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Anticipatory Vibrotactile Cueing Facilitates Grip
Force Adjustment during Perturbative Loading
Shogo Okamoto, Michael Wiertlewski, and Vincent Hayward, Fellow, IEEE
Abstract—Grip force applied to an object held between the thumb and index finger is automatically and unconsciously adjusted upon
perception of an external disturbance to the object. Typically, this adjustment occurs within approximately 100 ms. Here, weinvestigated the effect of anticipatory vibrotactile cues prior to a perturbative force, which the central nervous system may use for rapid
grip re-stabilization. We asked participants to grip and hold an instrumented, actuated handle between the thumb and index finger.
Under computer control, the handle could suddenly be pulled away from a static grip and could independently provide vibration to thegripping fingers. The mean latency of corrective motor action was 139 ms. When vibrotactile stimulation was applied 50 ms before
application of tractive force, the latency was reduced to 117 ms, whereas the mean latency of the conscious response to vibrotactile
stimuli alone was 229 ms. This suggests that vibrotactile stimulation can influence reflex-like actions. We also examined the effects ofanticipatory cues using a set of perturbative loads with different rising rates. As expected, facilitation of grip force adjustment wasobserved for moderate loads. In contrast, anticipatory cues had an insignificant effect on rapid loads that evoked an adjustment within
60-80 ms, which approaches the minimum latency of human grip adjustment. Understanding the facilitative effects of anticipatory cueson human reactive grip can aid the development of human-machine interfaces to enhance human behavior.
Index Terms—Grip force adjustment, vibrotactile stimulus, asynchronous cuesÇ
1

INTRODUCTIONW

HEN manipulating an object, humans adjust grip
forces in a largely unconscious manner [1]. In thecase of rapid, unexpected loading or unloading to the object,grip forces are automatically adjusted to stabilize the grip or
to avoid overly large grip forces. Mechanoreceptors in theskin, tendons, and muscles contribute to an economical andsecure grip via spinal and supraspinal sensorimotor circuitsthat operate at different levels of the nervous system [2]. Cutaneous mechanoreceptors play a particularly important role inthis, as demonstrated by the observation that digital anesthesia significantly reduces corrective prehensile behavior [3],[4], [5]. During anesthesia, grip forces tend to exceed the minimum required force [2], [6], [7], [8], [9] as a consequence of astrategic change in motor control and compensatory behaviors. A loss of economic grip is also observed when tactile sensitivity is weakened as a result of wearing gloves [10] or
during robotic telemanipulation [11]. Furthermore, vibrotactile stimulation of the finger pads, when synchronized withsudden loading, can promote grip force adjustment [12].
These findings indicate that cutaneous inputs provide early
warning signals in advance of grip failure. In the field of
robotics, grip force control that is based on early signalingS. Okamoto is with the Department of Mechanical Science and Engineering,
Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Japan.
E-mail: okamoto-shogo@mech.nagoya-u.ac.jp.
 M. Wiertlewski is with ISM, Aix-Marseille Universite, CNRS, ISM
UMR 7287, 13288, Marseille CEDEX 09, France.
E-mail: michael.wiertlewski@univ-amu.fr.
 V. Hayward is with Sorbonne Universites, UPMC Univ Paris 06, UMR
7222, ISIR, 75005, Paris, France. E-mail: vincent.hayward@isir.upmc.fr.
Manuscript received 3 Apr. 2015; revised 14 Jan. 2016; accepted 31 Jan. 2016.
Date of publication 8 Feb. 2016; date of current version 15 June 2016.
Recommended for acceptance by M. Santello.
For information on obtaining reprints of this article, please send e-mail to:
reprints@ieee.org, and reference the Digital Object Identifier below.
Digital Object Identifier no. 10.1109/TOH.2016.2526613

via artificial skin sensors is successful due to the sensitive
response to variations in contact status that result from thelow mechanical impedance of soft artificial skin [13], [14],[15], [16], [17], [18], [19].
In this study, we tested the potential for facilitation ofgrip force adjustment, taking advantage of cutaneous stimuli as early predictive signals, specifically, a vibratory cue
that stimulated finger pads in advance of abrupt loading. In
the first experiment, we demonstrated that vibrotactile cutaneous stimuli reduce the latency of adjustment. These
results were based on previous work [20], where we also
discussed the temporal relationship between the deformation of finger pads and grip force during loading. In the second experiment, we showed that the anticipatory effect ofvibrotactile stimuli varied with the degree of external perturbation. Although previous studies have investigated theeffects of a vibrotactile cue presented simultaneously withthe load [12], [21], the present study focuses on the effects ofvibrotactile cues that precede loading.

2

EXPERIMENTAL APPARATUS

The testing procedures and materials were approved by the“Comite de protection des personnes Ile-de-France II” permit 2011-06-16 (IRB registration 1,072). Fig. 1 shows theexperimental apparatus. The main component was an
instrumented grip handle, held by a thumb and index finger, and driven by two gear-less DC motors (2642W012CR,
Faulhaber, Germany) through a differential capstan mechanism. The two motors were driven by a current driver (4-QDC Servo Amplifier, Maxon, Switzerland) and mechanicallyconnected in parallel to provide additional torque. Use of afree idler as a tensioner enabled the application of a large
torque with only a small loss to friction [22]. The systemprovided a stalling force of 20 N with a loss of less than

1939-1412 ß 2016 IEEE. Personal use is permitted, but republication/redistribution requires IEEE permission.
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for detecting the slippage of grip, which constitutes a failureof adjustment.

3

EXPERIMENT 1: DO ANTICIPATORYVIBROTACTILE STIMULI FACILITATE GRIP
ADJUSTMENT?

3.1 Tasks and Instructions
Five naive participants were included in the experiment.
They were right-handed men (mean age, 31.2 years), andwere free of self-reported neural and tactile disabilities.
Each participant sat on a chair and held the grip handle
with his index finger and thumb in a relaxed manner. The
grip force used to hold the handle was not specifically controlled, and individual mean values were within 3.1-5.3 N,with standard deviations of 0.66-1.0 N. The participant was
requested to maintain a natural grip under the force of gravity. In addition, participants were instructed “not to let go of
the handle” and to “try to respond to the vibration as
quickly as possible.” After each trial, participants released
the handle and relaxed. During each trial, participants
closed their eyes and wore headphones playing pink noise
to conceal sounds emitted by the vibrotactile actuators. The
noise level was adjusted for each participant, such that noneof the sounds made by the equipment, including vibratory
stimuli and loading stimulus, could be heard when the participants did not hold the grip handle.
Fig. 1. Apparatus used, including the instrumented grip handle and apulling mechanism. a. Overall view. b. Differential capstan drive with two
DC motors. c. Side view of the grip handle. d. Perspective view of thegrip handle.

0.1 N. The position of the handle was measured with apotentiometer (BTIV 24S 16.24 K, Baumer, Switzerland, resolution: 0.0146 mm). Data sampling and commands to the
DC motor were attained using a data acquisition card
(DAQ, PCI-6221, National Instruments, Austin, TX) at a rateof 10 kHz.
We installed three high-precision load cells on the handle
as follows. Two force sensors (9313AA1, Kistler Instrumente
AG, Winterthur, Switzerland) were located in load paths
between the two main plates to measure the normal grip
force component. Another load cell (9217A, Kistler Instrumente AG) measured the tangential component of the grip
force. The normal force action on the lateral sensor was
decoupled via a leaf-suspension mechanism. Each finger
contacted a finely polished plastic surface embedded oneach plate. The same instrument was also used previously
to investigate the effect of slip-induced skin vibrations ongrip adjustment [23].
Two recoil type actuators (Haptuator Mark 2, TactileLabs, Deux-Montagnes, Canada) were used to vibrate thehandle. These were placed orthogonally to the load paths of
the force sensors such that they would not interfere with theforce measurement.
We also used two accelerometers to measure the net
deformation of the fingerpad due to the tractive force, aspreviously described [20]. One accelerometer was mounted
on the nail of an index finger and another on the grip handle. In the present study, these accelerometers were used

3.2 Stimuli
3.2.1 Time Sequence and Magnitudes of Traction
and Vibrotactile Stimuli
In each trial, after a random delay of 2-5 s, an impulsive
force command was sent to the DC motor, and the grip handle was accelerated upward. As a result, the load experienced by the hand of the participant abruptly increased, as
shown in Fig. 2A.
Although the time response of this interaction force
depended on the dynamics of the human hand and capstan
mechanism, the mean and standard deviation of the peak of
the load increase for all trials were 2.9  0.81 N, which wasobserved 195  51 ms after the onset of the motor command.
Hence, the mean increase in the rate of traction was 15.0 N/s.
The time at which the load increase reached 10 percent of thepeak value of traction was fairly stable (29  4.8 ms). These
conditions were selected through preliminary trials suchthat they would successfully induce grip adjustment formost people. Under certain test conditions, a vibratory stimulus was applied to the index finger and thumb of the participant. Its magnitude was set to 10 m/s2 , which corresponds
to 4 and 25 mm in displacement at 250 and 100 Hz,
respectively.
3.2.2 Stimulus Conditions
We tested four types of conditions (with one control condition) that differed in traction and vibration. In a training session, each participant experienced these four conditions
only once. In the main task, 40 trials, in which the following
four conditions appeared in random order, were performed
with each condition presented 10 times.

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predominantly FA I units that detect local slippage and are
responsible for grip adjustment [25]. We attempted to gain
greater insight into this matter; the use of 250 Hz was
intended to activate FA II units preferentially, whereas thelower frequency, 100 Hz, was intended to activate both FA I
and FA II units. The magnitude of our vibratory stimuli was
sufficiently large to activate these receptors in terms of theirdetection thresholds, which are below 1 mm for FA II at 100250 Hz, and below 10 mm for FA I at 100 Hz [26].

Fig. 2. Time course of the loading stimulus, vibrotactile stimulus, grip
response, and net grip handle displacement. A: Tractive loading force
typically reached a maximum at 130 ms after the torque command to themotors. B: Vibrotactile stimulus. C and D: Grip force response and grip
rate. E: Net displacement of the grip handle, which reached a maximum
at a different time from the load, due to the complex biomechanicaldynamics coupled to the dynamics of the motor/handle subsystem.

Condition 1: Load only. Traction was abruptly produced
without the preceding vibrotactile cue.
Condition 2: Vibration (250 Hz) only. A vibration of 250 Hz
was presented without subsequent traction. This condition
was aimed to measure voluntary reactions to the vibration.
Condition 3: Vibration plus load (250 Hz). The anticipatory
vibration of 250 Hz lasted 50 ms and then the tractive force
was initiated. This condition aimed to determine the influence of the preceding vibration on grip force adjustment.
Condition 4: Vibration plus load (100 Hz). This condition
was the same as condition 3, except for the frequency ofvibration (100 Hz). The aim was to determine if vibration
frequency influenced grip force adjustment, given the likely
contribution of fast adaptive mechanoreceptors.
Condition 5: Vibration (250 Hz) only. After all the trials ofconditions 1-4, we repeatedly tested condition 2 10 times tomeasure the delay in voluntary reaction toward the vibration in a more controlled manner. During this follow-up
test, the participant was informed that only the vibration
would be presented, and was instructed to respond to it as
quickly as possible.
As described above, we tested two types of vibration frequencies: 100 and 250 Hz. It has been shown that neurophysiologically that the two types of fast adaptive units, FA I and
FA II, respond to incipient slippage in the finger-object contact
area [24]. However, FA II units do not localize partial slippage
because of their large receptive fields, although they exhibit
high dynamic sensitivity [24]. Some studies suggest that it is

3.3 Data Analysis
Fig. 2 shows representative time courses for the dataacquired from a single trial. They include (A) traction
applied to the handle, (B) the vibrotactile cue, (C) grip force
response, (D) grip force rate, and (E) displacement of thehandle. The onset of grip force adjustment was observed
approximately 100 ms after the onset of the traction instruction, which is noted as t ¼ 0. Based on these data, wedefined the four parameters that are described in Sections
3.3.1-3.3.4 for each trial.
Some trials were excluded from the analysis. First, the trials for which the increase in grip force was not clearlyobserved with a 20 N/s threshold were not included in theanalysis. For most of these trials, the effect of perturbative
load was mitigated by the reflective motions of the handand arm, rather than by the increase in grip force. Second,
we excluded trials that involved full slippage of the fingerpad. Grip slippage rarely happened; at most, in two trials
per participant. The occurrence of slippage was judged
based on the outputs from the two accelerometers. If theshort-period (200 ms) integral of the difference between the
two accelerometers exceeded 10 mm, which far exceeds
the deformation of the fingerpad, we judged that slippage
had occurred. Nonetheless, in most cases, the occurrence ofslippage was noticeable for both the participant and theexperimenter. These erroneous or irregular trials wereobserved for all stimulus conditions and constituted only
7 percent of all trials. Since no control condition was used, it
is not known whether the vibrotactile cueing induced or
prevented these erroneous trials.
The data from the four parameters were then separatelypooled, and for each parameter, the largest and smallest values were automatically excluded within a single participant,and the remaining values were used for statistical analysis.
After removal of these outlier samples, 30, 29, 30, 31, and29 trials were considered for P1-P5, respectively, in the statistical analysis. Note that this process implied that the analyses of each of the different parameters were based on datafrom slightly different sets of trials. We therefore repeatedthe analysis on a trial-by-trial basis, and eliminated the trials
with the longest and shortest delay in the grip force adjustment. Using this coupled approach to outlier rejection, we
nevertheless arrived at the same statistical conclusions foranalysis of each of the four parameters.
We performed two-way ANOVA for each type of parameter, using the 4-level experimental conditions and participants as factors. Because we were mainly interested indifferences between condition 1 and conditions 3 and 4, we
also tested these two pairs, with Bonferroni correction, via
two-way ANOVA. Furthermore, in order to investigate
the effect of voluntary reaction to the vibratory stimuli,

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condition 2 was compared with conditions 3 and 4. For thisanalysis, we used six samples that were randomly selected
in terms of the combination of participant and experimental
condition, because the number of valid samples differedamong the combinations. Hence, 120 samples (six samples
 five participants  four conditions) were used for the
analysis of each parameter.

3.3.1 Latency of Grip Force Adjustment
For conditions 1, 3, and 4, the delay in grip force adjustment
was defined as the time period between the onset of theload instruction to the DC motor and the start of the change
in grip forces. For conditions 3 and 4, the instruction to themotor began at the end of the period of the vibratory stimulus, as described above. For conditions 2 and 5, the delay
was defined as the period from the end of the vibratory
stimulus. These definitions enabled us to compare delays
under different stimulus conditions on the same temporalbaseline. To determine the onset of grip adjustment, we
computed first-order derivatives of the grip force after
applying a FFT filter with a cut-off frequency of 100 Hz. An
example of the computed grip force rate is shown in
Fig. 2 D. The increase in grip force was judged with athreshold of 20 N/s, which was two to three times the levelof background noise.
3.3.2 Change in Grip Force
The increase in grip force was calculated as the difference
between the maximum force after onset of the tractive force
and the average of a 100-ms period before traction started
or vibration ended. Although the vibration caused a brief
noise upon the output from the force sensor, this did not
produce any systematic bias. For this calculation, the lowpass filter above described was used. The magnitude of thegrip force is directly associated with grip stability and has
been used as a parameter to characterize grip adjustment inearlier related studies [27], [28].
3.3.3 Rate of Increase in Grip Force
After the start of grip adjustment, the grip force reached its
maximum value within approximately 200 ms, which was
300 ms after the onset of the tractive load. The rate ofincrease in the grip force was defined by the maximum grip
force increase from commencement of the adjustment to thepoint of maximal grip force. This parameter also characterizes human adjustive behaviors.
3.3.4 Handle Displacement
Handle displacement was defined as the difference between
the highest position of the handle after traction and theaverage position recorded over the last 100 ms prior to thestart of traction. The position of the handle was calculated
directly from the output of the encoder, without the use offilters. A small handle displacement was considered as indicating a successful response to the perturbation. As discussed below, handle displacement corresponded to thechange in posture of the hand and arm, as we excluded trials with apparent slippage.

Fig. 3. Latency between pulling force and grip force adjustment. Means
and standard deviations among trials. For condition 2, latency was measured from the end of the vibratory stimulus. For conditions 1, 3, and 4,
latencies were measured from load onset. Top panel: All trials. Bottom
panel: Trials for participants P1-P5. Markers corresponding to conditions
1-4 are indicated from left to right for participants. ***: p < 0:001 by
ANOVA between two conditions.

3.4 Results
3.4.1 Latency of Grip Force Adjustment
Fig. 3 (top) and Table 1 show the means and standard deviations for the latency in grip force adjustment in each stimulus condition. Fig. 3 (bottom) shows the distribution ofindividual latencies. The latencies of adjustment were significantly longer for the vibration-only condition (condition
2). The mean latency for this condition was 229 ms from theend of the vibration, which corresponds to 279 ms from theonset of the vibratory cue. Lower latencies than in condition 2 were observed in the load-only condition (condition
1: 139 ms) and vibration plus load conditions (conditions 3
and 4: 116 and 117 ms from load onset, respectively). As
seen in Table 1, the grip force changes did not differ significantly among the conditions.
The effects of both the experimental condition (F ð3;100Þ ¼ 143:9, p < 0:001) and participant (F ð4; 100Þ ¼ 51:2,
p < 0:001) were indicated as significant factors in two-way
ANOVA of data of all conditions and participants. The comparison between condition 1 and conditions 3 and 4 indicated that the latencies of condition 1 were significantly
larger than those of conditions 3 (F ð1; 50Þ ¼ 61:4, p < 0:001)
and 4 (F ð1; 50Þ ¼ 48:4, p < 0:001). Furthermore, the comparison between condition 2 and conditions 3 and 4 indicatedthat the latencies of condition 2 were larger than those of

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TABLE 1Means and Standard Deviations of the Grip Adjustment Parameters among All Trials in All Participants

Condition

1 (load only)
2 (vibration only)
3 (load + vibration)
4 (load + vibration)

Latency[ms]

Grip increase[N]

Grip increase
rate [N/s]

Handle disp.
[mm]

Time formax. grip [ms]139  30229  97
116  23117  24

8:76  4:21
9:11  4:52
9:91  4:55
10:5  4:88

47:6  25:4
51:8  17:7
49:8  19:3
54:9  22:5

32:4  17:0–
32:0  15:0
30:5  13:8

352  82419  124
319  64315  59

conditions 3 (F ð1; 50Þ ¼ 195:8, p < 0:001) and 4 (F ð1; 50Þ ¼
186:4, p < 0:001). As shown in Fig. 3 (bottom), these trends
were observed in most of the participants.
To summarize these results, latencies under vibration plus
load conditions (conditions 3 and 4) were lower than thoseunder the load-only (condition 1) and vibration-only (condition 2) conditions. From the onset of the vibratory stimuli, theaverage response to the vibration was 279 ms (condition 2) or
222 ms (condition 5), whereas the responses to the vibration
plus load were 166 ms (condition 3) and 167 ms (condition 4).
Hence, latencies were significantly reduced in the vibration
plus load conditions. These values indicate that the reduced
latencies in the vibration plus load conditions were not due tovoluntary responses to the vibration, but that the preceding
stimuli themselves influenced grip force adjustment.
To check for learning effects during the trial, we also compared the latencies for the first and second halves of the trials
for each participant, but found no significant learning effects.
Table 1 also lists the mean time at which maximum grip
forces were observed. These values show trends similar to
those of the latencies. Maximum grip forces were observed
latest for condition 2 with a mean value of 419 ms. The values for conditions 3 and 4 tended to be smaller than that forcondition 1 which indicates that the latency of adjustment
influences the subsequent dynamics of the adjustment.
Participant 3 responded to the tractions under all stimulus
conditions more quickly than the other participants. This may
be partly because this individual’s force increase was 16.6 N
on average, which was greater than those of the other participants: 10.2 (P1), 4.4 (P2), 7.7 (P4), and 9.5 N (P1). Accordingly,
the average force increase rate of P3, which was 68.6 N/s, wasgreater than those of the others: 52.7 (P1), 34.4 (P2), 45.0 (P4),
and 55.2 N/s (P5). Since latency was defined based on theonset of the force increase, such a large grip force increase
may have led to the relatively smaller latencies seen for P3.

3.4.2 Change in Grip Force and Handle Displacement
Table 1 shows the means and standard deviations for theincrease in grip force for each stimulus condition. In termsof changes in grip force, there was no statistical difference
between the conditions; although there was a weak trend
for the preceding vibration to lead to a larger increase ingrip force, this was observed in only three of the five participants (P1-P3). Moreover, in the second experiment,
described below, vibration had no effect on grip force.
Therefore, no conclusions could be reached regarding theeffect of preceding vibration on any potential changes ingrip force. Although the increase in grip force and speed ofgrip force adjustment were correlated in earlier studies [27],[29], our results suggest they are not necessarily associated.
Such a difference between our results and those of earlier

studies may be due to the different profiles of tractive loads
used, as earlier studies used stepping or trapezoidal loads,
whereas we employed impulsive loads in this study.
Table 1 also shows the means and standard deviations
for handle displacement and the rate of increase in grip
force for each condition. There were no clear differencesamong the conditions.
Although the latency of grip adjustment, handle displacement, and grip force are dynamically linked, no correlations were observed. This may be because the variationsin handle displacement are also influenced by elbow andshoulder joints, and are not merely determined by correction of prehension.

3.4.3 Representative Time Course
Fig. 4 shows the mean time course of grip adjustment for
one participant (P5). All data were averaged while referring to each trial’s temporal origin. As described above,
grip forces most rapidly responded under the vibration
plus load conditions (conditions 3 and 4), followed by theload condition (condition 1) and the vibration condition(condition 2). In terms of the increase in grip force andhandle displacement, although there were no statisticaldifferences among all the participants, for participant 5
the vibration plus load conditions (conditions 3 and 4)

Fig. 4. Average results of one participant. Top panel: Grip force. Middle
panel: Derivative of grip force. Bottom panel: Position of the grip handle.
Condition 1: Load stimulus only. Condition 2: Vibrotactile stimulus only.
Condition 3: Load + vibrotactile stimuli (250 Hz). Condition 4: Load +vibrotactile stimuli (100 Hz).

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appeared greater than or at least equal to the load condition (condition 1).

3.5 Summary and Discussion of Experiment 1
In the above experiment, the average latency in grip force
adjustment toward the perturbative load was 139  30 ms(condition 1). This value was consistent with those of earlier studies [1], [4], [4], [27], which suggested that thedelay may vary over a wide range (60 to 170 ms), depending on the characteristics of the loads and experimental
conditions. When the average latency toward the load
was 139 ms, the use of the anticipatory vibrotactile stimulus reduced adjustment response times by 22-23 ms to
116 or 117 ms.
Mrotek et al. [28] suggested that preparatory activities
of muscles and cutaneous mechanical receptors may facilitate grip force adjustment. They compared grip force
adjustments during static holding as well as active liftingof an object, and found lower latencies in the active lifting
condition. Notably, pre-activated muscles potentially
increase motor responses [30], [31]. Mrotek et al. also
noted that pre-activated cutaneous receptors may reduce
adjustment latencies. Because of inertia, fingers receive
larger loads and cutaneous receptors are more highly
stimulated while lifting an object than in the static holding condition. Our results are consistent with those of
Mrotek et al., with the exception that we stimulated cutaneous receptors using vibratory stimuli rather than inertia
forces, which also led to faster response times.
No significant differences in adjustment parameters,
including response latency and changes in grip force, wereobserved between conditions 3 and 4, in which different
vibratory frequencies were presented, although we had
expected some effects of frequency based on differing frequency characteristics between different classes of mechanoreceptors. Despite the absence of vibration frequency
effects, it is not possible to draw any conclusions regarding
relationships between receptor classes and grip force adjustment, given the strong vibratory stimuli used in our
experiments.

4

EXPERIMENT 2: IS THE ADJUSTMENT IN GRIPFORCE DURING RAPID LOADING ENHANCED BY
ANTICIPATORY VIBROTACTILE CUES?

In Experiment 1, anticipatory tactile cues reduced
response latencies by 20 ms, from 139 to 119 ms. Thisfinding prompted us to ask whether a delay of approximately 60 ms shortest value reported in the literature [4],[27], can be reduced by an anticipatory cue? In Experiment 2, we investigated the effects of anticipatory cues
when a faster tractive force was applied to the handle.

4.1 Stimuli and Tasks
The presence of an anticipatory vibrotactile cue and therate of increase in traction were the two stimulus parameters examined in Experiment 2. Fig. 5 shows the five load
forces. The rates of these loads were greater than thoseused in Experiment 1, and their peak forces were approximately 3 N. Peak loads were separated by approximately
30 ms. The frequency, amplitude, and duration of theFig. 5. Averages of the five types of traction increases seen in one participant. Each condition reaches a peak load at a different loading rate. The
average and standard deviation of the peak load, time at which the peak
was observed, the time to reach 10 percent of the peak, and the risingrate for each type of traction among all the participants were as follows.
Traction 1: 3.1  0.35 N, 95  0.7 ms, 28  1.7 ms, and 32.4 N/s; Traction 2: 2.9  0.39 N, 115  0.6 ms, 37  3.5 ms, and 25.7 N/s; Traction
3: 3.2  0.39 N, 146  1.8 ms, 52  4.0 ms, and 22.0 N/s; Traction 4:
3.3  0.59 N, 172  0.8 ms, 65  6.2 ms, and 19.4 N/s; and Traction 5:
3.5  0.44 N, 200  11.3 ms, 75  6.0 ms, and 17.4 N/s, respectively.
Traction 1 was the most rapid, and Traction 5 was the slowest.

vibrotactile stimuli were the same as those in the previous
experiment (250 Hz, 50 ms before traction onset). Tenconditions (with/without vibrotactile stimuli  five typesof load) were tested in a random order in each set, and10 sets were performed by each participant.
The five participants from the previous experiment were
included in the second experiment, which was performed
on a different day, together with one additional righthanded female participant in her 20 s. The procedures andexperimental apparatus were the same as those used inExperiment 1.

4.2 Data Analysis
We analyzed the data in a similar manner as for Experiment
1. In order to test the general effects of the traction level andvibration on grip adjustment, we conducted a three-way
ANOVA on each type of parameter, with the level of traction, the presence of vibration, and participants as the threefactors included. For each combination, eight valid samples
were used, hence in total 480 samples (five traction levels 
two vibration mode  six participants  eight samples)
were analyzed. In order to investigate the potential dependence of the effect of vibration on the traction level, we also
tested the effect of vibration for each traction level by a twoway ANOVA, with the presence of vibration and participants included as the two factors.
Finally, to compare the effects of vibration among thetraction levels directly, we calculated the differences oflatencies between the conditions with and those without
vibration, for each traction level. Each difference was calculated using the two samples in the same set of experimental tasks. Hence, all the samples from the 10 sets
were used for this purpose. The number of data points
was 300 (five traction levels  six participants  10 differences). We then compared the differences in latencies
among the traction levels using two-way ANOVA, withthe traction levels and participants as factors. Twoamong the five traction levels were repeatedly tested(10 comparisons), with adjustment of the significancelevels by Bonferroni correction.

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TABLE 2Means and Standard Deviations of Latencies fromthe Onset of the Tractive Force
Traction level

Without vib. [ms]With vib. [ms]65  1779  1699  20113  19125  2165  1677  1794  18108  17118  1512345Abbreviation: vib., vibration.

cues appear to induce the best possible human response
performance, rather than exceed it.
Fig. 6. Latency in grip force adjustment. Means and standard deviationsof each condition are shown. Filled bars are from load onset. Open bars
are from the onset of vibratory stimuli. **: p < 0:01 by two-way ANOVA
that tests the effect of vibration for each traction level.

4.3

Results: Latency to Different Degrees ofTractive Force
Fig. 6 and Table 2 show the mean and standard deviationof the adjustment latency for each condition. Latencies
reduced as the tractive load rates increased, and thistrend was consistent with a previous report [27], where
the latencies varied with the magnitude and rate of traction. The three-way ANOVA indicated that the level oftraction (F ð4; 420Þ ¼ 599:6, p < 0:001), the presence ofvibration (F ð1; 420Þ ¼ 25:2, p < 0:001), and the participant (F ð5; 420Þ ¼ 237:7, p < 0:001) were significant factors. Two-way ANOVAs for each traction level suggested
significant effects of vibration for traction 5 (F ð1; 84Þ ¼
10:9, p < 0:01), traction 4 (F ð1; 84Þ ¼ 7:2, p < 0:01), andtraction 3 (F ð1; 84Þ ¼ 8:3, p < 0:01). For the two most rapid
levels of traction, no significant effect of vibration wasobserved. The reduction in latencies due to vibration was significantly larger for traction levels 5, 4, and 3, than for traction levels 2 and 1. The effects of vibrations for level 5 werelarger than those for levels 2 (F ð1; 108Þ ¼ 53:1, p < 0:001)
and 1 (F ð1; 108Þ ¼ 20:6, p < 0:001). Similarly, those for levels 4 (F ð1; 108Þ ¼ 21:6, p < 0:001) and 3 (F ð1; 108Þ ¼ 30:9;
p < 0:001) were larger than those for level 1.
We also tested the effects of vibration on other parameters;
however, vibration had no significant effect on grip force or
handle displacement, similar to the findings of Experiment 1.
4.4 Summary and Discussion of Experiment 2
The minimum delay observed in the experiment was 65.3 
17 ms for traction 1 (32.4 N/s, the maximum rate) in theabsence of vibration, which is comparable to the minimum
values obtained in earlier studies in humans (ca. 60 ms) [1],[4], [24], [27]. This minimum delay may be associated withthe shortest neural path, which begins at sensory inputs
evoked by cutaneous deformation and changes in the lengthof muscles and tendons of the hand and ends at the musculoskeletal response to motor instructions transmitted
through spinal or supraspinal circuits. The anticipatory
vibrotactile cue was effective for moderate perturbative
loads, while no significant effect was observed for rapid
loads, for which the average response was shorter than thatof the moderate perturbation. Thus, anticipatory vibrotactile

5

GENERAL DISCUSSION

The tactile afferents at the fingertip are responsible for thepartial slippage associated with an increase in the load tothe gripped object, and allow us to adjust grip forces largely
unconsciously before the object slips out of the hand [1],[24]. Partial slippage within the finger-object contact area
predicts subsequent full slippage. Our experiments indicatethat further anticipatory vibrotactile cueing, which starts
before loading, facilitates a correction in grip force. Here,
we discuss the possible effects of anticipatory vibrotactile
cues from two angles: facilitation of perception and muscle
activity, which are not necessarily mutually exclusive.

5.1 Facilitation of Perception via Vibrotactile Cueing
A number of studies have investigated the possibility offacilitating human motor responses by using multiple synchronous or asynchronous sensory cues [32], [33], [34], [35],[36]. Most previous studies used visual or auditory cues;
however, in studies of tactile cues, an electric stimulus thatpreceded the subsequent cue by 20-80 ms was found to
decrease human response times to the second stimulus inboth a simple reaction task [37] and in an identification
task [38]. One classical explanation of such phenomenon is
the independent race model [36]. In this model, multiple
signals from different channels are processed separately,
and the human response depends on which of these aredetected first. This hypothesis can be discussed by examining joint probabilistic variables.
Let latencies to vibrotactile and loading stimuli beprobabilistic variables following a Gaussian distribution,
respectively, Xv  Nðmv ; s 2v Þ and Xl  Nðml ; s 2l Þ, of which
population parameters follow the results of Experiment 1.
The response to the vibrotactile cue plus load would follow Xvþl  Nðmvþl ; s 2vþl Þ. The temporal baseline of thesevariables is shown in Fig. 7. The lower of the two latencies is expressed by Y ¼ minðXv ; Xl Þ. By definition, thecenter of the distribution of Y is smaller than those of Xv
and Xl . The probability density function of Y is determined by the following equation:pðyÞ ¼ pðxv ; xv < xl Þ þ pðxl ; xl < xv Þ
¼ pðxv Þpðxv < xl jxv Þ þ pðxl Þpðxl < xv jxl Þ¼ pðxv Þð1  Pl ðxv ÞÞ þ pðxl Þð1  Pv ðxl ÞÞ:(1)

Where Pv ðÞ and Pl ðÞ are the distribution functions of Xv
and Xl , respectively. Since Y no longer follows a Gaussian

240

Fig. 7. Probability densities of response latencies in two participants: P3
and P5. Xv , Xl , and Xvþl are the responses to the vibrotactile stimulus,load, and load with vibrotactile stimuli, respectively. Y is the density function estimated by the independent race model. For both the participants,Xvþl (observed) does not match Y (race model).

distribution, it is not expressed parametrically. Fig. 7 shows
examples of density functions of Y for P3 and P5, of whom
the population parameters were, respectively, (mv , s v , ml , s l ,mvþl , s vþl ) = (91, 21, 113, 5.5, 83, 12) and (231, 93, 147, 29, 128,19), in ms. The peak density of Y shifted slightly to the left ofthat of Xl ; however, the joint effect of Xv on Xl did not allow
Y to approximate the distribution of Xvþl . Clearly, Y andXvþl do not match for both the participants, and the observed
facilitation in the experiment is not consistent with the independent race model. For the other participants, the distributions of Y and Xvþl were less similar than those of P3 and P5.
Other representative models include the co-activation
model or the energy summation model, in which sensory
activations are summed across multiple sensory channels [34], [35], [36]. The independent race model andthese models are not mutually exclusive [33]; however,since the race model does not fit our data, the energy
summation model may be useful for interpreting our
results. Unfortunately, our experiments did not provide
data for exact validation of this model. Furthermore, thetwo-channel theory of perceptual masking [39] may also
be relevant to our observations. According to this theory,human responses to stimuli are collectively mediated bytransient (fast adaptive) and sustained (slow adaptive)
information processes. A weak anticipatory stimulus activates the slow adaptive process and biases the detectionof the following rapid stimulus, which decreases reaction
times to the latter stimulus.

5.2

Anticipatory Cues May Enhance Motor
Preparation or the Cutaneous-Motor Reflex
Although we discussed the possibility that anticipatory cues
may enhance the perception of traction-associated stimuli,
vibrotactile stimuli may also facilitate motor preparation.
First, it remains possible that the facilitation of grip
adjustment observed in this study was due to a reflexive
flexion of fingers toward vibratory stimuli to the skin.
Eklund et al. [40] reported an involuntary increase in finger
flexion force caused by vibrotactile stimuli to the palmarside of the proximal interphalangeal joints. Their stimuli
were 0.5-1.0 mm in amplitude at 100 Hz, which werepotentially stronger than those used in our experiments.

IEEE TRANSACTIONS ON HAPTICS,

VOL. 9, NO. 2,

APRIL-JUNE 2016

They considered that these reflexive phenomena weremediated by mechanoreceptors in the skin, unlike a tonic
vibration reflex in which muscle spindles activated byvibrations evoke a reflexive motion, because full or partial
anesthesia of the finger led to a similar attenuation ofreflexive responses to the vibrations [40], which is consistent with the effects of digital anesthesia on grip force
adjustment [3], [4], [5]. Such an unconscious increase in finger flexion forces have also been reported in other studies [41]. Similar reflexive responses hold for finger
extension by electric or mechanical tapping stimuli to thedorsal skin [42], where excitatory and inhibitory reflexes
were alternately evoked approximately 40 ms after the
stimuli. Furthermore, the magnitudes of the vibrotactile
stimuli we used were comparable to those needed to activate sensitive muscle spindles by imposing a vibration on
the skin above the muscles [43]. Under the vibrotactile
stimulus conditions 2 and 5 in Experiment 1, we did notobserve such reflexive increases in grip forces. Nonetheless, in our experiment, the anticipatory vibrotactile stimuli
may have improved grip-associated muscle activity withina subthreshold level, which may have facilitated subsequent adjustive behaviors, whereas they did not induce
apparent reflexive increases in grip forces per se.
Another explanation for the facilitation of grip adjustment could be a preparatory modulation toward a subsequent stimulus by the supraspinal system. Rossetti
et al. [44], [45] and Imanaka et al. [37] argued that conscious detection of and motor preparation by cutaneous
stimuli are processed in a neurally parallel or dissociatedmanner to some degree, based on studies of motor
responses to perceptually masked tactile inputs and studies involving tactile and somatosensory tasks in patientswith brain disorders. For example, Imanaka et al. noted
the following features [37]. A weak first stimulus approximating threshold level is perceptually masked by a subsequent relatively strong stimulus; however, such an
unconscious first stimulus reduces response latencies incognitive and non-cognitive tasks [37], [38]. Cutaneous
inputs usually reach the somatosensory cortex in a few
tens of milliseconds [46], whereas the experience of perception arises 23-550 ms after stimulation [47], [48]. In a
study of grip adjustment in monkeys, reflex-like changes
in cerebellar cortical neurons appeared with an averagelatency of 36 ms after the onset of a perturbative load tothe gripped object [49]. These reports suggest that motor
preparation does not necessarily start after the cognitionof sensory stimuli, and that the stimulus may affect motor
responses before it is even consciously recognized [48].
Moreover, cutaneous reflexes are facilitated or inhibitedby supraspinal systems [50], [51], although grip force
adjustment is not considered a definite cutaneous reflex.
For example, magnetic stimulation of the motor cortex
promotes grip force adjustment [52] as well as the flexion
reflex of the lower leg during walking [51]. Furthermore,ablation of the cerebellum influences the withdrawal
reflex in response to cutaneous pain stimuli [50]. Collectively, these reports suggest that the supraspinal system
receives early warning stimuli (including vibrotactile
stimuli) to modulate reflexive behaviors to the subsequent
stimulus (tractive load).

OKAMOTO ET AL.: ANTICIPATORY VIBROTACTILE CUEING FACILITATES GRIP FORCE ADJUSTMENT DURING PERTURBATIVE LOADING

5.3

Possible Application of the Anticipatory
Vibrotactile Cueing
It is somewhat premature to apply the findings of this study
to practical problems; however, one possible application issuggested below. As previously described, a grip adjustment strategy using a sensor to detect incipient slippage ofa robotic finger [19], [53] has been implemented on several
robotic hands [13], [14], [15], [16], [17], [18]. In contrast,
anticipatory tactile cueing for facilitating grip adjustment
functions more effectively in humans. For example, a situation can be imagined where an object is held by an individual wearing a device that can present vibrotactile stimuli tothe hand. Upon detecting a risk that a perturbative load islikely to be applied to the held object, the vibrotactile device
can deliver anticipatory signals to the wearer to facilitate
grip adjustment in case the actual perturbation occurs. The
results of this study are expected to contribute to the designof such a warning system that can facilitate an action to
avoid risks as well as warn of upcoming risks.

6

CONCLUSIONS

Grip force adjustment is an intelligent human function that
does not require significant cognitive engagement. The
objective of this study was to demonstrate and determine
how this reflex-like movement may be facilitated. In particular, we focused on the effects of an anticipatory cue thatpreceded a perturbative tractive force, which triggered anadjustment for stabilizing the grip on a handle. Participants
were presented with a vibrotactile stimulus, via stimulators
mounted on the grip handle, 50 ms before the onset of the
tractive force. In other conditions, either tractive force orvibrations were presented alone. The participants attempted
to maintain their grip on the handle and respond to thevibration quickly. With the anticipatory vibrotactile cue, theadaptive behavior started on average 116 ms after the onsetof the tractive force. This latency was less than that in theabsence of the anticipatory cue (139 ms) and that of the voluntary response to vibratory signals alone (229 ms). This
indicated that the anticipatory cue itself likely facilitatedgrip adjustment, rather than a conscious perception of thevibration. Furthermore, such facilitation was not effective
under rapid perturbations that involved latencies of approximately 60-80 ms, which were comparable to those of theshortest latencies described in previous studies. Anticipatory signals reduced the latencies of adjustment when moderate perturbations were applied, and these moderate
perturbations evoked adjustments more slowly than did
rapid perturbations. Although MacIntyre and McComas [38]and Imanaka et al. [37] showed that anticipatory tactile cues
could facilitate motor responses in choice tasks or simple
reaction tasks, this study demonstrated that anticipatory
tactile cues also affect grip force adjustment. These adjustments were non-cognitive, automatic corrective actions.
Our findings will aid the development of robotic and rehabilitative applications for promoting and potentially
improving human reactive behaviors.

ACKNOWLEDGMENTS
The authors thank Prof. Yon Visell, Dr. Alexander Terekhov, Mr. Sheng-Chao Wong, Rafa» Pijewski, and Mark

241

Farrington for statistical, mechanical, and electronic supports and discussion. Also, this study was in part supported
by MEXT Institutional Program for Young Researcher Overseas Visits, KAKENHI 15K13908, and European ResearchCouncil, Advanced Grant PATCH, agreement No. 247300.
S. Okamoto is the corresponding author.

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Shogo Okamoto received the MS and PhD
degrees in information sciences in 2007 and2010, respectively, from the Graduate School ofInformation Sciences, Tohoku University. Since
2010, he has been an assistant professor in the
Graduate School of Engineering, Nagoya University. His research interests include haptics andhuman-assistive technology.

Michael Wiertlewski received the PhD degree
 Pierre et Marie Curie, in Paris,
from the Universite
France, under the auspices of the Commissariat
 l’Energie Atomique (CEA-LIST) in Fontenaya
aux-Roses, France. He has been a CNRS sinceresearcher at Aix-Marseille Universite
2014. Before he was a postdoctoral fellow at
Northwestern University in Evanston, IL, working
on the physics of ultrasonic friction reduction.
The results of his research have been awarded
with the Best thesis award from the French GdR
Robotique and from the Eurohaptics Society. His research interests
include the design of tactile interfaces, physics of the skin-surface interaction, and the perception of tactual textures.
Vincent Hayward received the Dr-Ing degree in1981 from the University de Paris XI. He was a
postdoctoral fellow then a visiting assistant professor in 1982 at Purdue University, and joined de Recherches in
CNRS, France, as Charge
1983. In 1989, he joined the Department of Electrical and Computer Engineering at McGill University as an assistant, associate, and then a full
professor in 2006. He was the director of the
McGill Center for Intelligent Machines from 2001
to 2004. From 2008 to 2011, he held the “Chaire Pierre et Marie Curie whereinternationale d’haptique” at the Universite
is he is now a professor. He is interested in haptic device design andapplications, perception, and robotics and published more than
80 articles in scientific journals as well as more than 150 articles in international conferences and collections. He cofounded spin-off companies
and received several best paper and research awards. He was on theeditorial boards of the IEEE Transactions on Robotics, the ACM Transaction on Applied Perception, and the IEEE Transactions on Haptics. He
is a fellow of the IEEE.
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