RESEARCH ARTICLE

Control of Precision Grip Force in Lifting and

Holding of Low-Mass Objects
Yuichi Hiramatsu1☯*, Daisuke Kimura1, Koji Kadota1, Taro Ito2, Hiroshi Kinoshita1☯
1 Department of Biomechanics and Motor Control, Graduate School of Medicine, Osaka University, Osaka,
Japan, 2 Department of Health and Sports Sciences, Mukogawa Women’s University, Hyogo, Japan

☯ These authors contributed equally to this work.

* [email protected]

Abstract
Few studies have investigated the control of grip force when manipulating an object with an
extremely small mass using a precision grip, although some related information has been
provided by studies conducted in an unusual microgravity environment. Grip-load force
coordination was examined while healthy adults (N = 17) held a moveable instrumented
apparatus with its mass changed between 6 g and 200 g in 14 steps, with its grip surface set
as either sandpaper or rayon. Additional measurements of grip-force-dependent finger-sur-
OPEN ACCESS face contact area and finger skin indentation, as well as a test of weight discrimination, were
Citation: Hiramatsu Y, Kimura D, Kadota K, Ito T, also performed. For each surface condition, the static grip force was modulated in parallel
Kinoshita H (2015) Control of Precision Grip Force in with load force while holding the object of a mass above 30 g. For objects with mass smaller
Lifting and Holding of Low-Mass Objects. PLoS ONE
than 30 g, on the other hand, the parallel relationship was changed, resulting in a progres-
10(9): e0138506. doi:10.1371/journal.pone.0138506
sive increase in grip-to-load force (GF/LF) ratio. The rayon had a higher GF/LF force ratio
Editor: Stefan Glasauer, Ludwig-Maximilian
across all mass levels. The proportion of safety margin in the static grip force and normal-
University, GERMANY
ized moment-to-moment variability of the static grip force were also elevated towards the
Received: December 25, 2014
lower end of the object mass for both surfaces. These findings indicate that the strategy of
Accepted: August 31, 2015 grip force control for holding objects with an extremely small mass differs from that with a
Published: September 16, 2015 mass above 30 g. The data for the contact area, skin indentation, and weight discrimination
Copyright: © 2015 Hiramatsu et al. This is an open suggest that a decreased level of cutaneous feedback signals from the finger pads could
access article distributed under the terms of the have played some role in a cost function in efficient grip force control with low-mass objects.
Creative Commons Attribution License, which permits The elevated grip force variability associated with signal-dependent and internal noises,
unrestricted use, distribution, and reproduction in any
and anticipated inertial force on the held object due to acceleration of the arm and hand,
medium, provided the original author and source are
credited. could also have contributed to the cost function.

Data Availability Statement: All relevant data are

within the paper.

Funding: H.K. was supported by the Japan Society

for the Promotion of Science KAKENHI (http://www.
jsps.go.jp/english/index.html) Grant Number
Introduction
23500675. The funders had no role in study design,
data collection and analysis, decision to publish, or Small objects are commonly manipulated using a precision grip with the tips of the index finger
preparation of the manuscript. and the thumb. During the past few decades, considerable effort has been devoted by research-
Competing Interests: The authors have declared ers in neuroscience to studying sensori-motor function involved in this simple mode of grip for
that no competing interests exist. lifting, holding, and transporting objects [1,2]. Researchers commonly used an instrumented

PLOS ONE | DOI:10.1371/journal.pone.0138506 September 16, 2015 1 / 19

 Prehension of Lightweight Objects

movable object, aiming to evaluate finger forces normal (grip force) and tangential (lift or load
force) to the grip surface, and in some cases tangential torques [3–5]. They found that the grip-
to-load force balance was automatically adjusted to a given finger-surface frictional condition.
The more slippery the grasping surface, the higher the ratio of grip force to load force (hereafter
denoted as the GF/LF ratio). They also showed that the grip force was composed of two com-
ponents: a voluntarily and/or reflexively adjusted excess force for preventing the object slipping
from the fingers, and a minimum required force (slip force) that could be determined by cur-
rent finger-surface friction. The excess force, namely, a grip’s safety margin force, appeared to
be set relatively small in healthy young adults (generally some 20–50% of the employed grip
force in healthy adults) over the range of frictional properties of the objects manipulated daily
[6–12]. Further studies using microneurography demonstrated that tactile afferent signals were
used primarily for the central nervous system (CNS) to adjust the safety margin [13,14]. CNS
also relies on feed-forward or anticipatory control of grip and load forces for the lifting of
objects. Visual information on an object’s properties, such as mass (or weight), density, and
friction, and sensory memory acquired in previous lifts are usually used in this process [15–
18].
The instrumented object used by the previous researchers for studying grasp stability com-
monly had a mass of a few hundred grams or more [5,7–9,12,18–28]. The effect of a small mass
(< 100 g) of the object in normal-gravity conditions on grip-load force coordination had thus
not been examined. Using a gravity-altered environment induced by parabolic flights, on the
other hand, researchers have recently explored finger force coordination while manipulating
an object under a weightless, normal, or double weight condition [24–28]. Hermsdorfers et al.
[26] reported that the grip force on an object held stationary by two relatively naive subjects
during a parabola was scaled to the weight of the object for normal- and high-gravity condi-
tions. However, during weightlessness, although no grip force was needed to stabilize the
object, the subjects exerted grip force of above 2.5 N on the object during the first flight, which
progressively decreased to about 0.9 N at the fifth trial. Hermsdorfers et al. [26] stated that this
excess grip force could be purely a safety margin in the event of possible perturbation. Creve-
coeur et al. [25] later showed that this margin could be further reduced to less than 0.4 N after
10 consecutive parabolic flights with increased time for adaptation to the unusual
microgravity.
Sensori-motor control of fingertip forces for handling low-mass objects (e.g., <50 g) in a
normal-gravity environment may differ in several ways from that for objects of a few hundred
grams or more that were commonly used in tests in previous studies. Firstly, the grip force
needed for holding such a low-mass object should be quite weak, limiting the finger-surface
contacting area, as well as the magnitude of skin deformation at the finger pad. This may also
confine tactile sensations required for fine adjustment of the safety margin. Psychophysical
studies of sensory thresholds also previously demonstrated that the relationship between the
difference threshold for intensity and the intensity level of a stimulus (Weber’s fraction)
increases at extremely low intensities of stimuli, including mass of a hand-held object [29,30],
and finger force or pressure [31]. In addition, a common finding from numerous studies of
reduced fingertip tactile sensibility is that individuals use a higher GF/LF ratio with an elevated
safety margin than normal or necessary [7,10,12,20,32–35]. We thus conjecture that, during
the manipulation of extremely light objects, individuals may have to use a strategy of finger
force control that is to some extent similar to that for the condition of decreased tactile
sensibility.
Secondly, a steady control of grip force at extremely low levels during holding of a light
object may be more centrally demanding due to a decreased signal-to-noise ratio than those at
moderate to high levels required for holding heavier objects. Studies of optimal control of

PLOS ONE | DOI:10.1371/journal.pone.0138506 September 16, 2015 2 / 19

 Prehension of Lightweight Objects

motor system have shown that Fitts’ law emerges from the presence of signal-dependent noise
(SDN) in motor commands, i.e. the noise whose variance scales in proportion to the magnitude
of motor command [36–38]. The central idea is that motor command is chosen to minimize
the negative effects or cost of SDN on task performance. The presence of SDN predicts that
fluctuations in grip force during the precision grip would be proportionally change across all
levels of grip force (intended motor command) generated. This, however, may not be true for
small force production. Studies on isometric force production against an immovable object
have demonstrated that the coefficient of variation (CV) value of generated force as an index of
normalized force fluctuations (i.e. a noise-to-signal ratio), is clearly raised towards the smaller
end of the level of force generated [39–43]. Thus, there seems to be an additional source of neu-
ral command that elevates motor output variability when the level of force manipulating is low.
During precision-grip holding of an object with a small grip force safety margin, if a proportion
of fluctuation in the grip force is increased, there can be increased risk of slipping and acciden-
tally dropping the held object, which can also be fear for the holder. This can be avoidable by
increasing a proportion of grip force safety margin, leading to a higher GF/LF ratio. Whether
this would be the case during holding of a low-mass movable object remains to be examined.
Thirdly, the magnitude of slip force can also be quite small for extremely light objects. Wes-
tling and Johansson [12] reported that the slip-to-load force ratio was fairly constant for a lifted
object weighing more than 100 g, following Amontons’ first law of friction. Tribological stud-
ies, on the other hand, have shown that, against a flat surface with varied materials, friction of
the human skin increased non-linearly with decreased normal force typically less than 0.5 N
applied to the skin [44,45]. It is thus quite reasonable to hypothesize that the GF/LF ratio can
be lowered with this frictional change while manipulating lighter objects with a small grip
force.
The present study was intended to test the above-mentioned hypotheses in a normal gravity
environment. To examine variables of grip-load force coordination, healthy adults lifted and
held a force-sensor-equipped movable object with a mass ranging from very small (6 g) to
moderate (200 g) for slippery (rayon) and non-slippery (sandpaper) surface conditions. To
examine the mass sensibility under the current experimental conditions, using an object with
the same dimensions and grip surfaces as those of the instrumented test object, a weight dis-
crimination test was also performed by the subjects. In addition, to facilitate the understanding
of cutaneous mechanoreceptors that could be involved in the present precision grip task,
changes in the finger-surface contact area and the finger pad indentation with grip force were
examined.

Materials and Methods

Ethics Statement
All participants gave written informed consent to participate in the study, and the study was
approved by the Ethics Committee of the Graduate School of Medicine, Osaka University (No.
11208) in accordance with the ethical standards established by the 1964 Declaration of
Helsinki.

Subjects
Eight females and nine males ranging in age from 18 to 30 years (mean age = 22.2 years) partic-
ipated in the present study. They were all healthy and right-hand-dominant, as determined by
the Edinburgh MRC Handedness Inventory [46]. None of them had a previous history of mus-
culoskeletal or neurological problems in the upper limbs. This study was approved by the

PLOS ONE | DOI:10.1371/journal.pone.0138506 September 16, 2015 3 / 19

 Prehension of Lightweight Objects

Ethics Committee of the Graduate School of Medicine, Osaka University, and informed con-
sent was obtained from all subjects.

Grip apparatus
The grip apparatus shown in Fig 1 consisted of three lightweight force transducers, thin flexible
electric wires, and a polystyrene cushion form at the bottom. It had a mass of 6 g and a height
of 60 mm. It was a size- and weight-reduced version of the apparatus introduced in earlier
studies (see details shown in [9], [10], [12]). The design for the arrangement of the force trans-
ducers was thus basically the same as those of the earlier studies. Briefly, the grip and load force
transducers had a double-end supported beam structure, and each of those had 4 strain gauges
to form a resistive Wheatstone bridge circuit. The force sensing beams were precision-
machine-cut from a 0.12-mm-thick steel plate (length: 32 mm). The supports for the beams
were pieces of small block cut from 3-mm-thick hard aircraft-grade (AG) plywood, which were
screwed using microscrews, and also glued firmly to both ends of the beam. For the grip force
transducer, a pair of grip surface plates made of 1.5-mm-thick hard AG plywood were also
firmly glued to the center of the beams. The grip force transducers allowed the separate mea-
surement of grip (normal) forces generated by the thumb and index finger when gripping the
apparatus. The distance between the two grip surfaces was 7.2 mm. For the load (lifting) force
transducer, the beam with end supports was firmly fixed to a base made of 2.5-mm-thick AG
plywood with a vertical AG plywood bar for reinforcement against a bending moment.
There were 8 electric wires from the grip apparatus, which consisted of 2 for electrical
power input and 6 for strain gauge signal output from the 3 force transducers. To balance the
mechanical effect of the wires, they were divided into both sides of the bottom of the grip appa-
ratus. Two types of electric wire were used in this study. The first type, a 20-cm extremely fine

Fig 1. The light grip apparatus and the experimental table. The apparatus contained three sensors to
measure grip and load forces.
doi:10.1371/journal.pone.0138506.g001

PLOS ONE | DOI:10.1371/journal.pone.0138506 September 16, 2015 4 / 19

 Prehension of Lightweight Objects

(diameter: 0.11 mm) insulated copper strain gauge lead cable, provided an initial connection
from the grip apparatus to relay terminals fixed on both sides of the experimental table (Fig 1).
The second type was ordinary shield electric wires for strain gauges, which provided a connec-
tion between the relay terminals and the Kyowa DPM-601 strain amplifiers. The first type of
cable was almost weightless (>0.01 g) and flexible, so that the effect of wire elasticity could be
minimized. As a preliminary study, using 3 subjects, we tested the effect of mechanical interfer-
ence caused by the first type of cable on low grip force while lifting the grip apparatus under
selected low-mass conditions (6 g, 10 g, and 22 g) with a sandpaper surface. To this end, we
removed 4 wires from among the original 8 wires while keeping one grip force transducer
active. Grip force data from this force transducer were compared for each subject who per-
formed a task of lift-to-hold for 10 sec before and after removing the wires. The mean static
grip force computed from data from 20 trials did not differ significantly between the 4- and
8-wire conditions in each mass condition for each subject, suggesting that the mechanical effect
of the electric wires connecting the apparatus and the relay terminals on the table would be
quite small or negligible. Static loading tests on each sensor revealed linearity up to 3 N with
force resolution of 0.001 N.
During the experiment, different levels of apparatus mass were created by hanging an addi-
tional mass from the bottom of the apparatus using a string. The grip apparatus was always
placed on an experimental table (height = 45 cm), which had a 4-cm-diameter hole in the cen-
ter, and through this hole, the additional mass was hung. The bottom of the table was covered
with pieces of wooden panel to hide the added mass from the subject’s view. Fourteen appara-
tus mass conditions: 6 (no additional mass), 8, 10, 14, 22, 30, 40, 50, 70, 90, 110, 130, 150, and
200 g, were tested in this study. In order to modulate the frictional conditions at the grip sur-
face, a thin sheet of sandpaper (No. 240) or a piece of smooth rayon cloth was attached on the
grip surface using thin double-sided adhesive tape. The amplified force transducer output sig-
nals were digitized using a personal computer via 12-bit A/D converter sampling at 600 Hz for
each channel.

Experimental tasks and procedure box

Lift-hold task. All 17 subjects performed this task. Each subject prepared his/her right
hand by placing it near the apparatus, and waited for a short computer-generated beep indicat-
ing the onset of gripping and lifting of the apparatus by a precision grip using the index finger
and the thumb. The apparatus was lifted at the subject’s self-determined lifting speed to a
height of about 5 cm above the top plate of the table, where it was held stationary until a second
beep coming 11 sec after the first one. The subject then dropped the apparatus on the table by
slowly separating the fingers. Each subject performed 8 trials for each of the 14 mass conditions
for each of the two surfaces, and thus provided trial data consisting of a total of 224 values. For
each subject, the mass conditions were presented randomly while the surface was kept con-
stant. The surface order was randomized for each subject.
Prior to the experiment, each subject washed his or her hands with soap and tap water. The
subject was then seated in a comfortable and stable chair in front of the experimental table on
which the grip apparatus was placed. After careful verbal explanation by the experimenter
about the procedure, the subject observed 3–5 demonstration trials performed by the experi-
menter, and performed the task with different mass and surface conditions until feeling com-
fortable in terms of the ability to perform the task. Because sliding-to-dropping of the object
slowly at the end of each task was difficult for some subjects, this process was repeatedly prac-
ticed until the subject was confident about their ability to perform it. Prior to the data collection
for a given mass condition for a given surface, the subject again practiced the lift-hold task

PLOS ONE | DOI:10.1371/journal.pone.0138506 September 16, 2015 5 / 19

 Prehension of Lightweight Objects

three times in order to experience the new condition. This was performed systematically in
order to minimize the aftereffects of the prior condition on the current condition. Each subject
had a break of several minutes between different mass conditions to prevent fatigue.
Weight discrimination task. On a separate day from the lift-hold task, 9 of the subjects
underwent a weight discrimination task using two light grip objects (mass = 4 g) having the
same dimensions as the grip force measurement apparatus. No force sensors were installed in
this object. A piece of string 15 cm long with a hook was attached at the bottom of this object
in order to hang an additional mass. The grip surfaces were covered with either sandpaper (No.
240) or rayon material. The two objects were placed 10 cm apart and side-by-side on an experi-
mental table with two small holes. The bottom of the table was covered with wooden panels to
hide the added mass from the subject’s view. The object placed on the right side always had the
standard mass, and that on the left side had the test mass. Four sets of test mass, with each set
comprising 9 levels of test mass and one standard mass, were used to find a just noticeable dif-
ference (JND) in object mass within each set. The standard mass objects weighed 10, 24, 48,
and 112 g, and the weights of their corresponding test masses ranged from 5 to 15 g (1.25-g
intervals), from 15 to 33 g (2.25-g intervals), from 35 to 61 g (3.25-g intervals), and from 94 to
130 g (4.5-g intervals), respectively.
In a similar manner to the grip force measurement tasks, the subject lifted and held the
right-side object stationary for about 7 sec above the table and then replaced it on the table. Fol-
lowing a 4-sec rest, the subject was asked to lift and hold the left-side object for about 7 sec, and
to replace it on the table. The subject then reported verbally to the experimenter whether the
second object was lighter or heavier than the first one. For each mass set, this forced weight dis-
crimination was performed in 63 trials in which the test mass presented for each trial was
pseudo-randomly changed. This provided 7 values of response data for each test mass-surface
condition per subject. The orders of the mass set and surface presentation were randomized for
each subject. A total of 504 trials (63 trials x 4 mass sets x 2 surfaces) were thus performed by
each subject. To reduce the effect of mental and physical fatigue, two separate sessions were
used for testing different surface conditions. In addition, an adequate rest period (3 min or
more) was given before testing a new mass set.

Data analysis and statistical tests

All trial records of the grip and load force data from the lift-hold task were processed off-line
to compute six parameters evaluating grip and load force control. During this process, grip
forces from the thumb and index finger were averaged [9,12]. The parameters evaluated were
static grip force, coefficient of variation (CV) of static grip force, grip and load force ratio (a
GF/LF ratio), slip force, safety margin force, safety margin force relative to the static grip force
(relative safety margin), and a coefficient of static friction. The static grip force was calculated
by averaging the grip force and corresponding load force over the period between 4 and 8 sec
from the onset of the initial beep. During the same period, the standard deviation (SD) of the
static grip force was also computed to evaluate static grip force fluctuations (within-trial vari-
ability). The CV of static grip force was then computed by the SD divided by the static grip
force as a measure of standardized grip force variability. The GF/LF ratio was calculated by
dividing the static grip force by the mean of the load force between 4 and 8 sec from the initial
beep.
The slip force was the minimum grip force required to prevent slippage, and it was mea-
sured at the moment when the apparatus began to slip. To facilitate identification of the slip-
ping moment, we computed the load force rate by first digitally filtering the load force data
using a low-pass method (4th-order Butterworth) at a cut-off frequency of 30 Hz, and

PLOS ONE | DOI:10.1371/journal.pone.0138506 September 16, 2015 6 / 19

 Prehension of Lightweight Objects

subsequently calculating the differences in load force between consecutive samples. We also
computed the SD of the static load force during the period between 4 and 8 sec from the initial
beep to facilitate the determination of slip events. A slip event was characterized by a marked
fall in the load force as well as its rate. For each trial, the slipping moment was approximated
first visually from the load force and load force rate records displayed on the PC screen, and
secondly, for the approximated period, the slip event was defined algorithmically when the
load force dropped below the threshold value of -2 SD. The corresponding slipping moment
was further defined from the load force rate data when the value became negative. In the light
mass conditions (< 22 g), there were sometimes multiple slip-stick events. In such cases, the
earliest defined slip event was adopted. The identification of the slipping moment was difficult
for some trial data owing to numerous excessively small slips, possibly caused by microslips,
and small object tilting. Of 1904 trials (17 subjects x 14 masses x 8 trials) for each grip surface,
the numbers of trials for which a clear slip moment could not be ensured were 179 (9.4%) for
sandpaper and 198 (10.4%) for rayon. However, all subjects provided at least 6 trials of slip
force data for each of the mass and surface conditions. The safety margin was then the differ-
ence between the static grip force and the slip force. The static friction coefficient was calcu-
lated as the ratio of slip force to load force at the moment the finger slipped.
For each of the grip force parameters, the mean of 8 trials was computed for each mass-sur-
face combination for each subject, which was used for the subsequent statistical tests. Two-way
ANOVA with repeated measures was performed to test the effects of mass and surface on the
GF/LF ratio, relative safety margin, coefficient of static friction, and CV of static grip force. A
post hoc test was carried out by the Tukey multiple comparison method. Statistical significance
was accepted at P<0.05.

Additional measurements
In order to facilitate understanding of light object prehension, three additional measurements
were also performed for all 17 subjects. First, grip force-related changes in the contact area of
the finger skin were estimated using the right thumb and index finger. A transparent acrylic
plate (130 x 130 x 8 mm) having force sensors at each of its four corners and a fluorescent light
to emboss the plate contacting skin in a dark environment were used in this measurement. The
force transducers were firmly fixed to a metal plate that had a circular hole (diameter: 40 mm)
in the center to view the skin contacting the acrylic plate. The metal plate was fixed vertically
on a test table so that the subject could press his/her finger on the acrylic plate in a manner
similar to gripping the test apparatus. The skin contacting the plate was recorded using a high-
resolution digital video camera sampling at 30 Hz. Recorded video images following contrast
processing were obtained using Otsu’s clustering-based image threshold technique [47,48], and
the pixel-based computation of the area of contact (the white area) was subsequently per-
formed to compute the apparent contact area [49]. On the basis of externally triggered signals
during the measurement, the force data sampling at 120 Hz was time-matched with the area
data. Second, the stress-strain relationship of the fingertip during gripping of an object was
assessed for each subject. The same grip force transducer used for the grip apparatus was firmly
attached to a vertical plate fixed on the test table, and the subject’s right hand/forearm rested
and height-adjusted on a table gripped the force sensor using the right thumb or index finger
while a slide-type friction-free precision position sensor (Kyowa Ltd., DLT-50AS) was attached
to the nail of the testing finger to measure the fingernail position relative to the grip surface.
These position data were used to estimate finger skin indentation during grip force application.
The gripping force and finger position data were simultaneously recorded upon PC sampling
at 600 Hz.

PLOS ONE | DOI:10.1371/journal.pone.0138506 September 16, 2015 7 / 19

 Prehension of Lightweight Objects

Results
Lift-hold tasks
Fig 2 shows typical examples of mean grip and load forces as a function of time in one subject
during the lift-hold task with the apparatus set to 6, 90, and 200 g under the rayon surface con-
ditions. The grip and load forces generated were fairly smooth from the grip onset, and formed
a small peak shortly after the apparatus had been lifted from the table. The grip force then rela-
tively smoothly transitioned to a holding phase. A slight decrease in the magnitude of grip
force was noted in some of the heavier mass conditions until the moment of release at the end
of the 10-sec holding phase (see the 200-g data in Fig 2). These force patterns were fairly com-
mon to all subjects.
In Fig 3A, the mean values of static and slip forces for all subjects in relation to the appara-
tus mass for each surface condition are shown. The mean static force ranged from 0.18 N while
holding the 6-g object to 2.68 N for the 200-g apparatus for the rayon surface, and the corre-
sponding values for the sandpaper surface were 0.13 to 1.37 N, respectively. These changes
occurred approximately in proportion to the object mass for both surfaces, which agrees with
the findings of Westling and Johansson [12], who examined the range of object mass from 100
to 1 kg. Differences in static grip force and slip force increased with object mass, so the subjects
retained a greater grip force as a margin against slippage for the objects with a heavier mass
(Fig 3A). The subjects also provided a greater safety margin force when holding the apparatus
with the rayon surface than that with the sandpaper surface. For the 6-g mass, for example, the
mean margin force was 0.11 N with the sandpaper surface, while it was 0.15 N with the rayon
surface. The margin forces for both surfaces increased almost linearly with an increase in mass
of the apparatus, and while holding the 200-g mass, the margin force increased to 0.61 N for

Fig 2. Typical force-time history curves of grip and load forces during the lift-hold task performed by one subject. The data are the mean (solid lines)
± standard deviation (dashed lines) of 8 trials for the 6, 90, and 200 g mass conditions with the rayon grip surface.
doi:10.1371/journal.pone.0138506.g002

PLOS ONE | DOI:10.1371/journal.pone.0138506 September 16, 2015 8 / 19

 Prehension of Lightweight Objects

Fig 3. Changes in the static grip force and slip force (A), grip-to-load force (GF/LF) ratio (B), coefficient of friction (C), and relative safety margin (D)
in relation to object mass for each surface condition. The data represent the mean and standard deviation (vertical bars) values of 17 subjects.
doi:10.1371/journal.pone.0138506.g003

PLOS ONE | DOI:10.1371/journal.pone.0138506 September 16, 2015 9 / 19

 Prehension of Lightweight Objects

the sandpaper surface and 1.19 N for the rayon surface. ANOVA confirmed the main effects of
surface (F1, 247 = 41.7, p < 0.0001) as well as mass (F13, 247 = 104.9, p < 0.0001) on the grip
force safety margin.
Grip and load forces were standardized by the value of the apparatus mass lifted (Fig 2). It
became evident that the standardized grip force curve of the 6-g condition was much greater
than those of the 90- and 200-g conditions. The difference in grip force between 90 g and 200
g, on the other hand, was less clear. In Fig 3B, the mean value of the GF/LF ratio for all subjects
is shown. The ratios for both surface conditions were highest with the lowest mass condition,
which decreased non-linearly with apparatus mass. The ratios were fairly constant above an
apparatus mass of 30 g for both surface conditions. ANOVA revealed significant main effects
of mass (F13, 247 = 63.6, p < 0.0001) and surface (F1, 247 = 35.1, p < 0.0001), with no interaction
between these variables. In order to assess the level of lifted mass that caused the upper shift of
the GF/LF ratio from a constant value, multiple comparison was performed using the value of
the 200-g condition as a reference. This multiple comparison revealed that the ratios for object
mass of 14 g or below for the rayon surface and 22 g or below for the sandpaper surface were
significantly greater than those of the reference value of the corresponding surface.
The coefficient of static friction was highest with the 6-g condition, and it dropped non-line-
arly with increasing apparatus mass for both surfaces (Fig 3C). This non-linear increase of the
coefficient of static friction towards a lighter tangential load (<0.5 N) has also been reported
elsewhere [44,45]. The mean values of the coefficient of static friction for the sandpaper surface
were 1.49 for the 6-g object and 1.32 for the 200-g object, and those for the corresponding
object mass with a rayon surface were 1.18 and 0.71, respectively. These friction coefficient val-
ues for the 200-g object with sandpaper and rayon surfaces are comparable to those reported
elsewhere [4,6,12]. As expected, ANOVA revealed significant mass (F13, 247 = 30.9, p < 0.0001)
and surface effects (F1, 247 = 33.9, p < 0.0001) on the friction coefficient.
The relative safety margin, the proportion of the safety margin force to the static grip force,
was around 40% to 50% when holding an apparatus weighing 100 g or more (Fig 3D), which is
in accordance with the range of the relative margin reported in previous studies [4,12]. The val-
ues were clearly increased when holding lighter masses, and indeed they reached around 80%
when holding a 6-g mass for both surface conditions. The changes in the relative safety margin
with the mass were non-linear. ANOVA revealed a significant main effect of mass (F13, 247 =
157.1, p < 0.0001), with no surface and surface x mass interaction effects. A Tukey post hoc
test revealed that the values for objects weighing less than 90 g for the rayon surface and less
than 70 g for the sandpaper surface were significantly greater than those for the 200-g mass
(p < 0.01).

Static grip force fluctuations

The mean value of within-trial variability (SD) of static grip force for all subjects was increased
from 0.013 N with the 6-g mass to 0.095 N with the 200-g mass for the rayon surface, and the
corresponding values for the sandpaper surface were 0.011 N and 0.063 N, respectively. Their
increases with object mass were approximately linear (Fig 4A). The standardized grip force var-
iability (CV of the static grip force), on the other hand, had a non-linear relationship with
apparatus mass, while showing the highest mean for the 6-g condition for both surfaces (Fig
4B). ANOVA followed by a post hoc comparison with the 200-g data confirmed that the differ-
ences in the mean values of a 30-g mass or lighter for the rayon surface and a 14-g mass or ligh-
ter for the sandpaper surface were significant, clearly indicating that force fluctuations were
elevated when holding objects in the lower end of the mass range examined.

PLOS ONE | DOI:10.1371/journal.pone.0138506 September 16, 2015 10 / 19

 Prehension of Lightweight Objects

Fig 4. Within-trial variability of static grip force expressed by standard deviation (A) and coefficient of variation (B). The data represent the mean and
standard deviation (vertical bars) values of 17 subjects.
doi:10.1371/journal.pone.0138506.g004

Weight discrimination task

For the individual weight discrimination data for each surface condition, the mean probability
of correct response was computed using 7 trial data at each of the 9 test-mass levels. The 9
mean probability values were then plotted in relation to the value of %mass difference from the
test (standard) mass. A logistic function was fitted to these individual data to estimate the value
of JND defined as the stimulus magnitude of the comparison at which the proportion of cor-
rectly discriminated heavier test objects equal to 0.85 [50]. Typical examples of the JND esti-
mated for one subject with the 10-g and 112-g test sets under the rayon surface condition are
shown in Fig 5A. Note that the fitted curve for the 112-g test set had a steeper slope than that
of the 10-g test set, resulting in a greater Weber fraction value for the 10-g test set compared to
the 112-g test set.
Fig 5B shows the mean JND values for the 9 subjects computed for all four mass sets under
the rayon and sandpaper surface conditions. For both surfaces, the JND corresponded to a
Weber fraction value of 0.06 (6% of the standard mass) for the 112-g test set. The JND was
clearly elevated with a decrease in test mass, reaching 0.29 (29% of the standard mass) for the
10-g set, close to a fivefold increase from that for the 112-g set. ANOVA with a multiple com-
parison confirmed significant differences in the JND between 10-g and the other three mass
conditions, and between 24 g and 112 g. The ability to discriminate heaviness held by the fin-
gers was thus not proportional to the object mass. These findings confirmed that a small test
object of equal dimensions to the instrumented grip apparatus produced results of weight dis-
crimination similar to earlier observations by Oberlin [30], and Ross and Reschke [51], who
reported that Weber-fraction-related heaviness perception rose largely for objects with a small
mass below 50 g.

Mechanical properties of the finger pad

Fig 6 shows grip-force-related changes in the mean value of apparent surface contact area by
the index finger and thumb for all 17 subjects. The area sharply decreased when the applied

PLOS ONE | DOI:10.1371/journal.pone.0138506 September 16, 2015 11 / 19

 Prehension of Lightweight Objects

Fig 5. A typical example of the mean probability of correct response in relation to percent difference in test mass from the standard masses of 10
and 112 g for the rayon surface in one subject (A). Logistic function curves were fitted to examine their relationship. Changes in mean Weber's
fraction with test mass for all subjects for the rayon and sandpaper surfaces (B). The vertical bars indicate the standard deviation values.
doi:10.1371/journal.pone.0138506.g005

grip force was below 1 N, and the decrease was even sharper below a grip force of 0.5 N. Curve
fitting on the average apparent contact area (Area) as a function of grip force (GF) was per-
formed using a power function (Area = aGFb). Grip force between 0.01 N and 4 N gave values
of a and b for the index finger of 122.9 mm2/N, and 0.409 (r2 = 0.96) and those for the thumb
of 169.8 mm2/N and 0.436 (r2 = 0.96), respectively. These values are close to the average values
provided in a previous study [49].
In Fig 6, the finger pad indentation and grip force relationship is also given. Similar to the
changes in contact area, the pads for both the thumb and the index finger were largely
deformed upon the application of grip force up to 0.5 N, and the increase in deformation grad-
ually tapered with larger force application. Curve fitting with a power function (indentation =
cGFd) on the mean data provided values of c and d for the index finger of 1.57 m/N and 0.40
(r2 = 0.94), and for the thumb of 2.02 m/N and 0.40 (r2 = 0.95), respectively.

Discussion
Westling and Johansson [12] previously showed that, while holding a movable object using a
precision grip, the generated grip force was proportionally modulated in relation to the object
mass ranging from 100 g to 1 kg, so that the GF/LF ratio could be kept nearly constant for a
given grip surface. The present results basically support their findings, and further suggest that
the same relationship could be retained down to the lower range of object mass (>30 g). On
the other hand, for objects lighter than 30 g, the healthy adults employed a progressively higher
GF/LF ratio. The ratio for the 6-g object, namely, the lowest mass tested in this study, was
more than double those upon holding a mass of 100 g or above for both the sandpaper and the
rayon surfaces. A clear increase in the GF/LF ratio while holding an object was also reported by
researchers who performed precision grip experiments while their healthy young subjects were
experiencing microgravity induced by parabolic flights [25,26]. They found that a grip force

PLOS ONE | DOI:10.1371/journal.pone.0138506 September 16, 2015 12 / 19

 Prehension of Lightweight Objects

Fig 6. Mean finger-surface contact areas and finger pad skin deformation for the thumb and index
finger for all subjects in relation to varied magnitude of grip force applied.
doi:10.1371/journal.pone.0138506.g006

from 0.9 N to 0.4 N as a pure grip force safety margin was present while holding a weightless
object.
Because the grip force for holding an object having a certain mass can be made up of the
components of slip force and safety margin, either or both of these could be increased to pro-
vide a high GF/LF ratio. The evaluation of each of these in the present study confirmed that the
increase of the safety margin was exclusively responsible for the raised GF/LF ratio for the lift-
ing of very low-mass objects (< 30 g). It was also confirmed that the slip force did not increase,
but it instead progressively decreased towards the lower end of object mass. An increase of the
GF/LF ratio by an enlarged safety margin is discussed in association with the hypotheses posed
in the introduction.

Decreased tactile sensibility for holding a light object

Studies using local anesthesia of grasping digits [12,23,52–54] have repeatedly shown that cuta-
neous sensory inflow plays a crucial role for the CNS in properly adjusting the GF/LF ratio dur-
ing lifting and holding of an object. Loss of cutaneous sensation commonly causes disability of
proper surface friction and load force adaptation, resulting in a high GF/LF ratio with an exces-
sively elevated margin of grip force [52]. Experiments using gloves with different thicknesses of
material [10] and compression of the median nerve at different pressure levels [20] have fur-
ther demonstrated that graded hypoesthesia can lead to a corresponding increase in the magni-
tude of grip force used. It is thus possible to conjecture that graded increases in both the GF/LF
ratio and the relative safety margin with a lighter object are attributable to a corresponding
decrease in available cutaneous sensory input. A crucial factor determining the magnitude of
tactile sensory input can be the number or population of activated mechanoreceptors at the
gripping site. Four types of cutaneous mechanoreceptor (FAI, FAII, SAI, and SAII) innervating
the glabrous skin of the human hand are known to convey sensory signals to the CNS for
the control of grip force [55,56]. FA types have strong sensitivity to dynamic stimuli including

PLOS ONE | DOI:10.1371/journal.pone.0138506 September 16, 2015 13 / 19

 Prehension of Lightweight Objects

slip-induced skin vibration. SA types are sensitive to sustained skin indentation and stretch.
Among these four, FAI and SAI units (some FAII units as well) are known to play an important
role in providing afferent signals to the CNS to maintain static grip force at an intended low
level. The primary afferent signals are commonly from microslips localized to the peripheral
zone (10–30%) of the contact area, which appear when static grip force with a small safety mar-
gin is further decreased [1,13,57]. When the local slip zone exceeds about three-quarters of the
contact area, an overall slip commonly occurs, which gives a strong burst of afferent signals to
trigger a rapid increase in grip force [56,58]. The area of contact and skin indentation data sug-
gest that the available population of cutaneous units possibly activated decreases sharply below
a grip force of 0.4 N (Fig 6). The population signaling the localized slips would then be even
smaller. A grip force of 0.4 N corresponded to the static grip force observed while holding a
30-g object with a rayon surface, suggesting that the population of cutaneous receptors acti-
vated below this may prompt a feeling of insecurity regarding sensory feedback required for
stable grasping. The results from the present weight discrimination test showing a clearly
higher Weber fraction with a lighter object seem to support this.

Central control for lifting and holding an object with a low mass
Centrally organized motor commands must have contributed to the elevated GF/LF ratio along
with the high relative safety margin in the current low mass range (<30 g). Behavioral studies
have repeatedly shown that lifting of an object is basically performed by the prediction of its
mechanical properties, including mass, surface friction, size, and shape [17,18,22,59]. The
appearance of the object and sensory memories acquired through previous lifts are essential for
the CNS to make an accurate prediction on the generation of grip force at object-lift onset. A
smooth transition from lifting to stable holding of the gripped object also takes place with accu-
rate anticipation of an object’s properties [11,18]. To facilitate the sensory memory-based per-
formance in the present study, the data were always collected from repeated lifts with objects
having the same properties. As expected, we observed the profiles of grip and load forces with
fairly smooth increases without forming either an excessively high peak or multiple peaks dur-
ing the loading phase, and a smooth transition to a stable level for static holding across all
object mass conditions (Fig 2). On the other hand, we also observed a common high GF/LF
ratio during the phase of load force increase for the light objects, which poses questions first
about the effect of finger-surface frictional change with small grip force application, second
about the goodness of the sensory memory used, and third about the complexity of fine finger-
tip force control.
Firstly, a priori knowledge about the current frictional state at the finger-surface interface
plays a dominant role in the setting of the GF/LF ratio during object lifting [17]. Predictive grip
force production with a higher GF/LF ratio has been found during lifting and holding of a
more slippery object [9,56]. This was basically true in the present study, in which the force
ratio for the rayon was set higher during lifting and holding than that for the sandpaper at all
object masses. By contrast, this does not seem to be the case for the effect of the mass-related
frictional change. Slip force assessed in our subjects indicated that the friction clearly increased
at the lower mass range (<30 g) compared with that for the heavy range (> 100 g), and the
GF/LF ratio followed a similar pattern. Therefore, the possibility of an effect of friction on the
increased force ratio during low-mass-object lifting is unlikely.
This leads to the second possibility of doubt about the goodness of the sensory memory. As
discussed above, when manipulating a low-mass object, sensory afferents from the fingertips
were most likely insufficient. The results of the psychophysical test at the low mass range also
indicated the difficulty of accurate mass perception acquired from both proprioceptive and

PLOS ONE | DOI:10.1371/journal.pone.0138506 September 16, 2015 14 / 19

 Prehension of Lightweight Objects

cutaneous sensors. With such limited tactile sensory inflow, sensory memory of the current
object properties would also be formed less accurately and affect the goodness of memory-
based proper feed-forward scaling of the grip force. The increased GF/LF ratio at lifting onset
and during the holding phase can be considered as a compensatory and learned strategy
employed by individuals with declined cutaneous sensory function, such as observed in carpal
tunnel syndrome patients [34,35] and the elderly [7,9]. We conjecture that a similar strategy
was adopted by our healthy adults when manipulating regular items with a small mass while
facing a trade-off between the economy of some extra muscular work and a secure feeling of
grasp stability with increased tactile sensory inflow and a greater contact area.
The third possibility is difficulty in producing a sustained grip force at an intended low level
due to increased variability of motor unit discharge in the muscles used [41,43,60]. The propor-
tion of internal noise in the common neural drive to moto-neurons of target muscles is known
to be increased at low contraction intensities in some muscles, including those in the hand
[61,62]. This commonly leads to a greater proportion of fluctuations (CV values) in generated
force, causing a decline in optimal control of sensori-motor performance due to a decreased
signal-to-noise ratio [63]. Using the CV values of isometric force, studies have indeed demon-
strated that force fluctuations at weak levels (2–4% of maximum voluntary contraction) were
apparently greater than those at moderate levels (12–50%) [39,42]. Our static grip force CV
values followed a similar pattern; the value with 6-g mass was highest, which decreased non-
linearly with increased object mass.
Could the magnitude of force fluctuations observed when holding low-mass objects actually
threaten grasp stability? To test this, hypothetical (non-elevated) static grip force was estimated
for each of the low-mass conditions (<30 g) based on the assumption that the subjects used a
GF/LF ratio similar to that for larger-mass conditions (110–200 g) for the low-mass conditions.
The mean ratios of the heavier conditions were 1.44 for the sandpaper and 2.71 for the rayon,
which would provide estimated grip forces of 0.08 and 0.04 N for these surfaces when holding
the 6-g object, for example. Subtracting slip forces of 0.03 N for the rayon and 0.02 N for the
sandpaper from these values gives safety margin forces of 0.05 N and 0.02 N for these surfaces.
The 95% confidence interval values of static grip force fluctuations for these surfaces were
0.028 N and 0.024 N, respectively. Therefore, unless the subjects voluntarily increased the
safety margin during low-mass holding, the fluctuations could have exceeded the lowest limit
of the margin, inducing constant reflexive force adjustments or, in the worst case, a loss of the
held object, particularly for the sandpaper conditions with a small margin force.
The safety margin forces actually secured by the present subjects for the 6-g mass condition
were 0.11 N with the sandpaper and 0.15 N with the rayon. Related to the grip force margin,
earlier studies during parabolic flights demonstrated that a pure safety margin assessed from
stationary holding of a weightless object with a mass of 471 g with a sandpaper surface was
about 1 N [26], and that of an 800-g mass with a brass surface was 0.4 N when the subjects
were better adapted to parabolas [25]. Hermsdorfer et al. [26] stated that a margin force of
about 1 N would be needed even for a zero-weight object to guard against a sudden increase of
the inertial force that may result from perturbations of the stationary arm position. These mar-
gin values were thus much larger than our values measured under normal-gravity conditions.
This discrepancy most likely arose from motor commands for preparatory control of antici-
pated inertial force on the object due to the use of apparatuses with 8 to 12 times larger mass in
their studies than in ours. The larger safety margin may also be attributed to the microgravity
effect, which had not been completely eliminated within the limited period of adaptive
training.
Optimal sensori-motor control theories use cost functions to explain how actions are per-
formed [64]. The voluntary grip force for adjusting the safety margin should not be too high to

PLOS ONE | DOI:10.1371/journal.pone.0138506 September 16, 2015 15 / 19

 Prehension of Lightweight Objects

optimize the costs of energy through muscle commands. It could also be applicable to the cost
of finely adjusting low levels of grip force to cope with very light objects, which could be quite
expensive for central energy. The findings from a functional imaging study by Kuhtz-Busch-
beck et al. [14] indeed indicated that a precision grip of an object with deliberate lessening of
the safety margin from the ordinary level would demand greater cortical activation in the corti-
cal and subcortical areas, most likely reflecting increased alertness for increased difficulty of
grasp stability.
In summary, the instrumented small grip apparatus developed in this study extended our
understanding of sensorimotor control of finger forces employed by healthy young adults
when lifting and holding objects with an extremely low mass in a normal-gravity environment.
It was demonstrated that the GF/LF ratio, a portion of the safety margin in the static grip force,
and normalized moment-to-moment static grip force fluctuations were all elevated progres-
sively towards the lower end of the object mass range examined. These occurred irrespective
of friction at the grip surface. The findings thus indicate that a strategy of grip force control
for holding objects with a smaller mass becomes progressively different from that which was
proposed by earlier researchers who used a grip apparatus with a mass greater than 100 g
[1,6,12,18]. Test results of weight perception, finger-surface contact area, and skin indentation
indicated that feedback signals from the population of cutaneous mechanoreceptors activated
while holding an extremely light object were greatly limited. Overall, the present findings sug-
gested that the handling of objects with a very light mass (< 30 g) produced greater reliance on
higher cortical function, by which the portion of the safety margin force within the holding
grip force was raised in order to reduce the risk of losing the object from the fingers. The
declined peripheral sensory input, increased proportions of static grip force fluctuations, and
increased care regarding the effect of the inertial component of the load force were considered
to be related to the elevated cortical function.
As for future study on light objects, one should examine the rigidity of the apparatus. On a
very light and deformable object such as a thin plastic cup, it may be that, while load force
(object mass) is too low to be considered as the main factor (or the co-factor with friction) that
drives the CNS in forming a precision grip, the deformation of the material can be used instead.
In that case, using a very rigid metallic structure could create confusion of the system.
Precision grip is also a focal topic of recent research in rehabilitation. In this regard, an
instrumented grip apparatus with a small mass as developed in this study should be useful for
the examination of patients with neurological disorders and stroke. These patients commonly
incur long-term deficits in sensori-motor function of the hand, often having markedly lowered
grip strength with declined fine force control compared with their healthy peers. Finally, the
development of an instrumented wireless apparatus, and thus a freely movable device with a
small mass, is also urgently needed for the assessment and training of sensori-motor function
in neurological and stroke patients.

Author Contributions
Conceived and designed the experiments: YH HK TI. Performed the experiments: YH HK DK.
Analyzed the data: YH HK KK. Contributed reagents/materials/analysis tools: YH HK. Wrote
the paper: YH HK.

References
1. Johansson RS (1996) Sensory control of dexterous manipulation in humans. In: Wing AM, Haggard P,
Flanagan JR, editors. Hand and Brain: The Neurophysiology and Psychology of Hand Movements.
San Diego: Academic Press. pp. 381–414.

PLOS ONE | DOI:10.1371/journal.pone.0138506 September 16, 2015 16 / 19

 Prehension of Lightweight Objects

2. Nowak DA, Hermsdörfer J (2009) Sensorimotor Control of Grasping: Physiology and Pathophysiology.
UK: Cambridge University Press. 524 p.
3. Goodwin AW, Jenmalm P, Johansson RS (1998) Control of grip force when tilting objects: effect of cur-
vature of grasped surfaces and applied tangential torque. J Neurosci 18: 10724–10734. PMID:
9852607
4. Kinoshita H, Bäckström L, Flanagan JR, Johansson RS (1997) Tangential torque effects on the control
of grip forces when holding objects with a precision grip. J Neurophysiol 78: 1619–1630. PMID:
9310447
5. Zatsiorsky VM, Latash ML (2008) Multi-finger prehension: an overview. J Mot Behav 40: 446–476. doi:
10.3200/JMBR.40.5.446-476 PMID: 18782719
6. Burstedt MK, Flanagan JR, Johanson RS (1999) Control of grasp stability in humans under different
frictional conditions during multidigit manipulation. J Neurophysiol 82: 2393–2405. PMID: 10561413
7. Cole KJ, Rotella DL, Harper JG (1999) Mechanisms for age-related changes of fingertip forces during
precision gripping and lifting in adults. J Neurosci 19: 3238–3247. PMID: 10191336
8. Edin BB, Westling G, Johansson RS (1992) Independent control of human finger-tip forces at individual
digits during precision lifting. J Physiol 450: 547–564. PMID: 1432717
9. Kinoshita H, Francis PR (1996) A comparison of prehension force control in young and elderly individu-
als. Eur J Appl Physiol Occup Physiol 74: 450–460. PMID: 8954293
10. Kinoshita H (1999) Effect of gloves on prehensile forces during lifting and holding tasks. Ergonomics
42: 1372–1385. PMID: 10582505
11. McDonnell MN, Ridding MC, Flavel SC, Miles TS (2005) Effect of human grip strategy on force control
in precision tasks. Exp Brain Res 161: 368–373. PMID: 15480594
12. Westling G, Johansson RS (1984) Factors influencing the force control during precision grip. Exp Brain
Res 53: 277–284. PMID: 6705863
13. Johansson RS, Westling G (1990) Tactile afferent signals in the control of precision grip. In: Marc Jean-
nerod, editor. Attention and Performance XIII. Hillsdale, NJ: erlbaum. pp. 677–713.
14. Kuhtz-Buschbeck JP, Ehrsson HH, Forssberg H (2001) Human brain activity in the control of fine static
precision grip forces: an fMRI study. Eur J Neurosci 14: 382–390. PMID: 11553288
15. Flanagan JR, Johansson RS (2002) Hand movements. In: Ramachandran VS, editor. Encyclopedia of
the Human Brain. Vol. 2, San Diego: Academic Press. pp. 399–414.
16. Gordon AM, Forssberg H, Johansson RS, Westling G (1991) Visual size cues in the programming of
manipulative forces during precision grip. Exp Brain Res 83: 477–482. PMID: 2026190
17. Johansson RS, Westling G (1984) Roles of glabrous skin receptors and sensorimotor memory in auto-
matic control of precision grip when lifting rougher or more slippery objects. Exp Brain Res 56: 550–
564. PMID: 6499981
18. Johansson RS, Westling G (1988) Coordinated isometric muscle commands adequately and errone-
ously programmed for the weight during lifting task with precision grip. Exp Brain Res 71: 59–71.
PMID: 3416958
19. Cadoret G, Smith AM (1996) Friction, not texture, dictates grip forces used during object manipulation.
J Neurophysiol 75: 1963–1969. PMID: 8734595
20. Cole KJ, Steyers CM, Graybill EK (2003) The effects of graded compression of the median nerve in the
carpal canal on grip force. Exp Brain Res 148: 150–157. PMID: 12520402
21. Flanagan JR, Wing AM (1995) The stability of precision grip forces during cyclic arm movements with a
hand-held load. Exp Brain Res 105: 455–464. PMID: 7498399
22. Jenmalm P, Johansson RS (1997) Visual and somatosensory information about object shape control
manipulative fingertip forces. J Neurosci 17: 4486–4499. PMID: 9151765
23. Nowak DA, Hermsdörfer J, Glasauer S, Philipp J, Meyer L, Mai N (2001) The effects of digital anaesthe-
sia on predictive grip force adjustments during vertical movements of a grasped object. Eur J Neurosci
14: 756–762. PMID: 11556900
24. Augurelle AS, Penta M, White O, Thonnard JL (2003) The effects of a change in gravity on the dynam-
ics of prehension. Exp brain Res 148: 533–540. PMID: 12582839
25. Crevecoeur F, Thonnard JL, Lefèvre P (2009) Forward models of inertial loads in weightlessness. Neu-
roscience 161: 589–598. doi: 10.1016/j.neuroscience.2009.03.025 PMID: 19303921
26. Hermsdörfer J, Marquardt C, Philipp J, Zierdt A, Nowak D, Glasauer S, et al. (1999) Grip forces exerted
against stationary held objects during gravity changes. Exp Brain Res 126: 205–214. PMID: 10369143
27. Hermsdörfer J, Marquardt C, Philipp J, Zierdt A, Nowak D, Glasauer S, et al. (2000) Moving weightless
objects. Grip force control during microgravity. Exp Brain Res 132: 52–64. PMID: 10836635

PLOS ONE | DOI:10.1371/journal.pone.0138506 September 16, 2015 17 / 19

 Prehension of Lightweight Objects

28. White O, McIntyre J, Augurelle AS, Thonnard JL (2005) Do novel gravitational environments alter the
grip-force/load-force coupling at the fingertips? Exp brain Res 163: 324–334. PMID: 15635455
29. Engen T (1971) Psychophysics I. Discrimination and detection. In: Kling JW, Riggs LA, editors. Wood-
worth and Schlosberg’s Experimental Psychology. 3rd edition, New York: Holt, Rinehart and
Winston. pp. 11–46.
30. Oberlin KW (1936) Variation in intensive sensitivity to lifted weights. J Exp Psychol 19: 438–455.
31. Kobylecki S (1906) Über die Wahrnehmbarkeit plötzlicher Druckänderungen. Psychol Stud 1: 219–
304.
32. Kawashima N, Abe MO, Iwaya T, Haga N (2012) Abnormal capacity for grip force control in patients
with congenital insensitivity to pain. Exp Brain Res 218: 579–588. doi: 10.1007/s00221-012-3050-7
PMID: 22418782
33. Schenker M, Burstedt MK, Wiberg M, Johansson RS (2006) Precision grip function after hand replanta-
tion and digital nerve injury. J Plast Reconstr Aesthet Surg 59: 706–716. PMID: 16782566
34. Thonnard JL, Saels P, Van den Bergh P, Lejeune T (1999) Effects of chronic median nerve compres-
sion at the wrist on sensation and manual skills. Exp Brain Res 128: 61–64. PMID: 10473740
35. Zhang W, Johnston JA, Ross MA, Smith AA, Coakley BJ, Gleason EA, et al. (2011) Effects of carpal
tunnel syndrome on adaptation of multi-digit forces to object weight for whole-hand manipulation. PLoS
One 6: e27715. doi: 10.1371/journal.pone.0027715 PMID: 22110738
36. Harris CM, Wolpert DM (1998) Signal-dependent noise determines motor planning. Nature 394: 780–
784. PMID: 9723616
37. Jones KE, Hamilton AF, Wolpert DM (2002) Sources of signal-dependent noise during isometric force
production. J Neurophysiol 88: 1533–1544. PMID: 12205173
38. Hamilton AF, Jones KE, Wolpert DM (2004) The scaling of motor noise with muscle strength and motor
unit number in humans. Exp Brain Res 157: 417–430. PMID: 15014922
39. Galganski ME, Fuglevand AJ, Enoka RM (1993) Reduced control of motor output in a human hand
muscle of elderly subjects during submaximal contractions. J Neurophysiol 69: 2108–2115. PMID:
8350134
40. Griffin L, Painter PE, Wadhwa A, Spirduso WW (2009) Motor unit firing variability and synchronization
during short-term light-load training in older adults. Exp Brain Res 197: 337–345. doi: 10.1007/s00221-
009-1920-4 PMID: 19578838
41. Enoka RM, Christou EA, Hunter SK, Kornatz KW, Semmler JG, Taylor AM, et al. (2003) Mechanisms
that contribute to differences in motor performance between young and old adults. J Electromyogr Kine-
siol 13: 1–12. PMID: 12488083
42. Taylor AM, Christou EA, Enoka RM (2003) Multiple features of motor-unit activity influence force fluctu-
ations during isometric contractions. J Neurophysiol 90: 1350–1361. PMID: 12702706
43. Slifkin AB, Newell KM (1999) Noise, information transmission, and force variability. J Exp Psychol Hum
Percept Perform 25: 837–851. PMID: 10385989
44. Comaish S, Bottoms E (1971) The skin and friction: deviations from Amonton’s laws, and the effects of
hydration and lubrication. Br J Dermatol 84: 37–43. PMID: 5573184
45. Derler S, Gerhardt LC (2012) Tribology of skin: review and analysis of experimental results for the fric-
tion coefficient of human skin. Tribol Lett 45: 1–27.
46. Oldfield RC (1971) The assessment and analysis of handedness: The Edinburgh inventory. Neuropsy-
chologia 9: 97–113. PMID: 5146491
47. Otsu N (1975) A threshold selection method from gray-level histograms. Automatica 11: 23–27.
48. Sezgin M, Sankur B (2004) Survey over image thresholding techniques and quantitative performance
evaluation. J Electron Imaging 13: 146–168.
49. Delhaye B, Lefèvre P, Thonnard JL (2014) Dynamics of fingertip contact during the onset of tangential
slip. J R Soc Interface 11: 20140698. doi: 10.1098/rsif.2014.0698 PMID: 25253033
50. Green DM (1990) Stimulus selection in adaptive psychophysical procedures. J Acoust Soc Am 87:
2662–2674. PMID: 2373801
51. Ross HE, Reschke MF (1982) Mass estimation and discrimination during brief periods of zero gravity.
Percept Psychophys 31: 429–436. PMID: 7110901
52. Häger-Ross C, Johansson RS (1996) Nondigital afferent input in reactive control of fingertip forces dur-
ing precision grip. Exp Brain Res 110: 131–141. PMID: 8817264
53. Augurelle AS, Smith AM, Lejeune T, Thonnard JL (2003) Importance of cutaneous feedback in main-
taining a secure grip during manipulation of hand-held objects. J Neurophysiol 89: 665–671. PMID:
12574444

PLOS ONE | DOI:10.1371/journal.pone.0138506 September 16, 2015 18 / 19

 Prehension of Lightweight Objects

54. Cole KJ, Abbs JH (1988) Grip force adjustments evoked by load force perturbations of a grasped
object. J Neurophysiol 60: 1513–1522. PMID: 3193168
55. Birznieks I (2003) Tactile sensory control of dexterous manipulation in humans. Ph.D. Thesis, Umeå
University.
56. Johansson RS, Westling G (1987) Signals in tactile afferents from the fingers eliciting adaptive motor
responses during precision grip. Exp Brain Res 66: 141–154. PMID: 3582528
57. Johansson RS, Vallbo AB (1979) Tactile sensibility in the human hand: relative and absolute densities
of four types of mechanoreceptive units in glabrous skin. J Physiol 286: 283–300. PMID: 439026
58. Adams MJ, Johnson SA, Lefèvre P, Lévesque V, Hayward V, André T, et al. (2012) Finger pad friction
and its role in grip and touch. J R Soc Interface 10: 20120467. doi: 10.1098/rsif.2012.0467 PMID:
23256185
59. Flanagan JR, King S, Wolpert DM, Johansson RS (2001) Sensorimotor prediction and memory in
object manipulation. Can J Exp Psychol 55: 89–97.
60. Moritz CT, Barry BK, Pascoe MA, Enoka RM (2005) Discharge rate variability influences the variation in
force fluctuations across the working range of a hand muscle. J Neurophysiol 93: 2449–2459. PMID:
15615827
61. Dideriksen JL, Negro F, Enoka RM, Farina D (2012) Motor unit recruitment strategies and muscle prop-
erties determine the influence of synaptic noise on force steadiness. J Neurophysiol 107: 3357–3369.
doi: 10.1152/jn.00938.2011 PMID: 22423000
62. Farina D, Negro F, Dideriksen JL (2014) The effective neural drive to muscles is the common synaptic
input to motor neurons. J Physiol 592: 3427–3441. doi: 10.1113/jphysiol.2014.273581 PMID:
24860172
63. Keen A, Yue H, Enoka RM, Enoka M (1994) Training-related enhancement in elderly humans in the
control of motor output. PMID: 7896604
64. Todorov E (2004) Optimality principles in sensorimotor control. Nat Neurosci 7: 907–915. PMID:
15332089

PLOS ONE | DOI:10.1371/journal.pone.0138506 September 16, 2015 19 / 19

Copyright of PLoS ONE is the property of Public Library of Science and its content may not
be copied or emailed to multiple sites or posted to a listserv without the copyright holder's
express written permission. However, users may print, download, or email articles for
individual use.