Department of Anatomy and Cell Biology, University of Melbourne, Parkville, Victoria 3052, Australia
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ABSTRACT |
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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 m1, 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.
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INTRODUCTION |
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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?
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METHODS |
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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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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
, 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.
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RESULTS |
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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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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 m1). 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 m1, 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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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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DISCUSSION |
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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.
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ACKNOWLEDGMENTS |
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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.
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FOOTNOTES |
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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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REFERENCES |
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