
DARIAN-SMITH, I. AND KENINS, P. Innervation density of mechanoreceptive
fibers supplying glabrous skin of the monkeys index finger. J. Physiol.
(Lond.) 309: 147155, 1980.
FREEMAN, A. W. AND JOHNSON, K. O. A model accounting for effects of
vibratory amplitude on responses of cutaneous mechanoreceptors in macaque monkey. J. Physiol. (Lond.) 323: 43 64, 1982.
GOODWIN, A. W., BROWNING, A. S., AND WHEAT, H. E. Representation of
curved surfaces in responses of mechanoreceptive afferent fibers innervating
the monkeys fingerpad. J. Neurosci. 15: 798 810, 1995.
GREENSPAN, J. D., KENSHALO, D. R., SR., AND HENDERSON, R. The influence of
rate of skin indentation on threshold and suprathreshold tactile sensations.
Somatosens. Mot. Res. 1: 379 393, 1984.
HARRINGTON, T. L. AND MERZENICH, M. M. Neural coding in the sense of
touch: human sensations of skin indentation compared with the responses of
slowly adapting mechanoreceptive afferents innervating the hairy skin of
monkeys. Exp. Brain Res. 10: 251264, 1970.
, W., SCHMIDT, R. F., AND ZIMMERMANN, M. Single unit responses and the
JANIG
total afferent outflow from the cats foot pad upon mechanical stimulation.
Exp. Brain Res. 6: 100 115, 1968.
JOHANSSON, R. S. Tactile sensibility in the human hand: receptive field characteristics of mechanoreceptive units in the glabrous skin area. J. Physiol.
(Lond.) 281: 101123, 1978.
JOHANSSON, R. S. Tactile afferent units with small and well demarcated
receptive fields in the glabrous skin area of the human hand. In: Sensory
Function of the Skin in Humans, edited by D. R. Kenshalo. New York:
Plenum, 1979, p. 129 145.
JOHANSSON, R. S. AND VALLBO, . B. Spatial properties of the population of
mechanoreceptive units in the glabrous skin of the human hand. Brain Res.
184: 353366, 1980.
JOHNSON, K. O. Reconstruction of population response to a vibratory stimulus
in quickly adapting mechanoreceptive afferent fiber population innervating
glabrous skin of the monkey. J. Neurophysiol. 37: 48 72, 1974.
JOHNSON, K. O. AND HSIAO, S. S. Neural mechanisms of tactual form and
texture perception. Annu. Rev. Neurosci. 15: 227250, 1992.
JOHNSON, K. O., HSIAO, S. S., AND BLAKE, D. T. Linearity as the basic law of
psychophysics: evidence from studies of the neural mechanisms of roughness magnitude estimation. In: Somesthesis and the Neurobiology of the
Somatosensory Cortex, edited by O. Franzen, R. S. Johansson, and L.
Terenius. Basel: Birkhauser, 1996, p. 213228.
JOHNSON, K. O. AND LAMB, G. D. Neural mechanisms of spatial tactile
discrimination: neural patterns evoked by Braille-like dot patterns in the
monkey. J. Physiol. (Lond.) 310: 117144, 1981.

, M. Stimulus-response functions of rapidly adapting mechanoreceptors

KNIBESTOL
in the human glabrous skin area. J. Physiol. (Lond.) 232: 427 452, 1973.
, M. Stimulus-response functions of slowly adapting mechanoreKNIBESTOL
ceptors in the human glabrous skin area. J. Physiol. (Lond.) 245: 63 80,
1975.
, M. AND VALLBO, . B. Intensity of sensation related to activity of
KNIBESTOL
slowly adapting mechanoreceptive units in the human hand. J. Physiol.
(Lond.) 300: 251267, 1980.
KRUGER, L. M. AND KENTON, B. Quantitative neural and psychophysical data
for cutaneous mechanoreceptor function. Brain Res. 49: 124, 1973.
LAMOTTE, R. H. AND WHITEHOUSE, J. M. Tactile detection of a dot on a smooth
surface: peripheral neural events. J. Neurophysiol. 56: 1109 1128, 1986.
LEVINE, M. W. Firing rate of a retinal neuron are not predictable from
interspike interval statistics. Biophys. J. 30: 9 25, 1980.
MOUNTCASTLE, V. B. The problem of sensing and the neural coding of sensory
events. In: The Neurosciences: An Intensive Study Program, edited by F. O.
Schmitt, G. Quarton, and T. Melnuchuk. New York: Rockefeller Institute
Press, 1967, p. 393 408.
MOUNTCASTLE, V. B., LAMOTTE, R. H., AND CARLI, G. Detection thresholds for
stimuli in humans and monkeys: comparison with threshold events in
mechanoreceptive afferent nerve fibers innervating the monkey hand.
J. Neurophysiol. 35: 122136, 1972.
MOUNTCASTLE, V. B. AND POWELL, T. P. Neural mechanisms subserving
cutaneous sensibility, with special reference to the role of afferent inhibition
in sensory perception and discrimination. Bull. Johns Hopkins Hosp. 105:
201232, 1959.
MOUNTCASTLE, V. B., TALBOT, W. H., AND KORNHUBER, H. H. The neural
transformation of mechanical stimuli delivered to the monkeys hand. In:
Touch, Heat, Pain and Itch, edited by A. V. de Reuck and J. Knight.
London: Churchill Livingstone, 1966, p. 325351.
PHILLIPS, J. R., JOHANSSON, R. S., AND JOHNSON, K. O. Responses of human
mechanoreceptive afferents to embossed dot arrays scanned across fingerpad
skin. J. Neurosci. 12: 827 839, 1992.
POULOS, D. A., MEI, J., HORCH, K. W., TUCKETT, R. P., WEI, J. Y., CORNWALL,
M. C., AND BURGESS, P. R. The neural signal for the intensity of a tactile
stimulus. J. Neurosci. 4: 2016 2024, 1984.
PUBOLS, B. H. Effect of mechanical stimulus spread across glabrous skin of
raccoon and squirrel monkey hand on tactile primary afferent fiber discharge. Somatosens. Mot. Res. 4: 273308, 1987.
PUBOLS, B. H. AND BENKICH, M. E. Relations between stimulus force, skin
displacement, and discharge characteristics of slowly adapting type I cutaneous mechanoreceptors in glabrous skin of squirrel monkey hand. Somatosens. Mot. Res. 4: 111125, 1986.
PUBOLS, B. H. AND PUBOLS, L. M. Coding of mechanical stimulus velocity and
indentation depth by squirrel monkey and raccoon glabrous skin mechanoreceptors. J. Neurophysiol. 39: 773787, 1976.
SCHNEIDER, W. The tactile array stimulator. Johns Hopkins APL Tech. Digest
9: 39 43, 1988.
TALBOT, W. H., DARIAN-SMITH, I., KORNHUBER, H. H., AND MOUNTCASTLE,
V. B. The sense of flutter-vibration: comparison of the human capacity with
response patterns of mechanoreceptive afferents from the monkey hand.
J. Neurophysiol. 31: 301355, 1968.
VEGA-BERMUDEZ, F. AND JOHNSON, K. O. Surround suppression in the responses of primate SA1 and RA mechanoreceptive afferents mapped with a
probe array. J. Neurophysiol. 81: 27112719, 1999.
WERNER, G. AND MOUNTCASTLE, V. B. Neural activity in mechanoreceptive
cutaneous afferents: stimulus- response relations, Weber functions, and
information transmission. J. Neurophysiol. 28: 359 397, 1965.
WERNER, G. AND MOUNTCASTLE, V. B. Quantitative relations between mechanical stimuli to the skin and neural responses evoked by them. In: The Skin
Senses, edited by D. R. Kenshalo. Springfield, IL: Thomas, 1968, p. 112
137.
WHEAT, H. E., GOODWIN, A. W., AND BROWNING, A. S. Tactile resolution:
peripheral neural mechanisms underlying the human capacity to determine
positions of objects contacting the fingerpad. J. Neurosci. 15: 55825595,
1995.