1Krieger Mind/Brain Institute; 2Department of Neuroscience; and 3Biomedical Engineering Department, The Johns Hopkins University, Baltimore, Maryland 21218
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ABSTRACT |
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Brisben, A. J., S. S. Hsiao, and K. O. Johnson. Detection of vibration transmitted through an object grasped in the hand. A tool or probe often functions as an extension of the hand, transmitting vibrations to the hand to produce a percept of the object contacting the tool or probe. This paper reports the psychophysical results of a combined psychophysical and neurophysiological study of the perception of vibration transmitted through a cylinder grasped in the hand. In the first part of the psychophysical study, 19 subjects grasped a cylinder, 32 mm diam, with an embedded motor that caused vibration parallel to the axis of the cylinder. The relationship between threshold and frequency was the traditional U-shaped function with a minimum between 150 and 200 Hz. Except a study by Békésy in which subjects grasped a rod that vibrated parallel to the skin surface, thresholds above 20 Hz were lower and the slopes were steeper than any reported previously. Thresholds were <0.01 µm in some subjects. Data from both the psychophysical and the neurophysiological studies suggest that detection performance at frequencies >20 Hz was based on activity in Pacinian afferents. The extreme sensitivity compared with previous reports may have resulted from differences in contact area, direction of vibration, contact force, and the shape of the stimulus probe. The effects of each of these variables were studied. At 40 and 300 Hz (frequencies near the lower and upper end of the Pacinian range) thresholds were 9.8 and 18.5 dB (68 and 88%) lower, respectively, when subjects grasped the cylinder than when a 1-mm-diam probe vibrated perpendicular to the skin. These differences were accounted for as follows: 1) thresholds at a single fingerpad obtained with the large cylindrical surface were, on average, 20 and 60% lower, respectively, than thresholds with the punctate probe; 2) thresholds at the palm were, on average, 15 and 40% lower, respectively, than at the fingerpads; 3) thresholds obtained when the subjects grasped the cylinder averaged 40 and 20% less, respectively, than when the cylinder contacted only the palm; 4) thresholds with the cylinder contacting two fingers were 10 and 30% lower, respectively, than thresholds with the cylinder contacting a single finger; and 5) thresholds with vibration parallel to the skin surface were, on average, 10 and 30% lower, respectively, than thresholds with vibration perpendicular to the skin. Contact force, which was varied from 0.05 to 1.0 N, had no effect.
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INTRODUCTION |
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When we have become skilled in the use of a tool or
a probe, we often perceive the events at the working surface of the
tool or probe as effectively as if our fingers were at that surface. Katz (1925) demonstrated this when he showed that we can discriminate some textures as effectively with a probe as with direct contact with
the fingers. Further, he showed that this capacity is based on
transmitted vibrations; subjects' judgements were impaired when the
transmitted vibrations were dampened. The Pacinian corpuscle is
strongly implicated as the mechanoreceptor primarily responsible for
the perception of transmitted vibration. This was shown initially by
Hunt (1961)
, who used an accelerometer to show that the
spontaneous discharge of a Pacinian afferent fiber was synchronized
with ambient vibrations in the building where he was conducting his
experiments. Indeed, a standard diagnostic procedure for identifying
Pacinian responses is to tap lightly on the table holding the
neurophysiological preparation. Subsequent studies linking
psychophysical and neurophysiological data showed that the limits of
vibratory detection at high frequencies depend on activity in Pacinian
afferents (Lindblom and Lund 1966
; Mountcastle et
al. 1972
; Verrillo 1963
).
Although tactile vibratory perception has been studied extensively
(Békésy 1939; Bernstein et al.
1986
; Bolanowski et al. 1988
; Craig
1968
; Goble et al. 1996
; Lamore and
Keemink 1988
; Lofvenberg and Johansson 1984
;
Mountcastle et al. 1972
, 1990
; Rabinowitz et al. 1987
; Verrillo 1968
),
no previous study has addressed the perception of transmitted
vibrations through an object held in the hand. Predicting the human
ability to detect and discriminate transmitted vibrations with any
certainty is still not possible. When we grasp an object, it contacts
multiple skin sites simultaneously, vibrations may occur in any
direction, the grip force is usually determined by demands of the motor
task rather than the need to optimize one's sensory capacity, and
there is typically no constraining surround as in many studies of
vibratory detection. One of these variables, the direction of vibration relative to the skin, has not been studied at all. Thus we have undertaken combined psychophysical and neurophysiological experiments in which a manual probe, a cylinder 32 mm diam, transmits vibrations induced by a motor embedded within the cylinder.
The first experiment shows that at frequencies >20 Hz thresholds are
lower and the threshold-versus-frequency curves are steeper than any
reported previously except those by Békésy
(1939), whose stimulus procedures were similar to those used in
this study. The results of the first experiment suggest that the
detection performance at frequencies exceeding 20-25 Hz is based on
neural activity in Pacinian afferent fibers. This interpretation is
supported directly by a companion neurophysiological study in monkeys
using the same stimulus procedures, which showed that only Pacinian responses could account for the detection performance at 40 Hz (unpublished observations). These data suggest that the detection of
transmitted vibration over almost the entire frequency range relevant
for the perception of transmitted vibration is based on activity in
Pacinian afferent fibers. Four more experiments were performed to
determine how contact area, contact force, direction of vibration, and
the shape of the contactor affect this performance at low (40 Hz) and
high (300 Hz) frequencies within the range served by Pacinian
mechanisms. Except contact force, each of these factors affected
detection performance.
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METHODS |
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Subjects were seated comfortably in front of a computer
terminal. Their right arm and hand rested on a foam support mounted on
the vibration isolation table (Technical Manufacturing, model 63-17595)
that held the vibratory stimulator. A screen blocked the subjects'
view of the apparatus and their hand. Although there was no audible
signal associated with the vibratory stimuli near threshold, subjects
wore headphones delivering pseudo-white masking noise (bandwidth 100 Hz
to 15 kHz) to obscure any possible sounds related to the vibratory
stimuli. When subjects actively grasped the stimulus (experiments
1 and 2), the arm and hand were unrestrained. Otherwise, the subject's right hand was restrained in a mold made of
thermoplastic (North Coast Medical), which was covered with moleskin;
the fingers were embedded in plasticine, and the thumb was suspended
with a sling made of moleskin to keep it away from the stimulators.
Skin temperature was monitored throughout the experiments and never
fell below 30°C. After each stimulus trial the computer prompted the
subject for a response. Subjects signaled readiness for the next trial
by hitting a key. The subjects received no feedback during any of the
experiments in this study. Each experimental session consisted of two
to four tasks and lasted for 1 h. Occasionally, subjects participated
in two sessions in a single day, but in this case the sessions were
separated by
3 h.
Stimulators
The stimulators were mounted on the vibration isolation table.
Vibratory stimuli were delivered parallel or perpendicular to the skin
surface (see methods specific to each experiment). Vibratory stimuli
perpendicular to the skin surface were delivered with a
servo-controlled linear motor (Chubbuck 1966). Except
experiment 1, vibratory stimuli parallel to the skin surface
were delivered by the stimulator shown in Fig.
1, which consisted of an acrylic cylinder, 32 mm diam and 160 mm long, driven by a linear motor (Schneider 1988
) mounted within the cylinder. The linear
motor functioned as a shaker, delivering a force to the cylinder that was equal and opposite to the force required to accelerate the shaft of
the linear motor. The cylinder was mounted with monofilaments, as
illustrated in Fig. 1, to allow movement in the axial direction while
constraining movement in the off-axial directions. This assembly was
mounted on a counter-balanced pivot arm with an adjustable counterweight that allowed the contact force to be adjusted. In experiment 1, the cylinder was driven by the Chubbuck linear
motor (Chubbuck 1966
) mounted externally.
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No matter which stimulator was used, the motion of the object in
contact with the skin was monitored continuously by a triaxial accelerometer (Kistler, M8692B5, ±50 m · s2 range,
0.005 m · s
2 sensitivity, which corresponds to 80- and
1.4-nm peak displacements at 40 and 300 Hz, respectively) mounted so
that one of its axes was collinear with the direction of vibration. In
all experiments in which the Chubbuck linear motor was used, the
accelerometer was mounted in series between the motor and the stimulus
surface contacting the skin. In all experiments in which the stimulator pictured in Fig. 1 was used, the accelerometer was mounted on the end
of the cylinder. Vibratory amplitudes in the off-axial directions were
<10% of the axial amplitudes in all experiments. Although both linear
motors (Chubbuck 1966
; Schneider 1988
)
had their own displacement transducers, the vibratory amplitudes
reported here were derived from the accelerometer because of its
greater sensitivity. When the vibratory amplitudes were large enough to register clearly on the motors' displacement transducers (amplitudes >1 µm), the measurements from the accelerometer and the motors agreed.
Sinusoidal, vibratory waveforms were created with an array processor card (AP2, Tucker-Davis Technologies, TDT) and stored with a temporal resolution of 5,000 samples per second. The driving voltages for the servomotors were produced with a 16-bit D/A converter (DA3-4, TDT), a low-pass anti-aliasing filter with a 1-kHz cutoff frequency (FT5, TDT), and a programmable attenuator (PA4, TDT, 0-99.9 dB, 0.1-dB resolution).
Psychophysical methods
Trials were initiated by the subject hitting a key. Trials consisted of two (experiment 1) or three (all other experiments) intervals, each 1 s long, in which the vibratory stimulus might appear. After each trial, the subject was required to choose the interval in which the stimulus occurred. A three interval forced choice (3 IFC) trial, the stimulus, and the timing of cues are illustrated in Fig. 2.
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Detection thresholds were determined with adaptive tracking procedures.
During each task the stimulus frequency was fixed and the amplitude
varied from trial to trial based on the tracking rules. The initial
stimulus amplitude was always higher than the subject's threshold. In
experiment 1, a one-up, two-down adaptive tracking procedure
was used in which the stimulus was increased after each incorrect
response and decreased after each pair of successive correct responses.
In the remaining experiments, which employed a 3 IFC design, a one-up,
three-down tracking rule was used because it has been shown to obtain
thresholds more efficiently (Green 1990; Green et
al. 1989
; Kollmeier et al. 1988
; Shelton and Scarrow 1984
). In this method, the stimulus amplitude is
increased after each incorrect response and decreased after three
successive correct responses. In both methods, amplitudes were changed
initially by 4 dB and then by 1 dB after three reversals. Each task
continued until 12 reversals were obtained at the 1-dB step size. The
threshold was estimated as the average of those last 12 reversal
amplitudes. Detection thresholds obtained in this way correspond, on
average, to 70.1% correct responses for the one-up, two-down procedure and 79.4% for the one-up, three-down procedure (Levitt
1970
).
The 12 reversal amplitudes were also used to obtain the standard error of the estimate of the threshold. The 12 reversals provide, in pairs, 6 estimates of the threshold, the mean threshold, and the standard error of the mean. More specifically, the six pair-wise estimates of threshold were used as repeated measures in analyses of variance. All analysis was done with SPSS for Windows Version 7.0 (SPSS, Chicago, IL).
Methods specific to each experiment
EXPERIMENT 1: ACTIVELY GRIPPING THE CYLINDER. In this experiment the subject was instructed to grasp a cylinder with whatever force felt most comfortable. The forces actually used were not measured, but subjects reported using a light-to-moderate force. The cylinder was suspended by filaments as in Fig. 1 but was driven axially by the Chubbuck linear motor, which was attached at one end. Most of the glabrous skin of the hand was in contact with the cylinder during this experiment. The experimental design, described above, was a 2 IFC design, and a one-up, two-down adaptive tracking rule was used to find the threshold.
EXPERIMENT 2: EFFECT OF STIMULUS LOCATION WITH THE CYLINDRICAL STIMULATOR. This experiment employed the stimulator illustrated in Fig. 1 and had two parts. In the first part, subjects grasped the cylinder actively as in experiment 1, the purpose being to repeat and verify the results of experiment 1 with the newer stimulator and the 3 IFC psychophysical design. In the second part, subjects' hands were restrained (see general methods above) in an open, palm-up position, while the cylinder rested on the skin with a 0.5-N contact force; that is, vibratory stimuli are delivered under passive conditions.
The contact area associated with each of the different stimulus placements was measured by coating a subject's hand with blotting ink and lowering the cylinder onto the skin, which transferred the ink to the surface of the cylinder. The cylinder was raised, and a piece of paper was wrapped around it to obtain an impression of the contact area. The cylinder was then cleaned with isopropyl alcohol, and the procedure was repeated for each stimulus condition presented in this experiment. The resulting ink blots were placed on a digitizing sketch pad (Summa Sketch, Summagraphics) and digitized with a software graphics program (AutoCAD, Autodesk), which calculated the contact areas.EXPERIMENT 3: EFFECT OF CONTACT FORCE. Experiment 3 was conducted with the cylinder illustrated in Fig. 1, and the hand was restrained as in experiment 2. Vibratory detection thresholds were obtained for five contact forces: 0.05, 0.1, 0.2, 0.5, and 1.0 N. At 1.0 N the force is light but firm. Contact force was set by adjusting a counterweight at the opposite end of the pivot arm on which the cylinder was mounted. The force applied by the cylinder was measured with a digital force gauge (Omega Engineering).
EXPERIMENT 4: EFFECT OF STIMULUS LOCATION WITH THE
PUNCTATE PROBE.
The purpose of experiment 4 was to compare thresholds
obtained with the cylinder in experiment 2 with thresholds
obtained with a punctate probe at the same stimulus sites. The
subjects, the hand restraint, and the procedures were the same as in
experiment 2. The punctate probe was made of Delrin
(Dupont), was 1 mm diam at the tip, and was mounted on the Chubbuck
linear motor (Chubbuck 1966). The tip of the punctate
probe was glued to the skin surface (Freeman and Johnson
1982
), and the indentation depth was adjusted until there was
no reaction force (so the skin vibrated around its resting position
without harmonic distortion).
EXPERIMENT 5: EFFECTS OF STIMULUS DIRECTION AND CONTACT AREA. Two probes, a cylindrical surface and a punctate probe, 1 mm diam, were used in experiment 5. The cylindrical surface was constructed from the same stock used to make the cylinder in experiment 2 (acrylic plastic, 32 mm diam) and was mounted on the shaft of the Chubbuck motor. The axis of the cylinder was perpendicular to the motor shaft so the surface of the cylinder contacting the skin vibrated in a direction perpendicular to the skin surface. Indentation depth was set to produce a reaction force of 0.2 N. The punctate probe was identical to the probe used in experiment 4 (a Delrin shaft machined to a tip, 1 mm diam) and was clamped to the cylinder illustrated in Fig. 1 with a Delrin collar. The punctate probe's shaft was mounted perpendicular to the axis of the cylinder and oriented so that it was perpendicular to the skin. As in experiment 4, the punctate probe was glued to the skin, and the pivot arm was balanced to produce no net force on the skin. Activation of the motor within the cylinder produced motion parallel to the skin surface.
Gluing the probe to the skin. The purpose of gluing the probe to the skin was to ensure that the differences in threshold between the cylinder and the punctate probe (experiment 4) and between vibration perpendicular and parallel to the surface of the skin (experiment 5) did not arise because the skin did not follow the sinusoidal motion of the probe when vibrated perpendicular to the skin surface. When the cylinder and punctate probe vibrate parallel to the skin surface, they remain in constant contact with the skin; consequently, the stimulus energy is confined to the fundamental frequency being tested. When a probe vibrates perpendicular to the skin surface, it may or may not remain in contact with the skin throughout each sinusoidal cycle (Goodwin et al. 1989 ![]() |
RESULTS |
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The experimental designs are summarized in Table
1. In the first experiment, vibratory
thresholds were determined for 19 subjects who actively grasped a
cylinder vibrated in a direction parallel to the skin. The thresholds
were lower than those obtained previously with probes vibrated
perpendicular to the skin surface (e.g., Bernstein et al.
1986; Gescheider et al. 1994
; Lamore and Keemink 1988
; Mountcastle et al. 1972
;
Rabinowitz et al. 1987
; Verrillo
1968
). Factors that may have resulted in the lower thresholds are studied in experiments 2-5. The effect of stimulus
location is studied in experiments 2 and 4. The effect of stimulus type (cylinder or punctate probe) is studied in
experiments 4 and 5; the effect of task mode
(active or passive), contact area, and stimulus location are studied in
experiment 2; the effect of contact force is studied in
experiment 3; and the effect of stimulus direction is
studied in experiment 5. The same four subjects participated in experiments 2-5 to make within-subject comparisons
possible.
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Experiment 1: actively gripping the cylinder
The purpose of this experiment was to determine the human capacity
to detect transmitted vibration when grasping a cylinder whose size and
shape (32 mm diam, 160 mm long) were much like the handle of a common
tool (e.g., a screwdriver) or probe (e.g., a cane). A relatively large
number of subjects were studied to obtain a representative sample of
this human capacity; 19 subjects (11 male, 8 female, ages 21-45)
participated in this experiment. Figure 3
illustrates the average thresholds at frequencies ranging from 10 to
300 Hz. The threshold was 14 µm at 10 Hz, declined to 5.6 µm at 20 Hz, and then reached a minimum of 0.03 µm at 150 and 200 Hz. The
decline in threshold was 85% per frequency doubling (15.7 dB per
octave) between 20 and 150 Hz. The slope and magnitudes of the
thresholds illustrated in Fig. 3 are nearly identical with those
reported by Békésy in experiments where subjects grasped a
rod vibrating parallel to the skin surface (Békésy
1939
) (
15.4 dB per octave slope and 0.03 µm threshold at
200 Hz). Apart from Békésy's results, the slope is steeper
and the minimum threshold is lower than any in the literature. We
surmised that this may be attributed to differences in contact mode
(active vs. passive), stimulus location on the hand, contact area, the
direction of vibration, or the force of application. We explored each
of these potential factors in experiments 2-5.
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Experiment 2: effect of stimulus location with the cylindrical stimulator
Four subjects (2 male, ages 19 and 26, and 2 female, ages 27 and 34) participated in this and the remaining experiments (experiments 2-5). In this experiment and the remaining experiments, the data are displayed on logarithmic coordinates, means are geometric means, and the analyses were done on the logarithms of the thresholds. Every analysis includes a factor for individual subjects so that differences between subjects are not counted as random variation; this makes each analysis more sensitive to the stimulus parameter being varied. Differences between subjects were statistically significant in all tests (P < 0.01).
Experiment 2 employed the stimulator shown in Fig. 1. Stimuli were applied under passive conditions (0.5 N force, see METHODS) to eight different sites: three on the middle finger (distal: D3d; middle: D3m; and proximal phalanx: D3p), three on the middle and ring fingers combined (distal: D34d; middle: D34m; and proximal phalanges: D34p), and two on the palm (Palm-d and Palm-p, see Fig. 4). Subjects also grasped the cylinder actively, as in experiment 1, so the data from the four subjects in experiments 2-5 could be compared with the larger group that participated in experiment 1. The mean contact areas at each site are listed in Fig. 4.
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The average thresholds are shown in Fig. 4. All the analyses of statistical significance were based on ANOVA. At 40 Hz, the threshold at the middle phalanx was significantly greater than the rest, and the threshold resulting from the active grip was less than the rest (P < 0.05). Apart from that, the differences between conditions shown in Fig. 4 failed to reach significance (P > 0.05). At 300 Hz, the threshold was lowest when the subjects grasped the cylinder, next lowest when the cylinder contacted the palm, and then rose as the cylinder moved away from the palm on the fingers. All these differences were highly significant (P < 0.01).
When two phalanges were stimulated, the thresholds were, on average,
lower than when only a single phalanx was stimulated (see Fig. 4).
Because the force rather than the pressure was held constant, the areal
increase averaged 44% rather than 100%. This resulted in an average
drop in threshold of 1.55 dB (0.7 dB at 40 Hz;
2.4 dB at 300 Hz),
which is equivalent to 2.95 dB drop per doubling in contact area.
Experiment 3: effect of contact force
The effects of contact force (see Fig.
5) were evaluated at the distal phalanx
of the middle finger (D3d in Fig. 4) and the distal part of the palm
(Palm-d in Fig. 4). Contact force was varied in five steps from 0.05 to
1.0 N. Overall, contact force had no significant effect. The regression
slope of the logarithm of threshold on the logarithm of force yielded
positive coefficients in two of the four conditions and negative
coefficients in the other two conditions. In one case (300 Hz, Palm-d)
the slope was statistically significant (0.8 dB per doubling of
contact force, P < 0.05, t-test), but when
corrected for multiple comparisons it was not significant. These
results suggest that contact force played little, if any, role in the
detection performance measured in experiment 1.
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Experiment 4: effect of stimulus location with the punctate probe
The aim of experiment 4 was to compare thresholds obtained with the cylinder in experiment 2 with thresholds obtained with a punctate probe at the same stimulus sites. Figure 6, A and B, show the results of experiment 4. On average, the punctate thresholds on the fingers were lower at 40 Hz and higher at 300 Hz than the thresholds on the palm, but the difference was only significant at 300 Hz (ANOVA, P = 0.002). The more interesting comparison, however, is the comparison between thresholds with the two kinds of probes, which is illustrated in Fig. 6, C and D. The punctate thresholds were significantly greater than the thresholds with the cylinders at both the fingers and the palm (P < 0.001, t-test). At 40 Hz, the difference was significantly greater on the palm (9.0 dB on average) than on the fingers (3.1 dB on average; ANOVA, P = 0.014). At 300 Hz, the difference, which averaged 9.2 dB, did not depend on location in any significant way.
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Experiment 5: effects of vibratory direction and contact area
The cylinder was vibrated parallel to the skin surface in experiment 3; the punctate probe was vibrated perpendicular to the skin surface in experiment 4. The other two conditions required of a balanced 2 × 2 factorial experiment designed to determine the effects of contact area and vibratory direction (cylinder vibrated perpendicular to the skin surface and punctate probe vibrated parallel to the skin surface) are investigated in experiment 5. One of these conditions was effected by mounting a cylinder segment (same diameter as the cylinder illustrated in Fig. 1) on the shaft of a linear motor and by vibrating it perpendicular to the skin. The other condition (punctate probe vibrated parallel to the skin surface) was effected by attaching a punctate probe with the same dimensions as the probe used in experiment 4 to the cylinder (Fig. 1) and vibrating it parallel to the skin surface. The probe was glued to the skin to ensure skin movement comparable with that in experiment 4. Experiment 5 was performed on D3d at 40 and 300 Hz.
The data are displayed in Fig. 7. Thresholds obtained with the cylinder at 40 Hz were, on average, 23% (2.3 dB) lower than the punctate thresholds; thresholds obtained with vibration parallel to the skin surface were, on average, 14% (1.3 dB) lower than the thresholds obtained with perpendicular vibration. At 300 Hz, the effects of probe type and vibratory direction were similar but larger, being 61% (8.2 dB) and 32% (3.3 dB), respectively. Only the relationship between probe type and thresholds was statistically significant at 300 Hz (P = 0.04, 2-way ANOVA of threshold vs. direction and stimulus type). Thus we infer that stimulus direction has a small effect at both low and high frequencies and that the differences between thresholds obtained in experiments 3 and 4 are primarily attributable to differences in contact area.
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DISCUSSION |
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The first experiment in this study was aimed at determining the
human capacity to detect transmitted vibration when grasping a cylinder
whose size and shape were much like the handle of a common tool (e.g.,
a screwdriver) or probe (e.g., a cane). The result was that the
detection thresholds were lower than any reported previously except
those by Békésy (1939), who also had
subjects grip a probe actively between the fingertips. As in
Békésy's experiment, the cylinder vibrated parallel to the
skin surface, and the subjects were free to adopt a grip force that
seemed most comfortable. The mean thresholds at 10 and 20 Hz were
comparable with thresholds observed in previous studies in which a
probe contacted the skin without a constraining surround
(Békésy 1939
; Mountcastle et al.
1972
; Van Doren 1990
) and were higher than those
observed in some studies in which an annulus surrounded the vibrating
probe (Bernstein et al. 1986
; Lamore and Keemink 1988
). At frequencies above 30 Hz, however, the mean thresholds in experiment 1 (e.g., 0.66 µm at 40 Hz and 0.03 µm at
200 Hz) are as low or lower than any reported previously. The
difference is most pronounced at 40 Hz where the thresholds were 6-18
dB lower than any reported previously (Békésy
1939
; Bernstein et al. 1986
; Lamore et
al. 1986
; Mountcastle et al. 1972
;
Rabinowitz et al. 1987
; Verrillo et al.
1983
). Between 20 and 150 Hz, the thresholds in
experiment 1 dropped at 15.7 dB per octave; in
Békésy's (1939)
experiments, thresholds
dropped at 15.4 dB per octave over the same range. The average peak
sensitivity reported here, 0.03 µm (0.02 µm
root-mean-square) detection threshold at 200 Hz, is the same as
that reported by Békésy and is lower than that reported in
other studies (e.g., Bernstein et al. 1986
;
Gescheider et al. 1994
; Lamore and Keemink
1988
; Mountcastle et al. 1972
; Rabinowitz et al. 1987
; Verrillo 1968
). The minimum
threshold for some subjects was <0.01 µm, which represents a
vibratory excursion at the skin surface not much greater than the
thickness of a cell membrane.
Experiments 2-5 were designed to examine the factors yielding this sensitivity. In these experiments we varied contact area, stimulus location, contact force, probe shape, and stimulus direction. The results are summarized in Fig. 8, where the stimulus conditions A-H are arranged in order of decreasing thresholds at both 40 and 300 Hz. Between the condition with the highest threshold (vibration perpendicular to the skin of the pad of the 3rd digit with a 1-mm-diam probe) and the lowest threshold (subjects actively gripping a 32-mm-diam cylinder vibrating parallel to the skin surface), the thresholds at 40 and 300 Hz dropped by 9.8 and 18.5 dB, respectively. The factors that were examined contributed in varying degree to the gradual decline in threshold across the various stimulus conditions represented in Fig. 8. Contact force had no effect over the range tested. Direction of vibration had a small effect: vibration parallel to the skin surface produced thresholds at 40 and 300 Hz that were 1.3 and 3.3 dB lower, respectively, than with vibration perpendicular to the skin surface. Contact area, probe type, and stimulus location had the major effects.
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Neural mechanisms
Vibratory detection has been studied extensively. The large number
of studies of vibratory detection results from the large number of
variables that can affect vibratory perception: vibratory frequency,
duration, direction, contact geometry, contact area, contact force,
state of adaptation, context (e.g., masking), mode (active vs.
passive), skin site, skin temperature, age, and pathology. The results
of these many studies are accounted for well by the hypothesis that
vibratory detection depends on some critical level of activity in
Pacinian afferents at high frequencies (Lindblom and Lund
1966; Talbot et al. 1968
; Verrillo
1963
) and in a separate set of afferents at low frequencies
(Verrillo 1963
), which have been identified as Meissner
afferents (Mountcastle et al. 1972
).
The result of this dual mechanism is a curve of
threshold-versus-frequency with two limbs (Békésy
1939; Talbot et al. 1968
; Verrillo
1968
) whose intersection defines the transition frequency between the regions dominated by Meissner and Pacinian afferents. The
high-frequency limb is steeper than the low-frequency limb; therefore
changes in the stimulus that modify Meissner or Pacinian engagement
(e.g., contactor area) have a predictable effect on the transition
frequency (Gescheider et al. 1978
; Goble et al. 1996
; Lamore and Keemink 1988
; Talbot et
al. 1968
; Verrillo 1963
). Most important in
relation to the present study is the demonstration by Verrillo
(1963)
that increasing vibratory contact area produces increasing vibratory sensitivity in the high-frequency region, which
drives the transition point between the Meissner and Pacinian domains
to lower frequencies.
We believe that the transition frequency between the Meissner and
Pacinian domains in experiment 1 was 20-25 Hz. Threshold slope changes by 2:1 at 20 Hz (see Fig. 3); the slopes below and above
20 Hz were 7.9 and 15.7 dB per octave, respectively, and the change in
slope is highly significant (paired sample t-test, P < 0.001). Békésy's results
(Békésy 1939), which are similar to our own,
extend down to 0.3 Hz. In those experiments, the transition point
between the low- and high-frequency domains occurred at 20-25 Hz.
Between 0.3 and 20 Hz, the threshold declined at 2 dB per octave;
between 20 and 200 Hz, the decline was 15.4 dB per octave. Our
inference that detection performance above 20-25 Hz was based on
activity in Pacinian afferents is supported by neurophysiological studies in our laboratory in which the stimulus methods were the same
as in experiment 2. Recordings from primary afferents in the
rhesus monkey showed that only Pacinian thresholds are low enough at 40 Hz to account for the psychophysical thresholds (unpublished observations). In the remainder of this section, we discuss studies of
the Pacinian corpuscle and then speculate on the specific mechanisms underlying the results of experiments 2-5.
Pacinian response properties
The first neurophysiological study of the Pacinian corpuscle was
an inadvertent demonstration of its extreme sensitivity to transmitted
vibration. Adrian and Umrath (1929) indented an exposed Pacinian with a punctate probe and observed a sustained discharge that
increased monotonically with increasing force. Because of this
observation, the Pacinian corpuscle was thought to be a pressure receptor. The Pacinian's insensitivity to sustained deformation, its
selective sensitivity to transient deformation, and its extreme sensitivity to vibration were discovered subsequently (Gray and Malcolm 1950
; Sato 1961
; Scott
1951
), but the reason for Adrian and Umrath's observation was
not discovered until Hunt (1961)
showed that a sensitive
Pacinian responds to the ambient vibrations transmitted through a
building. Adrian and Umrath were evidently coupling ambient vibration
to their Pacinian more effectively as they drove their probes into the
Pacinian lamellae.
The most remarkable feature of the Pacinian corpuscle is its large size
and its multilayered, lamellar structure surrounded by a continuous
capsule (Pease and Quilliam 1957; Zelena
1994
). The principal function of these lamellae, we believe, is
to protect the extremely sensitive receptor ending from the high static
and low-frequency forces that occur in many motor acts, thereby leaving the ending sensitive to transmitted vibrations with amplitudes as small
as 10 nm. The capsule is continuous and can retain fluid under slight
pressure (Gray and Sato 1955
; Pease and Quilliam 1957
). Slow mechanical distortion causes a simple
redistribution of the fluid in the outer lamellae, leaving the inner
lamellae and the unmyelinated ending undisturbed, whereas rapid
mechanical events are transmitted to the core through the viscous shear
forces in the fluid as it is redistributed within the lamellae
(Hubbard 1958
; Lowenstein and Skalak
1966
). The critical feature of the Pacinian corpuscle (and
other corpuscular receptors like the Meissner corpuscle) is that it
bathes its extremely sensitive receptor within an aqueous medium that
is completely incompressible at all physiologically relevant loads.
This provides a partial explanation for the complete insensitivity to
force that we observed between 0.05 and 1.0 N.
Effects of stimulus location
The effect of stimulus location could depend on variation in the
density of Pacinian receptors, variation in receptor sensitivity between locations, and on biomechanical factors such as proximity to a
large mass of Pacinian corpuscles or proximity to a structure, such as
bone, that transmits vibrations for great distances. There is no
physiological evidence for variation in Pacinian sensitivity between
locations in the hand (Mountcastle et al. 1972;
Talbot et al. 1968
). Direct anatomic methods
(Bushong 1963
; Cauna and Mannan 1958
,
1959
) and indirect methods based on fiber counts in the
median nerve at the wrist (Johansson and Vallbo 1979
)
provide consistent estimates of the number and distribution of Pacinian corpuscles in the human hand. Serial reconstructions of a fetal finger
by Cauna and Mannan (1958
, 1959
) yielded
counts of 62, 55, and 61 Pacinian's in the radial half of the distal,
middle, and proximal phalanges. Bushong (1963)
found 176 Pacinian corpuscles in half a fetal thumb. These studies suggest that
there are ~350 Pacinian corpuscles per finger. Attributing half that
number to the fifth finger yields an estimate of ~1,600 Pacinian
corpuscles in the fingers. Bushong (1963)
also
reconstructed approximately half the palm of a fetus and found 428 Pacinian corpuscles, which yields a rough estimate of 800 Pacinian
corpuscles for the entire palm and 2,400 Pacinian corpuscles for the
entire hand. This ratio of 2:1 for the distribution of Pacinian
corpuscles between the fingers and the palm corresponds almost exactly
to the ratio found by Johansson and Vallbo (1979)
; in a
sample of 374 mechanoreceptive afferents recorded from the median nerve
they found 28 Pacinian corpuscles in the fingers and 15 in the palm.
Thus Pacinian corpuscle density appears to be higher in the fingers
than in the palm. However, the total number of Pacinian corpuscles near
a stimulus applied to the palm is much larger than the number near a
stimulus applied to any single finger. For example, suppose that near
threshold the stimulus engages the most sensitive Pacinian corpuscles
at distances up to 25 mm from the probe. In this case, the stimulus labeled palm-d in Fig. 4 will affect a population of 6-700 Pacinian corpuscles (2-300 in the palm and ~100 in the proximal phalanges of
the four fingers, D2-D5). The stimulus applied to D3d will, in
contrast, affect only ~1-200 Pacinian corpuscles.
The two factors with the greatest effect, contact area and stimulus
location, are accounted for by assuming that vibratory detection
depends on a threshold level of activation in the Pacinian population,
which might be specified as the activation of a specified minimum
number of Pacinian afferents or the production of a specified minimum
population impulse rate. When the receptor thresholds vary widely, as
they do in Pacinian afferents (Freeman and Johnson 1982;
Mountcastle et al. 1972
), increasing vibratory amplitude increases the total population response by increasing the total tissue
volume in which the vibratory field exceeds the threshold of the most
sensitive afferents, by recruiting less sensitive afferents to the
active population, and by increasing the discharge rate in those
already recruited to activity (Johnson 1974
). When the
contact region is small (e.g., the punctate probe in experiment 4) and is applied to a region in which relatively few Pacinian corpuscles are close to the probe (e.g., a fingerpad), a greater vibratory amplitude is required to produce the minimum Pacinian engagement required for threshold. When the contact region is large and
the probe is applied to a location where there are many Pacinian
corpuscles nearby (e.g., the palm-d placement in experiment 2) the vibratory amplitude required to produce a fixed level of activity will be lower.
Effects of contact force
Our report that a 20-fold change in contact force from 0.05 to 1 N
had no detectable effect on threshold is at odds with previous reports
of the effect of force over the same force range (Craig and
Sherrick 1969; Lamore and Keemink 1988
;
Verrillo 1962
). The study with stimulus conditions most
like the conditions in this study is by Lamore and Keemink
(1988)
, who reported almost a 30-db decline in threshold
between 0.05 and 0.5 N at 210 Hz when applying a 14-mm-diam probe with
no surround to the distal pad of the third finger and to the thenar
eminence; between 0.5 and 2.0 N their threshold was essentially
constant (at 0.05 µm at the thenar eminence). An explanation for the
difference between our study and previous studies can be found in a
study by Goodwin et al. (1989)
on the skin's failure to
follow vertical, sinusoidal skin indentation; under some stimulus
conditions (e.g., high-frequency and low indentation depth before
vibration) the peak-to-peak skin excursion is a small fraction of the
peak-to-peak probe excursion. The reason relates to the forces
producing skin contact during withdrawal. During withdrawal, the only
forces driving the skin are its own viscoelastic restoring forces. If
the probe withdraws more rapidly than the skin's natural recovery
rate, it leaves the skin. Reduced skin-following at higher frequencies
is explained by higher probe withdrawal velocities. Increased
skin-following with increased mean indentation depth is explained by
Newton's second law: increased mean force produces increased depth
until the restoring (reaction) force equals the indentation force.
This, in turn, produces increased recovery velocity, better
skin-following, and increased peak-to-peak skin excursion. This
accounts for the substantial reduction in threshold reported by
Lamore and Keemink (1988)
with increasing force. In our
experiments in which the probe vibrated parallel to the skin surface,
the probe was always in contact with the skin; therefore the skin
movement produced by the probe was independent of the mean force.
Because the forces that we and others (Lamore and Keemink
1988; Verrillo 1962
) have used in psychophysical
experiments are two to three orders of magnitude lower than forces that
may occur in manual tasks, extending these investigations to higher
forces is important. Nevertheless, common experience suggests that we are sensitive to minute transmitted vibrations even when gripping an
object with high force. The preservation of this sensitivity in the
presence of high static forces likely results from the corpuscular
structure of the Pacinian corpuscle as discussed above. Predicting the
outcome of a psychophysical experiment with contact forces >1-2 N is
difficult. Increasing force beyond 1-2 N could lower thresholds by
coupling transmitted vibrations to bones and tendons that might
transmit the vibrations more effectively to distant Pacinian
corpuscles. Conversely, the engagement of other mechanoreceptors by
higher forces might mask the effects of small, transmitted vibrations.
Effects of stimulus direction
Thresholds were lower on average when the probe vibrated parallel
to the skin surface than when it vibrated perpendicular to the skin
surface. The effect was relatively small (15% at 40 Hz and 30% at 300 Hz), but it was consistent at all four combinations of stimulus type
(cylindrical surface and the punctate probe) and frequency. No previous
studies of which we are aware directly compare the effects of stimulus
direction on vibratory detection. The reasons that vibration parallel
to the skin surface is more effective than vibration perpendicular to
the skin surface is not clear. The ultimate stimulus is dynamic strain
(Hubbard 1956; Lowenstein and Skalak
1966
). The explanation may be that horizontal skin vibration
produces shear strain in the subcutaneous tissues (Pereira et
al. 1991
) more effectively than does perpendicular vibration
when tissue motion is constrained by hard tissues 3-4 mm below the
surface of the skin.
Active versus passive touch
The idea that active and passive touch are different in some
fundamental way (Gibson 1962) has a long history
(reviewed in Vega-Bermudez et al. 1991
). To determine
whether there is a difference between perceptual capacity in active and
passive touch, the stimulus conditions must be identical in the two
conditions. Under these circumstances, the result has been either that
the perceptual capacity is the same in the two circumstances
(Vega-Bermudez et al. 1991
) or that it is superior in
the passive condition (Magee and Kennedy 1980
). The
explanation advanced for the latter finding is that active touch
requires division of attention between the sensory and motor tasks
(Magee and Kennedy 1980
).
In the experiments reported here, active touch produced the lowest
thresholds. However, the difference between the thresholds during
active gripping (H in Fig. 8) and the lowest threshold during passive presentation (G in Fig. 8, Palm-P in Fig. 4),
which amounted to 4 dB at 40 Hz and 2 dB at 300 Hz, is not large enough to demonstrate some special advantage for active touch. The difference is no greater than would be predicted from the larger total contact area (36.4 vs. 10 cm2) and therefore the larger number of
Pacinian corpuscles engaged by the stimulus in the active grip
condition. Another possibility that we cannot exclude is that the
muscle contraction that accompanies active grasping may have made
muscle spindles more sensitive to high-frequency vibration, but the
thresholds reported in experiment 1 are, as far as we know,
much lower than any reported for the activation of muscle spindle
afferents (Brown et al. 1967; Gregory and Proske
1988
).
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ACKNOWLEDGMENTS |
---|
The authors thank S. Patterson for building the stimulator used to deliver vibrations in this study and Drs. James Craig and Vernon Mountcastle for helpful advice and criticism.
This work was supported by National Institute of Neurological Disorders and Stroke Grants NS-18787 and NS-34086, and by the W. M. Keck Foundation.
Present address of A. Brisben: Baltimore Biomedical, Inc., 1414 Key Highway, Suite 320, Baltimore, MD 21230.
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FOOTNOTES |
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Address for reprint requests: K. O. Johnson, Krieger Mind/Brain Institute, Dept. of Neuroscience, Johns Hopkins University, 3400 North 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 8 April 1998; accepted in final form 17 November 1998.
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REFERENCES |
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