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Monkey Hand Postural Synergies During Reach-to-Gra
Monkey Hand Postural Synergies During Reach-to-Gra
Monkey Hand Postural Synergies During Reach-to-Gra
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Mason, Carolyn R., Lalin S. Theverapperuma, Claudia M. Hen- Slocum and Pratt 1946) and culminated in Napier’s classifica-
drix, and Timothy J. Ebner. Monkey hand postural synergies during tion of prehension into power and precision grasp. The distinc-
reach-to-grasp in the absence of vision of the hand and object. J tion between grasps was based on achieving force/object sta-
Neurophysiol 91: 2826 –2837, 2004. First published February 4, 2004;
10.1152/jn.00653.2003. Understanding how the CNS controls reach- bility (Napier 1956). Numerous studies have demonstrated that
to-grasp will require behavioral and neurophysiological studies of the evolution of hand shape is coupled tightly to the reach
reach-to-grasp in the monkey, including the evaluation of whole-hand (Bootsma et al. 1994; Chieffi and Gentilucci 1993; Jeannerod
grasp with explicit force requirements. In this study, monkeys per- 1984; Paulignan et al. 1990). During perturbations of reach-
formed a reach-to-grasp task in which the size, shape, and orientation to-grasp movements corrective changes in both components
of the objects were varied. The monkeys were required to grasp each are coupled (Castiello et al. 1993, 1998). The coupling between
object at five force levels based on visual feedback. Seventeen posi-
transport and object size is particularly evident when reach is
tions on the wrist and hand were monitored to quantify kinematics.
Hand shaping began with initiation of reach and continued throughout perturbed (Castiello et al. 1993, 1998; Paulignan et al. 1991a).
the reach, matching object properties even without vision of the hand Similarly, accuracy constraints affect both reach (Bootsma et
or object. Grasp aperture scaled to object size. Singular value decom- al. 1994; Fitts 1954) and grasp (Bootsma et al. 1994). These
position analysis of the marker positions identified two dominant hand findings are consistent with the hypothesis that global syner-
postures. The first eigenvector or “eigenposture” consisted of an open gies are involved in the control of reach-to-grasp.
hand configuration midway between flexion and extension that ex- In humans static and dynamic grasp can be described using
plained ⬎93% of the variance. The second eigenposture consisted of a small number of postural synergies (Mason et al. 2001;
hyperextension of all joints that accounted for another 4 –5% of the Santello and Soechting 1997; Santello et al. 1998, 2002). Using
variance. The two eigenpostures were similar across force levels and either principal component analysis (PCA) or singular value
between monkeys. Reach kinematics consisted of a U-shaped hand
path with a bell-shaped velocity profile. Trajectory and speed were
decomposition (SVD), linear combinations of two to three
independent of grasp force and object properties. In summary, hand basis vectors (hand postures) can describe ⬃75–95% of the
shaping during the reach occurred without vision of the hand or variability of hand shape across different objects and grasp
object, and hand kinematics were not dependent on grasp force. types, real or mimed movements, and conditions with or with-
Furthermore, the reach was independent of grasp force and object out tactile input. The evolving shape of the hand throughout
properties. These observations imply that the kinematics of reach-to- transport and grasp can be reconstructed from either the prin-
grasp and grasp force are controlled independently. Similar to hu- cipal components or eigenpostures (Mason et al. 2001; Santello
mans, monkeys may use a simplifying strategy to reduce the degrees et al. 2002). The timing of the contributions of the individual
of freedom of the hand during reach-to-grasp. basis vectors to hand shaping may differ yet remain synchro-
nized during reach (Mason et al. 2001; Santello et al. 2002).
INTRODUCTION
These findings provide further evidence that synergies are
operative during reach-to-grasp, presumably to simplify the
Prehension movements of the hand are one of the more complexity of the control problem (Mason et al. 2001; Santello
highly developed motor skills of human and non-human pri- et al. 1998, 2002).
mates. When coupled to the transport capabilities provided by Understanding the neural mechanisms underlying the syn-
the arm and its additional degrees of freedom, the result is a ergies used to control reach-to-grasp will require neurophysi-
vast behavioral repertoire that ranges from reaching and grasp- ological studies in the non-human primate. A first step will be
ing, to using tools and manipulating the environment. Under- to quantitatively describe reach-to-grasp in the monkey includ-
standing how the CNS controls reach-to-grasp is a central ing characterizing the kinematics of hand shape, force control,
question in motor control. Considerable attention has been and grasp synergies as well as the contribution of vision.
given to the use of synergies as a means of reducing the Earlier investigations in the monkey have evaluated qualita-
number of degrees of freedom of the hand during reach-to- tively the grasp of objects of various shapes and sizes (Gardner
grasp (Mason et al. 2001; Santello and Soechting 1997; San- et al. 1999; Murata et al. 1997; Rizzolatti et al. 1988) or force
tello et al. 1998, 2002). generated during final lateral pinch grasp (Smith et al. 1975).
Movements of the limb, hand, and fingers are highly coor- Furthermore, most electrophysiological studies on grasp have
dinated. The earliest studies of grasp attempted to define spe- evaluated pinch and force control (Maier et al. 1993; Smith and
cific patterns of prehension (Griffiths 1943; McBride 1942; Bourbonnais 1981; Smith and Lacquaniti 1981; Smith et al.
Address for reprint requests and other correspondence: T. J. Ebner, Dept. of The costs of publication of this article were defrayed in part by the payment
Neuroscience, University of Minnesota, Lions Research Bldg., Room 421, of page charges. The article must therefore be hereby marked ‘‘advertisement’’
2001 Sixth St. SE, Minneapolis, MN 55455 (E-mail: ebner001@umn.edu). in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
2826 0022-3077/04 $5.00 Copyright © 2004 The American Physiological Society www.jn.org
REACH-TO-GRASP IN THE MONKEY 2827
for each object with the requirement that the monkey successfully and the average force during static object hold were calculated from
complete a trial before a new force window was introduced. A the average traces. Time to enter the force window was defined from
force-sensing resistor (FSR, Interlink Electronics, Camarillo, CA), 1 force onset to when the force trace first exceeded the lower boundary
cm in diameter was located on the face of the smallest cube opposite of the specified force window. The rate of force production was
to the monkey to detect the forces applied by the index or middle defined as the slope of the force trace during the first 200 ms of force
fingers. The remaining 15 objects had a 1.27-cm-diam FSR on the production. In addition, the peak grasp-force rate (GFR) was also
face of each object opposite the monkey. The 5 ⫻ 5 cm start pad was calculated and analyzed (Gordon et al. 1993; Salimi et al. 1999) to
located by the monkey’s side and had a 3.8 ⫻ 3.8 cm FSR on the further probe the correspondence between the force requirements and
superior surface to detect hand contact. production and the objects grasped. The peak GFR was defined as the
The three-dimensional (3-D) positions of monkeys’ wrists, hands, first peak in the grip force rate (e.g., first derivative of the grip force
and fingers were recorded using a video-based motion analysis system trace) immediately after force onset. The average force during static
(Motion Analysis, Santa Rosa, CA). Seventeen reflective markers object hold was defined as the average force once the force trace had
(3-mm diam) were glued to the monkeys’ hands at the following stabilized for 500 ms. A within-subject factorial ANOVA with re-
positions: proximal to the dorsal wrist crease, at the dorsal wrist peated-measures across all conditions was utilized. When justified by
crease, at each finger metacarpophalangeal (MCP), proximal interpha- significant findings, a post hoc Student’s t-test with an adjusted P
langeal joints (PIPs) and distal interphalangeal joints (DIPs), and at value to account for multiple comparisons was calculated. If the
the thumb carpometacarpal joint (CMC), thumb MCP and interpha- findings were significant, the magnitude of effect (2) was calculated
langeal joint (IP) (see Fig. 3). Kinematic data collection was triggered (Howell 1987) to determine how much of the overall variability could
at the onset of the go cue. The markers were monitored with six be explained by the variable of interest. Statistical Analysis Software
cameras throughout the entire reach to grasp (3 s), digitized at 60 Hz, was used for all statistical analysis.
and tracked throughout reach-to-grasp. The position data were filtered The evolution of the hand posture during reach-to-grasp was quan-
with a 6-Hz Butterworth filter. Virtual marker locations approximat- tified using three methods. The first method determined the distance
ing the joint centers were then calculated based on measurements of between the thumb IP joint and the middle finger DIP joint. This
the dissected forearm and hand of monkey G and the diameter of the measurement does not provide any predictable information on the
markers. These virtual marker locations were exported for analyses digit tip positions. Digit tip positions were not monitored and varied
using Matlab and Excel. Cartoons of the hands and eigenpostures with the activity of the flexors/extensors action on the distal phalanx.
were constructed using 3-D rendering software [Persistence of Vision The distance was used as a measure of grasp aperture. The effects of
Raytracer (POVray)]. Note that because the distal marker was located objects and force on average peak aperture were compared using an
on the DIP the positions of the distal phalanges were not monitored ANOVA. A Pearsons’s correlation coefficient was calculated between
and not reconstructed. maximum grasp aperture and object grasp dimension. The second
compared the actual grasps across force levels for each object and
Analyses across the objects for a given force level using root-mean square
(RMS) differences of the 17 marker locations (Mason et al. 2001).
The force traces for each object-force combination were aligned on The results were plotted against time. The ranges of the mean RMS
force onset. The onset was defined as the 20-ms bin when the force differences for each set of curves were calculated.
first exceeded 0.1 N and remained ⬎0.1 N for 400 ms. The aligned The third method utilized SVD analysis (Hendler and Shrager
force traces were averaged for each object-force combination. The 1994) to detect patterns of hand posture during reach-to-grasp across
time to enter the specified force window, the rate of force production, a number of objects. Similar to PCA (Glaser and Ruchkin 1976),
which also identifies patterns, one advantage of SVD is that it pro- ⬍5 cm/s. Movement end was set at this level so as not to include
vides information on the temporal evolution of the identified basis adjustments in wrist position made in the early portion of the object
postures throughout reach to grasp. The calculation of the SVD was grasp. Each hand path and speed trial were aligned on movement
based on the matrix X constructed of the x, y, and z positions of the onset and averaged for the five trials for each object-force calculation.
17 hand markers as a function of time. This included the 12 frames Using the average hand path, the total distance traveled was deter-
before movement onset, the frames during movement, and ⱖ60 mined from movement onset to movement end and compared across
frames (1 s) of static grasp for each of the 16 objects. Matrix X was objects and force levels using a Student’s t-test with correction. The
then deconvolved into three matrixes using X ⫽ U⌺VT. Matrix U peak speed and percent time to peak speed were determined from the
consists of the patterns of the marker positions that defined the average speed profile and compared across objects and force levels
eigenvectors (i.e., eigenpostures). Matrix V consists of the temporal using a Student’s t-test with correction. The magnitude of the effect
weightings of the eigenpostures, a sequence of values that defined the size was calculated to determine how much of the overall variability
contribution of each eigenposture throughout the reach-to-grasp. The can be explained by object (Howell 1987).
superscript T denotes the transpose. Last, ⌺ is a diagonal matrix
consisting of the eigenvalues for the eigenposture-temporal weighting
RESULTS
pair in a greatest-to-least rank order. The eigenvalues indicate the
relative amount of variance explained by each eigenposture-temporal Grasp force
weighting pair. The variances were obtained by squaring the eigen-
values and dividing by the sum of squares. The SVD analysis was Both the rate of force production and grasp force were
completed for each force level separately so as to explicitly compare evaluated for dependence on object. An example of the force
the eigenpostures generated across each force levels as well as across production for all objects and force levels is shown in Fig. 2.
all force levels. Variances accounted for by the eigenpostures were Initially force increased rapidly with an occasional overshoot
compared using a corrected ANOVA as were the means of the finger
positions of the eigenpostures. Phase plane plots of the first two
above the force window before the onset of the target object
temporal weightings were constructed. hold period (e.g., 2 lowest force curves for the smallest cube or
For each reach-to-grasp movement, the hand path was determined the 2nd lowest force curve for the 10-sided polygon). Across
from the wrist crease marker positions and wrist speed (i.e., tangential all sessions and for both monkeys, the time to cross the lower
velocity) was derived from the positional data. Movement onset was threshold of the force window did not differ significantly
defined as a wrist speed ⬎1 cm/s and movement end was defined as across objects [F(14,14) ⫽ 0.82, P ⬎ 0.05] or force level
[F(4,4) ⫽ 4.89, P ⬎ 0.05]. Time to force window did not vary key applied force between the index and middle fingers and the
because, as expected, monkeys generated higher force levels heel of the hand, therefore the thumb remained adducted along
more rapidly than lower force levels. The rate of force produc- the index finger (Fig. 3). For example, the grasp of the rect-
tion in the first 200 ms was significantly different across force angular solid (2nd row) required an open hand. Peak extension
levels [F(4,4) ⫽ 8.57, P ⬍ 0.05] but not across objects of the PIPs was greater than for the 1-cm3 cube. In the final
[F(14,14) ⫽ 0.83, P ⬎ 0.05]. The analysis of peak GFR also hand posture, the MCPs were extended and the DIPs of the
resulted in significant differences across force levels [F(4,4) ⫽ index and middle fingers were positioned in very close approx-
10.32, P ⬍ 0.05] but not across objects [F(14,14) ⫽ 1.10, P ⬎ imation with the more lateral fingers abducted. The hand
0.05]. During the target object hold period the forces generated opened in a similar fashion for the polygon (3rd row), before
were distinct for the five force levels [F(4,4) ⫽ 286.86, P ⬍ flexing at the MCPs and PIPs to enclose the object. The upright
0.05] but did not differ across objects [F(14,14) ⫽ 0.82, P ⬎ cylinder (bottom) was approximately the same size as the
0.05]. Therefore both the generation and maintenance of the polygon. However, the monkey used a different hand orienta-
grasp force were independent of the objects. tion to grasp the object. The hand started in the standard
position with the forearm pronated and the hand resting on the
Hand shape start pad. As the hand reached peak speed, the forearm began
to supinate toward the midposition of forearm rotation. In the
The shaping of the monkey’s hand during reach-to-grasp final hand position, the hand was in neutral forearm rotation,
exhibited several of the characteristics documented for hu- the MCPs and PIPs were flexed, and the index and middle
mans, including preshaping during reach (Jeannerod 1981, fingers were positioned together to apply force to the FSR.
1984; Paulignan et al. 1990). Hand shaping occurred in the Each of the four objects required the monkey to orient its hand
absence of vision. Figure 3 illustrates one monkey’s (G) grasp differently to effectively grasp and apply force on the target
of four different objects at the middle force level (0.3– 0.5 N) object. The changes in the orientation of the hand began with
with its left hand. The shaping of the hand in preparation for reach onset as is evident when the third and fifth hands of each
the grasp began early in the reach and continued to evolve as row are compared. The hand began pronated on the start pad
the hand approached the target. During the reach of the 1 cm3 and rotated to different degrees toward neutral as the reach
cube (top), the thumb was initially abducted and then was progressed. The variations in orientation are evident in the final
gradually brought into opposition so as to oppose the pad of the hand postures.
index finger. The remaining fingers began to extend at the PIPs Monkey L, which was trained on 15 objects, used its thumb
as the monkey lifted its hand off the start pad. The maximum in opposition to the fingers in either a precision grasp or power
extent of extension of the MCPs and PIPs occurred after peak grasp. Therefore the aperture between the thumb IP joint and
speed as the hand began to close in preparation for the pinch the DIP joint of the third finger was determined and related to
grasp. In the final hand posture, the thumb and index finger object dimensions. This finger/thumb opposition differed from
were positioned in opposition. Hand and wrist positions did not the finger/palm opposition favored by monkey G as noted in the
change during the grasp and holding phase of the task because preceding text. Peak apertures for the 15 objects and five force
the objects were rigidly mounted solid structures with noncom- levels for 5 sessions are shown in Fig. 4A. The peak aperture
pliant force sensors mounted on the object surface. was not affected by the grasp force required [F(4,301) ⫽ 0.99,
Finger positions and hand orientations varied with the ob- P ⬎ 0.05]. However, peak aperture was dependent on object
jects grasped. During grasp of the remaining objects, the mon- [F(14,301) ⫽ 240.65, P ⬍ 0.05] and scaled linearly (r ⫽ 0.87)
to the target object grasp dimensions (Fig. 4B). Therefore in the shortly after movement onset during the reach. For the four
absence of vision the aperture of the hand scaled to the object. objects shown, the mean RMS difference (averaged throughout
As described in METHODS, several analyses were used to reach-to-grasp) as a function of force was 11.5 mm (range:
examine the changes in hand shape as a function of force levels 4.5–18.7 mm), implying that the required grasp force affected
and objects. The first analysis was based on the average RMS hand shape minimally. An ANOVA was used to compare the
difference between the 17 markers as a function of force or mean RMS differences for each object as a function of force
object. The RMS differences based on comparing the middle for both animal and all sessions. The RMS differences for the
force levels and the other force levels are shown for four individual objects did not differ significantly (P ⬎ 0.5) with
objects in Fig. 5, A–D. The RMS differences for the different force.
force requirements were small when at the start pad and for In contrast, the RMS differences among hand postures were
most of the reach-to-grasp, particularly during the target object quite large across the objects. In Fig. 5, E and F, the RMS
hold period. There was some increase in the RMS values differences between the grasp of the upright cylinder and all
objects tested at the middle force level (0.3– 0.5 N) for the two
animals are plotted. The mean RMS difference was 63.8 mm
with a range 27.2–184.2 mm. The results show large differ-
ences in hand shape as a function of the objects. The RMS
differences were minimal during the initial hold period, in-
creased during the reach, and were greatest during static hold.
The differences in hand postures for the static grasps of the
different objects were 5–10 times greater than the differences
for the grasps of the same object at the different force levels
(Fig. 5, A–D). An ANOVA was used to compare the mean
RMS differences between the upright cylinder and the other
objects, blocking on session. For each monkey, the mean RMS
difference was significantly difference across the objects [mon-
key G: F(14,36) ⫽ 7.02, P ⬍ 0.05; monkey L: F(13,34) ⫽
20.92, P ⬍ 0.05]. The RMS differences reflect changes in hand
aperture, in hand shape (e.g., relative angles of different joints),
and hand orientation (see Fig. 3) that are highly dependent on
the object grasped and much less dependent on the grasp force.
The second analysis was based on an SVD analysis of hand
postures, deriving “eigenpostures” (Figs. 6 and 7). The first
eigenposture can be characterized as an open hand posture with
the MCPs and PIPs in approximately mid-flexion (Fig. 6). By
definition, E2 is orthogonal to E1 and consisted of hyperex-
tension of the MCPs and PIPs (Fig. 6). The second eigenpos-
ture contributed to the opening and closing the hand during the
reach. Across objects for each force level or across all objects
and force levels, the first eigenposture (E1) explained on av-
erage 93.5% of the variance and the second eigenposture (E2)
explained on average 4.9%. The third eigenposture explained
only 1% of the variance not shown. E1 and E2 were similar
across days and animals (Fig. 7).
The eigenpostures were not dependent on grasp force (Fig.
6). The variance accounted for by E1 and E2 were not signif-
icantly different across force levels [for E1, F(5,5) ⫽ 0.28, P ⬎
0.05; for E2, F(5,5) ⫽ 0.41, P ⬎ 0.05]. Similarly, the means of
the finger positions for the two eigenpostures were not depen-
dent on force [for E1, F(5,5) ⫽ 0.07, P ⬎ 0.05; for E2,
F(5,5) ⫽ 2.44, P ⬎ 0.05]. These findings reinforce the other
observations that grasp force had minimal effect on hand
shape.
Phase plane plots of the temporal weightings of E1 versus
E2 demonstrated how the two components differentially con- FIG. 6. Eigenpostures as a function of grasp force. The 1st row shows E1
tributed to object grasp. In Fig. 8, A–D, the phase plane plots and E2 obtained from the hand position data across all objects and force levels.
for the five force levels and four objects are illustrated. At the The remaining rows illustrate the E1 and E2 across all objects at each force
level. Data are from 1 session of monkey G.
onset of reach, the weighting of E1 decreased while the weight-
ing of E2 increased. This weighting shows that E2 contributed similar for a particular animal, reinforcing the concept that a
to the initial hand opening. Further opening of the hand in- global synergy is operative and that by simply varying the
volved increasing the weight of E1 and slowly decreasing the amplitude and timing of E1 and E2 the hand can be shaped.
weight of E2. After peak opening of the hand, the weighting of The eigenpostures and their temporal weightings suggest that
E2 decreased quickly, initiating the hand closure. The unique the CNS uses a simplifying strategy to control the hand during
shaping of the hand for each object is reflected in the diver- reach-to-grasp. Last, the phase plots varied very little with
gence of the curves after peak speed. For the small cube (Fig. grasp force (Fig. 8, A–D) underscoring the findings that hand
8A), the closure to precision grasp involved the simultaneous shape is independent of force.
decrease in the weighting of E1 and E2 after the end of wrist
movement. This was interrupted by a brief increase in the Reaching
weighting of E1. In contrast, closure of the hand on the
rectangular solid (Fig. 8B) resulted from a rapid decrease of the Wrist paths were highly consistent across force levels and
weighting of E2 that was followed by a rapid decrease in the objects. This occurred without vision of both the hand and
weighting of E1. In contrast, for the 10 sided polygon (Fig. target. As shown in Fig. 9, A and B, the wrist paths to three
8C), E1 and E2 decreased simultaneously. However, the over- objects at the five force levels were slightly curved as the
all shape of the phase plot profiles for different objects were animal reached slightly upward and approached the target
J Neurophysiol • VOL 91 • JUNE 2004 • www.jn.org
REACH-TO-GRASP IN THE MONKEY 2833
The entire hand, not just the thumb and index finger, was
shaped for each object. This is evident in the analysis of the
RMS differences of finger positions in which large differences
were observed for the various objects. These differences de-
veloped during the reach and were maintained during the static
grasp period. The differential shaping of the monkey’s hand
was also evident in the phase plane plots of the temporal
weightings for E1 and E2. The trajectories began to diverge
about the time of peak speed and continued to diverge until a
stable grasp is achieved. The divergence represents the differ-
ences in the hand opening and closing for the enclosing of the
object of various sizes and shapes. The occurrence of peak
aperture after the peak speed is similar to the preshaping of the
hand for object grasp in humans (Jeannerod 1984; Paulignan et
al. 1990). These findings are also consistent with human stud-
ies showing that by midway through the reach the hand shape
begins to reflect the object to be grasped and culminates with
object contact (Santello et al. 1998). Like the human (Mason et
al. 2001), the monkeys utilized a specific hand shape for each
object rather than use a default shape or simply opening and
closing the hand around the object.
It is possible that constraints on hand shaping were intro-
duced by the task design due to the placement of the force
sensors on the object, the force production requirements, and
the rigid mounting of the objects. However, these results sug-
gest that the monkeys targeted object grasp strategies over
force production requirements and FSR positioning when shap-
ing the hand. Specifically, hand-shaping preferences varied
across objects and across each monkey for the same object. For
example, monkey G used a precision grasp (e.g., thumb in
FIG. 9. Wrist paths and speed profiles for different objects and forces. A
and B: 3-dimensional reconstruction of the wrist path for the 5 force levels for
opposition of the fingers) only for object 1 but preferred to used
objects 1 (A) and 13 (B). C: wrist paths for all objects at the middle force level. a palm/finger opposition for all remaining objects. In contrast,
E, the end of the reach. D and E: speed profiles of the wrist during the monkey L preferred to use either a precision or power grasp
reach-to-grasp for objects 1 (D) and 13 (E) for the 5 force levels. F: speed with its thumb in opposition to the fingers. The hand-shaping
profiles for all objects at the middle force level for monkey G. Each wrist path preferences across both objects and monkeys is most likely a
and speed profile is the average of 5 trials aligned on movement onset from
monkey G. reflection of each primates’ grasping preference. Furthermore,
these preferences appear to have more to do with the object
or hand synergies. These basis postures are also independent of shape, size, and orientation as well as hand size rather than
grasp force. predominantly on the location of the FSR on the object. If the
monkeys’ movements were predominantly targeted on force,
Hand shaping during reach-to-grasp then it is unlikely that such a variation of hand postures across
both objects and monkeys would exist (this is especially true
Hand shape evolved throughout the entire task sequence. At given that all FSRs were place in the same frontal position on
the initiation of the reach, the monkeys extended their fingers all objects). Another constraint imposed by the experimental
to release the start pad. Finger extension during the first phase design was the rigid fixation of the object. It is probable that
of transport has been noted in human grasp (Jeannerod 1981, the grasp of a free-standing object would have resulted in
1984; Marteniuk et al. 1990; Paulignan et al. 1990). Some different grasp strategies to ensure stability of the object and
researchers have argued that hand shaping in humans may hand. When the same reach-to-grasp task was performed by
actually begin prior to the initiation of reach (Jeannerod and human subjects, grasp of free-standing objects resulted in a
Biguer 1982; Mason et al. 2001). For the monkeys, the posi- greater variability in both hand shaping and grasp force when
tions of the fingers and orientation of the hand varied in compared with the grasp of rigidly mounted objects (Hendrix
preparation for the grasp of different objects as the reach and Ebner 2003). Further studies are needed to examine how
progressed. Furthermore, the shaping reflected the grasp di- object fixation alters both the behavior strategy and the under-
mension of the object. The hand aperture (based on the span lying neural control.
between the thumb and middle finger) scaled with the object The unique shaping of the hand for the different objects was
size. Although scaling of maximum aperture to object size has achieved without vision of the hand or object. Therefore much
been observed previously in humans and the monkey (Bootsma of the evolution of the hand shape during reach-to-grasp can be
et al. 1994; Fraser and Wing 1981; Jeannerod 1984; Marteniuk achieved via feedforward control and proprioceptive/tactile
et al. 1990; Roy et al. 2000, 2002), this study demonstrates that feedback. A similar control strategy can also be observed
scaling also occurs to a large group of objects of different during normal human grasping (Jeannerod 1984; Mason et al.
shapes and sizes. 2001; Santello et al. 1998, 2002). Human subjects without
J Neurophysiol • VOL 91 • JUNE 2004 • www.jn.org
REACH-TO-GRASP IN THE MONKEY 2835
vision of the object exhibit most of the properties described for hand postures or hand synergies. E1 explained an average 93%
hand shaping with vision. For example when human subjects of the variance and E2 an additional 4 –5%. These two eigen-
are able to see the object but not their hand, the maximum grip postures, an open hand flexed posture (E1) and an extended
aperture remains a function of object size (Jeannerod 1984; posture (E2), are modulated in differing contributions through-
Wing et al. 1986). When subjects shape their hands out of view out reach to achieve the final hand posture. The consistency
and grasp different cubes, the joint angles of the fingers vary across days, grasp forces, and monkeys implies that these hand
linearly with cube sizes (Santello and Soechting 1997). Other synergies are integral to how these animals grasp the selected
recent studies in humans show that hand preshaping occurs in objects. The consistency is strengthened by the observation
the absence of continuous vision of both the hand and object that the animals used somewhat different strategies to grasp the
(Schettino et al. 2003; Winges et al. 2003) as well as under objects. The same synergies can describe both strategies.
memory-guided reach-to-grasp (Santello et al. 2002). The re- The basis postures in the monkey were remarkably similar to
sults of this study and other human studies show that hand- those observed in human reach-to-grasp (Mason et al. 2001;
shaping synergies are similar across human and non-human Santello and Soechting 1997; Santello et al. 1998, 2002). For
primates and that vision is not necessary for such synergies to humans with vision of their hands and objects, E1 also consists
be operative. of an open hand with flexed fingers and E2 consists of hyper-
If hand shaping occurs in the absence of vision, then what extension of the fingers. The variance accounted for by the first
role does vision play in hand shaping? It has been suggested two principal components in humans (⬃75– 85%) is somewhat
that vision may be used primarily to localize the position of the less than that observed in the monkey (Mason et al. 2001;
object in space and may play less of a role in the actually Santello et al. 1998; 2002). This difference in variability is
shaping of the hand to the object (Santello et al. 2002). Other likely a reflection of the much more diverse object set used in
more salient factors, such as the transport component of the the human studies. In addition, unlike the human studies, the
grasp and the size and shape of the object (Schettino et al. DIP angles were not recorded in the current study and could
2001), appear to be the determinants of hand shaping rather have also contributed to a difference in the overall variance
than vision. Although a rigorous examination of reach-to-grasp accounted for in the first two principle components. The sec-
with and without vision of the hand and object was not done in ond basic posture in humans adds a great deal of the shaping
this study, our findings are consistent with human hand-shap- needed for the different objects (Santello et al. 1998, 2002).
ing studies showing that shaping of the whole hand and grasp The findings are similar in the monkey. The phase plots of E2
aperture also occur in the absence of vision. versus E1 show that the contribution of E2 to the grasp begins
In interpreting the hand-shaping results and the SVD anal- during the reach and then increases in importance. Therefore
ysis described in the following text, a comment on the objects the basis postures and the timing of their contributions to hand
studied is needed. The object shapes and sizes, and the corre- shape are similar for humans and monkeys.
sponding hand postures only represent a limited subset of the Not only are these hand postures the same for humans and
full repertoire of hand shapes and grasps that can be achieved monkeys, the postures are relatively unchanged whether the
by the monkey. Therefore the interpretation of the factors grasp is real or mimed (Mason et al. 2001). The present study
affecting the preshaping of the hand and the hand synergies shows that the basis postures are not dependent on grasp force
used must be limited to the objects studied. and occur in the absence of vision of the hand and object.
Tactile sensory input also plays a limited role in defining these
Reach basis postures in humans (Santello et al. 2002). Reaching to
virtual objects versus real objects alters the principal compo-
The kinematics of the reach component were comparable to
nents primarily at the time of object contact. Therefore the
human kinematics (Jeannerod 1981, 1984; Marteniuk et al.
similarities in the basis postures and their relative invariance in
1990; Paulignan et al. 1990). The hand path was U-shaped and
humans and monkeys suggest that these synergies are funda-
was consistent across force levels within an object. The diver-
mental to the control of reach-to-grasp. We propose that these
gence of the hand paths at the end of the reach for the different
hand synergies reduce the complexity of controlling the hand
objects was related to the required orientation of the hand to
as has been suggested previously (Mason et al. 2001; Santello
grasp the object. The wrist speed profile was bell-shaped as for
and Soechting 1997; Santello et al. 1998, 2002).
reaching movements (Abend et al. 1982; Georgopoulos et al.
The neural substrate underlying the hand synergies remains
1981; Soechting and Lacquaniti 1981) and for reach-to-grasp
to be defined, although several observations point to possible
(Jeannerod 1984; Marteniuk et al. 1990; Paulignan et al. 1990;
neural correlates. In a preliminary report, a factorization algo-
Roy et al. 2000; Wallace and Weeks 1988). Both the hand path
rithm was used to extract a small number of EMG postures
and the speed were not affected by the required force level and
from extrinsic hand muscles during reach-to-grasp in a monkey
only minimally affected by object. The fact that reach varied so
(d’Avella et al. 2002). These time-varying muscle synergies
little as a function of grasp force and object removes the
may underlie the basis postures described in this report and in
possible confound that alterations in the reach contributed to
humans (Mason et al. 2001; Santello and Soechting 1997;
the shaping of the hand or the hand synergies. This is a
Santello et al. 1998, 2002) Our initial description of the dis-
particularly salient issue when examining the neural mecha-
charge properties of primary motor cortex neurons during
nisms underlying reach-to-grasp.
reach to grasp reveals temporal firing patterns that scale with
the different objects (Mason et al. 2002). Furthermore, the
Hand synergies
firing was significantly modulated in relation to object proper-
The SVD analysis demonstrates that a large amount of the ties. Both findings are consistent with encoding of global
complexity of reach-to-grasp can be reduced to a few basic aspects of hand shape such as hand synergies. Recently Lemon
J Neurophysiol • VOL 91 • JUNE 2004 • www.jn.org
2836 C. R. MASON, L. S. THEVERAPPERUMA, C. M. HENDRIX, AND T. J. EBNER
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