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Exp Brain Res (2009) 199:59–70

DOI 10.1007/s00221-009-1972-5

RESEARCH ARTICLE

Palmar arch modulation in patients with hemiparesis after


a stroke
Archana P. Sangole Æ Mindy F. Levin

Received: 26 April 2009 / Accepted: 29 July 2009 / Published online: 19 August 2009
Ó Springer-Verlag 2009

Abstract Hand shape modulation has traditionally been P \ 0.001) in palmar arch modulation particularly during
studied within the framework of reach-to-grasp tasks by P3 wherein fine adjustments are made to the grip in prep-
examining the control of arm transport, grip aperture aration for object manipulation. While control subjects
scaling, and finger joint excursions. However, global completed most of hand shape modulation early in the task,
parameters characterizing arm and hand movement can be stroke survivors took longer to complete each phase. Fur-
enhanced by additional knowledge of biomechanical thermore, stroke survivors started with a flatter hand which
changes in the hand. We previously examined palmar arch required relatively more arch modulation during the latter
modulation during grasping in healthy subjects by identi- part of the task, thereby reflecting a temporal and spatial
fying thenar and hypothenar displacement. This method concurrency between the phases. Stroke survivors with
was used to characterize hand shape modulation in 10 well-recovered hand grasping ability tended to incorporate
stroke survivors with mild hand paresis, as assessed by the compensations/adaptations in hand posture during specific
Chedoke-McMaster clinical scale, during two types of grasping phases. Palmar arch analysis provides us with a
grasps (spherical, cylindrical). Palmar arch modulation was more complete understanding about how hand biome-
examined during the three phases of prehensile movement: chanics, specifically palmar concavity articulation, is
transport shaping (P1), preshaping (P2), and contact changed post-stroke. This will allow us to better identify
shaping (P3). Compared to the control group, the stroke the motor compensations used for grasping and to re-focus
survivors showed significant differences (spherical: rehabilitation interventions to reduce compensations and
F2,18 = 12.025, P \ 0.001; cylindrical: F2,18 = 9.054, improve functional motor recovery.

Keywords Prehension  Grasp  Hand posture 


A. P. Sangole (&)
Preshaping  Palmar arch  Hand biomechanics 
Department of Mechanical Engineering,
Ecole Polytechnique, 2900 Edouard-Montpetit, Reaching  Stroke
Montreal, QC H3T 1J4, Canada
e-mail: archana.sangole@polymtl.ca
Introduction
A. P. Sangole
Sainte-Justine University Hospital Center,
Montreal, QC, Canada Reach-to-grasp tasks have been primarily described by how
the hand is transported to the object (arm transport) and
M. F. Levin
how arm–hand movement is modulated in preparation for
Center for Interdisciplinary Research in Rehabilitation,
Montreal, QC, Canada and during grasping (hand shape modulation; for review,
e-mail: mindy.levin@mcgill.ca see Sangole and Levin 2007). From the perspective of
understanding the control of hand function, the classical
M. F. Levin
theory explains prehension as a system of two independent
School of Physical and Occupational Therapy,
McGill University, 3654 Promenade Sir-William-Osler, visuomotor channels comprised of a transport component
Montreal, QC H3G 1Y5, Canada and a grasp component (Jeannerod 1984, 1999).

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60 Exp Brain Res (2009) 199:59–70

Alternative perspectives are that prehensile movement is a and has been extensively used as a descriptor in reach-to-
complex or higher order motor behavior consisting of grasp related studies (Castiello 2005). However, by the
elementary actions that occur concurrently in a given time time of maximal grip aperture, hand shape modulation has
window (Smeets and Brenner 1999; van Bergen et al. 2007; already occurred and all that remains is the action of hand
Sangole and Levin 2008b) or as a result of a change from closure on the object. Previous studies have shown that in
one frame of reference to another (Pilon et al. 2007; stroke survivors, grip aperture scaling to object size is
Feldman et al. 2007; Ma and Feldman 1995). The ele- preserved and despite longer reaching and grasping times,
mentary motor actions occurring concurrently involve arm- the relative time to maximal aperture occurs earlier than in
transport, grasp, hand rotation, or orientation (Soechting healthy controls (Michaelsen et al. 2009). On the other
and Flanders 1993; Stelmach et al. 1994; Desmurget et al. hand, tasks performed using compensatory strategies to
1995, 1996, 1998; Desmurget and Prablanc 1997; Rand and facilitate hand opening (such as using the object to open the
Stelmach 2005; Paulignan et al. 1990; Mamassian 1997, hand) can be characterized by a maximal grip aperture
van Bergen et al. 2007) and hand-shape modulation which is similar in magnitude to healthy subjects because it
(Sangole and Levin 2008a, b). Much of the understanding is dictated by the size of the object. From the standpoint of
of hand function has been derived from examining how the designing effective treatment interventions, not only is it
grip aperture changes during arm transport (Santello and important to know where there is a deficit, e.g., differences
Soechting 1997, 1998; Gentilucci et al. 2003; Saling et al. in grip aperture, but also it is necessary to know why there
1996) or the angular excursion of finger joints during is a difference, e.g., weakness in the thenar or hypothenar
grasping (Kamper et al. 2003; Santello et al. 1998, 2002; muscles causing either flattening of the hand or unstable
Mason et al. 2001; Ansuini et al. 2006). grip. While the measure of maximal grip aperture can be
While temporal and spatial relationships between the used to describe deficits in the coordination of reaching and
elementary motor actions (Rosenbaum et al. 1995; Rossi grasping and the ability to preshape the hand to object
et al. 2002), e.g., arm–hand and trunk–arm coordination dimensions and orientation, it does not provide insights
have been well-described, there is still limited knowledge into the underlying associated biomechanical changes of
about how stroke impacts each action. A better under- the hand, which are likely to exist concomitantly. Char-
standing of the motor deficits in post-stroke patients may be acterizing grasping deficits may require descriptors more
gained by characterizing changes in each elementary action specific to the hand which may not be apparent in measures
of grasping within the framework of the whole task. Stroke related to a global characterization of arm or finger
survivors with upper limb hemiparesis often have difficulty movement.
manipulating objects during functional tasks (Brunnstrom One such descriptor that may provide important addi-
1970; Fries et al. 1993; Lai et al. 2002; Muellbacher et al. tional biomechanical information about hand shape mod-
2002). Grasping deficits have been described in terms of ulation in subjects with stroke is that of the palmar arch
altered hand orientation as the hand approaches the object (Sangole and Levin 2008a, b). The palmar concavity plays
which may be related to compensatory movement strategies an essential role in hand shape modulation to ensure a
of the arm and trunk (Roby-Brami et al. 2003; Michaelsen secure or stable grasp conforming to the intended use of the
et al. 2004). While altered movement strategies and their object (Kapandji 1982; Lewis 1977; Landsmeer 1962).
compensations for reaching and grasping have been descri- Palmar dynamics during two types of power grasping have
bed such as increased shoulder elevation, reduced elbow been previously described in healthy subjects. Prehensile
extension, and shoulder horizontal adduction accompanied movement was divided into three components of hand
by excessive trunk movement (Roby-Brami et al. 2003; shape modulation: transport shaping, preshaping, and
Cirstea and Levin 2000), there is less evidence associating contact shaping. Transport shaping reflects hand shape
these strategies with deficits in the ability to modulate hand modulation as the arm extends to reach for the object
configuration or aperture (e.g., Michaelsen et al. 2004). (during the transport component). The other two phases
The grasp component of reaching is composed of at characterize the grasping component: preshaping is the
least two phases, one that adjusts the hand configuration modulation of the hand as it begins to encompass the object
and aperture according to object shape and orientation and contact shaping reflects the fine adjustments to the
(opening phase) and another that closes the hand and fin- grasp during the initial stages of the intended use of the
gers on the object (closure phase). As the hand reaches to object. We hypothesized that post-stroke patients would
grasp an object, the grip aperture attains a maximal width, have deficits in the ability to conform the palm to the object
and then begins to establish contact with and encompass which would lead to problems in grasping and object
the object (Jeannerod 1984). The time at which maximal manipulation. In addition, a deficit in the ability to ensure a
grip aperture is attained is a fundamental kinematic land- stable grasping interface may lead to the adoption of
mark commonly used to describe hand shape modulation movement compensations at the hand or arm level,

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Exp Brain Res (2009) 199:59–70 61

ultimately interfering with motor recovery (Alaverdashvili encourage a more natural reaching and grasping movement
et al. 2008). Therefore, in this study, we characterized hand pattern (Trombly 1992; Ada et al. 1994; Chen et al. 2008).
shape modulation during object manipulation involving the Subjects were seated in a comfortable chair with a back
whole hand in individuals with post-stroke hemiparesis. In support. In the initial position, the hand was placed on an
addition, hand opening and closing was divided into three adjustable platform with the arm positioned at approxi-
phases in order to examine which phase is most affected mately 45° shoulder abduction, 90° elbow flexion, and the
and the associated impact on the biomechanics of palmar forearm in 90° pronation (Fig. 1). Objects were placed at a
concavity formation which cannot be derived from discrete distance of 90% of the subject’s arm length in the sagittal
parameters such as maximal grip aperture. plane in front of the ipsilateral shoulder on an adjustable
table, approximately 5 cm above the initial hand position
(Mark et al. 1997; Levin et al. 2002). Arm length was
Materials and methods measured as the distance between the medial border of the
axilla and the wrist crease. The participants grasped the
Subjects object and transported it medially to a surface, approxi-
mately 10 cm higher than the initial support surface, also
Study participants included ten stroke survivors (4 women, located at 90% of the arm’s length just beyond the midline
mean age 65 ± 9 years, range 51–79) with hemiparesis, before returning the hand to the initial position. The initial
see Table 1 and eight healthy adult volunteers (4 women, and final hand and object positions were standardized
mean age 55 ± 10 years, range 41–68). The control group across subjects and trials for both grasping tasks. Move-
participants were right-handed and had no history of injury ment was initiated in response to a verbal cue and subjects
to the hand or arm. Stroke survivors had a diagnosis of were asked to perform the activity at a comfortable speed.
unilateral stroke and were at least 4 months post-stroke at
the time of the study. Those with some functional arm and Data recording and analysis
hand movement [Chedoke-McMaster Hand Assessment
Scale (Gowland et al. 1993) C 3] were included. All par- A six-camera ViconÒ motion analysis system was used to
ticipants were informed of the aim of the study and signed record three-dimensional movement of the arm and hand.
consent forms approved by the local Ethics Committee. Reflective markers (5-mm) were placed on the radial and
Tasks were performed by the affected side in the stroke ulnar styloids of the wrist, with two additional markers
survivors and the dominant side in the control group. placed on the forearm. Hemispherical reflective markers
(3-mm) were attached to the dorsum of the hand and the
Experimental procedure finger joints. The marker configuration is illustrated in
Fig. 2a. The two markers at the base of the 2nd and 5th
Hand shape modulation was examined during two natural metacarpal bones (MCP) constituted the carpal markers
power grasps—spherical (ball: 10.5 cm diameter) and and the respective landmark for the palmar arch formula-
cylindrical (plastic glass: 8.5 cm diameter, 14 cm high). tion was calculated by bisecting the line segment con-
Participants performed 10 trials in separate blocks for each necting these two markers. Data were recorded at 120-Hz
grasp type. Object transport and manipulation components for 8 s and filtered using a second order Butterworth filter
were included in order to replicate a functional task so as to with a cut-off frequency of 10 Hz.

Table 1 Clinical and


Subject Sex Age Side of Time since Chedoke-McMaster Purdue test Dominant
demographic data of the stroke
(yrs) hemiparesis injury (yrs) score arm/hand LA/A side side
survivors
S1 F 55 Left 9 4/3 10/3 R
S2 F 60 Left 2 5/4 9/5 R
S3 F 67 Left 3.2 7/7 13/10 R
S4 M 68 Left 1.9 5/6 13/2 L
S5 M 77 Right 6 5/6 9/4 L
S6 F 79 Left 4.2 4/5 11/3 R
The maximal score for both the S7 M 59 Right 2.1 7/6 13/9 R
arm and hand on the Chedoke- S8 M 67 Right 3.3 5/5 11/6 L
McMaster scale is 7 S9 M 70 Right 3.1 4/3 10/1 R
LA less affected, A affected, S10 M 51 Left 1.4 7/3 10/0 R
R Right, L Left

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62 Exp Brain Res (2009) 199:59–70

included the initial portion of the object manipulation


phase since fine adjustments occur to the grip as object
Adjustable
manipulation begins, i.e., phase 3 as identified in our
height method. The same has been shown in our earlier study
Adjustable (Sangole and Levin 2008a, b). The tangential velocity was
height
computed by numerical differentiation of the x, y, and z
coordinates. Movement onset was defined as the time at
Adjustable
height which the tangential velocity of the ulnar marker exceeded
and remained above 5% of the peak wrist velocity. This
Fig. 1 Schematic illustration of the experimental set-up and the two time was referred to as zero-ms for subsequent data anal-
grasp types (spherical and cylindrical)
ysis. The end of the movement (end of task) was defined as
the instance when maximal tangential velocity was attained
The prehensile movement was divided into three phases during object transport. This definition of task phase
(P1: transport shaping, P2: preshaping, and P3: contact includes fine adjustments in hand shape modulation up
shaping) using the tangential velocity trace of the ulnar until the initial stages of object transport (Sangole and
marker of the wrist (Fig. 2b). Phase 1 (P1) involved hand Levin 2008a, b). Two parameters were measured at the
movement from onset to the time of maximal wrist beginning of each phase and at the end of the task: palmar
velocity; phase 2 (P2) extended from the end of P1 to the arch position and time.
time when object transport began, i.e., the first minimum of We defined the palmar arch as being composed of two
the tangential velocity trace; and phase 3 (P3) extended components (thenar and hypothenar) articulating with a
from the end of P2 to the time of maximal velocity of rigid middle plane formed by the carpus-index MCP-mid-
object transport, i.e., second peak in the wrist tangential dle MCP. This formulation was considered reasonable
velocity trace, also considered to be the end of task (END). because there is little or no relative movement between the
While ‘preshaping’ in phase 2 reflects initial hand–object respective carpo-metacarpal joints of the index and middle
contact, movements in phase 3 reflect the fine adjustments fingers (Levangie and Norkin 2001). The thenar and
in grip posture that occur during object stabilization at the hypothenar components are henceforth referred to as the
time of object transport, hence the term ‘contact shaping’. thenar arch and the hypothenar arch, respectively. The
Current methods generally define the end of grasp at the thenar arch was defined using the carpus, thumb MCP, and
completion of arm transport (at the end of phase ‘2’). We index finger MCP, while, the hypothenar arch was defined

Fig. 2 a Marker configuration (A)


on the hand and wrist (dorsal
view), and b Phases of the
reach-to-grasp movement (P1:
transport shaping, P2:
preshaping, P3: contact shaping;
separated by vertical dotted
lines) identified in the tangential
velocity trace of the wrist ulnar
marker for a control subject (left
panel) and a representative trial
of a stroke patient (right panel)

(B) P1 P2 P3 P1 P2 P3
500
Tangential velocity (mm/s)

400

400
300
300
200
200

100
100

0 0
0.00 0.25 0.50 0.75 1.00 1.25 1.50 0.00 0.50 1.0 1.50 2.00 2.50
Time (s) Time (s)

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Exp Brain Res (2009) 199:59–70 63

Fig. 3 Biomechanical (A) (B)


formulation of the palmar arch: Ring Middle
a dorsal view showing the MCP MCP Index
Little MCP
markers used for the arch
hypothenar MCP
definition and the respective Thumb
planes and b transverse view at plane
Hypothenar
the metacarpal joint (MCP) middle MCP
arch
level plane Thenar
arch

thenar Palmar arch = thenar arch +


plane hypothenar arch

using the carpus, middle finger MCP, and little finger MCP. each phase and phase-wise change in arch angle), thenar–
Thus, the biomechanical formulation of the palmar con- hypothenar contributions, (b) total task time and the time
cavity combined the articulations of the thenar and hypo- required to complete each phase, (c) and MCP-PIP linearity
thenar arches (Fig. 3a, b). A smaller angle reflects more for each grasp type. A mixed design ANOVA with factors
concavity. This characterization helped to identify thenar group (stroke, control) and phase (P1, P2, P3, End position)
and hypothenar contributions to the palmar arch formation was used. Comparisons between grasp types were done
and is therefore more descriptive of hand function. only for the total task times and the three phase completion
Movements of the thumb are reflected in the thenar arch times. Post-hoc comparisons were adjusted using Bonfer-
and those of the 5th metacarpal are captured in the hypo- roni’s correction. Correlations between palmar arch mea-
thenar arch. Additional details are provided in Sangole and sures and clinical scores of hand motor impairment and
Levin (2008a, b). function [Chedoke-McMaster and Purdue scores (Backman
In order to examine phase-wise differences in grasping et al. 1992)] were computed with Pearson statistics. An
patterns between the two groups, the change in palmar arch initial significance level of P \ 0.05 was used for all tests.
angle and in thenar–hypothenar contributions during each
phase was calculated by expressing the change in angle in
each phase (P1, P2, P3) as a percentage of the total change Results
from the beginning of P1 to END (Sangole and Levin
2008b). The total task time and time taken to complete Phase-wise changes in palmar arch modulation
each phase were also compared. For each subject, these and thenar–hypothenar contribution
values were averaged across trials. Coordination of the
index and middle fingers was investigated by examining For each task, palmar arch measures at the beginning of
the linearity between the angular displacements at the each phase (P1, P2, P3) and at the end of the task were
metacarpal (MCP) and proximal phalangeal (PIP) joints of compared. The values at the initial position (P1) and at the
each finger. Those trials in which the trajectories could not end of the task were similar between groups (Table 2) but
be successfully reconstructed due to missing markers were the hand was flatter (greater arch angle) in the stroke group
excluded (approximately 20%). prior to object contact (beginning of P3) for both the
In a power grasp, the thumb, index, and middle fingers spherical (F2,18 = 4.097, P \ 0.05; P3: P \ 0.001) and the
play an essential role (Napier 1956). Since our biome- cylindrical grasp (F2,18 = 18.7, P \ 0.001; P3:
chanical formulation of the palmar arch takes into account P \ 0.001).
the MP joint of the thumb, its modulation would be Figure 4a illustrates phase-wise arch modulation as a
reflected in that of the thenar arch, while the same is not percentage of the total, e.g., P1 as a percentage of
true for the index and middle fingers. Therefore, in the P1 ? P2 ? P3. Arch modulation, throughout the three
analysis, the relative motions of the MCP and PIP joints of phases of grasp for each grasp type differed between
the index and middle fingers were examined for linearity. groups (spherical: F1,2 = 12.025, P \ 0.001; cylindrical:
From related studies (Kamper et al. 2003), it was hypoth- F1,2 = 9.054, P \ 0.001). The stars indicate the phases in
esized that there is a linear relationship between the which significant differences were observed between
movements of the MCP and PIP joints of the index and groups. Most of the hand modulation occurred in P1
middle fingers. (P \ 0.002, spherical: control 45% ± 15, stroke
The analysis thus included separate comparisons of (a) 40% ± 15; cylindrical: control 63% ± 14, stroke
palmar arch modulation (arch angle at the beginning of 43% ± 14). In the cylindrical grasp, the stroke subjects

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64 Exp Brain Res (2009) 199:59–70

Table 2 Measures of palmar arch angle in initial and final positions (palmar arch = thenar ? hypothenar) at the beginning of each phase (P1,
P2, P3) and at the end of the task (End) in the reach-to-grasp task in control (C) subjects and in subjects with stroke (S)
Subject Spherical Cylindrical
P1 (deg) P2 (deg) P3 (deg) End (deg) P1 (deg) P2 (deg) P3 (deg) End (deg)

C1 123 ± 8 118 ± 4 109 ± 2 108 ± 4 130 ± 7 115 ± 3 103 ± 6 104 ± 2


C2 128 ± 8 100 ± 7 103 ± 3 90 ± 7 120 ± 5 102 ± 2 105 ± 1 100 ± 1
C3 124 ± 5 107 ± 9 97 ± 3 92 ± 7 120 ± 6 108 ± 2 106 ± 2 105 ± 3
C4 120 ± 7 114 ± 1 110 ± 1 107 ± 6 119 ± 5 108 ± 1 110 ± 2 105 ± 2
C5 138 ± 10 119 ± 2 108 ± 2 107 ± 2 130 ± 11 111 ± 2 105 ± 1 105 ± 1
C6 108 ± 5 102 ± 4 99 ± 1 93 ± 10 106 ± 3 95 ± 9 97 ± 8 99 ± 2
C7 124 ± 3 120 ± 3 105 ± 2 104 ± 6 124 ± 4 114 ± 2 104 ± 2 107 ± 14
C8 123 ± 2 112 ± 2 116 ± 4 114 ± 4 126 ± 2 109 ± 1 110 ± 2 111 ± 3
Avg ± SD 124 ± 8 112 ± 8 106 ± 6* 102 ± 8 122 ± 8 108 ± 6 105 ± 4* 105 ± 4
S1 125 ± 3 123 ± 5 114 ± 4 118 ± 5 121 ± 4 116 ± 3 109 ± 3 108 ± 4
S2 131 ± 13 123 ± 6 120 ± 7 120 ± 4 137 ± 1 120 ± 17 121 ± 6 112 ± 21
S3 138 ± 5 108 ± 15 113 ± 6 97 ± 11 111 ± 34 94 ± 31 97 ± 12 86 ± 16
S4 139 ± 8 122 ± 3 112 ± 4 106 ± 2 141 ± 6 127 ± 12 118 ± 13 112 ± 4
S5 134 ± 8 127 ± 2 114 ± 1 112 ± 4 129 ± 5 114 ± 5 107 ± 4 98 ± 3
S6 126 ± 3 109 ± 24 100 ± 16 98 ± 19 119 ± 5 117 ± 5 107 ± 7 100 ± 16
S7 122 ± 3 111 ± 1 102 ± 2 100 ± 5 121 ± 1 108 ± 5 109 ± 14 102 ± 2
S8 120 ± 3 117 ± 1 109 ± 4 102 ± 2 120 ± 9 117 ± 2 115 ± 4 101 ± 11
S9 138 ± 9 139 ± 5 128 ± 6 124 ± 4 136 ± 8 130 ± 8 119 ± 11 101 ± 1
S10 135 ± 4 88 ± 14 103 ± 10 89 ± 3 133 ± 2 n/a n/a 98.6
Avg ± SD 131 ± 7 117 ± 14 112 ± 9 107 ± 10 127 ± 10 116 ± 10* 111 ± 7* 102 ± 8
* Difference between groups (P \ 0.001)

modulated hand shape more than the control subjects in P2 contributions differed for each grasp type similarly in both
(P \ 0.01, control 23% ± 14, stroke 32% ± 12) and P3 groups. For the spherical grasp, there was more thenar
(P \ 0.001, control 14% ± 9, stroke 25% ± 11). The contribution to the total arch modulation (palmar concav-
pattern of relative phase-wise change differed in each ity) during P2 (control: thenar 49° ± 9, hypothenar
group (Fig. 4b, c bottom panels). In the stroke group, 63° ± 5; stroke: thenar 48° ± 13, hypothenar 68° ± 5;
palmar arch shape changed less in P1 and more in P2 and P \ 0.01) and P3 (control: thenar 47° ± 7, hypothenar:
P3 compared to the control group for both grasp types 59° ± 5; stroke: thenar 47° ± 10, hypothenar 59° ± 5;
(P \ 0.01). Figure 4b and c (top panels) shows the amount P \ 0.003) compared to P1 and more hypothenar contri-
of change of arch angle in degrees. Since the hand in the bution during P3 (P \ 0.005), Fig. 5b. In the cylindrical
stroke subjects was several degrees flatter in the initial grasp there was more thenar contribution only during P3
position, hand shape in each phase in this group was 5°–7° (P \ 0.002), Fig. 5c, whereas the hypothenar contribution
more than the control group and was more evident in P2 was the same across all phases.
and P3, particularly for the cylindrical grasp.
Figure 5a illustrates the proportion of phase-wise thenar Total task time and phase completion times
and hypothenar arch modulation relative to the total arch
modulation. The stars indicate areas of significant differ- Participants with stroke took approximately 60% longer to
ences between groups. When considering thenar and complete the task for the spherical (control: 871 ± 280 ms,
hypothenar angles, smaller angles reflect greater arch stroke: 1,443 ± 455 ms) and cylindrical (control:
concavity and therefore increased contribution to the arch 929 ± 264 ms, stroke: 1,953 ± 740 ms) objects, respec-
formation. Thus, the shorter bars in the histogram shown in tively, compared to the control group. The relative time
Fig. 5, indicate that the thenar part of the hand contributed spent in each phase varied. Overall, there were significant
more to arch formation than the hypothenar part for both differences between groups (F1,1,2 = 47.84, P \ 0.001),
grasps in both groups (approximately 15°; spherical: between grasp types (F1,1,2 = 6.05, P \ 0.02), and a
F2,18 = 4.711, P \ 0.014; cylindrical: F2,18 = 5.153, phase-wise interaction for the cylindrical grasp
P \ 0.01; Fig. 5a). Phase-wise thenar and hypothenar (F218 = 3.811, P = 0.006). The time spent in completing

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Exp Brain Res (2009) 199:59–70 65

Fig. 4 a Phase-wise percent of Control Stroke


arch modulation; Phase-wise (A)100 p<0.002
interaction in arch modulation 90 p<0.002
(°; top panels) and percent of 80 p<0.01

Arch modulation (%)


arch modulation (bottom 70 p<0.001
panels) for b spherical grasp 60
type and c cylindrical grasp type 50 Contact shaping (P3)
40 Pre-shaping (P2)
30 Transport shaping (P1)
20
10
0
Spherical Cylindrical Spherical Cylindrical
grasp grasp grasp grasp

(B) Spherical grasp (C) Cylindrical grasp


Estimated marginal means (°)

16 16
Control
14 14
Patients
12 12

10 10

8 8

6 6

4 4
1 2 3 1 2 3
Estimated marginal means (%)

50
60

40 50

30 40

30
20
20

10 10
1 2 3 1 2 3
Phase Phase

each grasp phase in stroke subjects was longer compared to function on the Purdue Pegboard test) required relatively
the control subjects for all three phases, particularly for the less time to complete phases 2 and 3 of the spherical grasp
cylindrical grasp [spherical grasp: P1 (control: as compared to their performance on the cylindrical grasp.
302 ± 59 ms, stroke: 437 ± 138 ms, P \ 0.02) and P3 The total grasp time was negatively correlated with the
(control: 248 ± 88 ms, stroke: 520 ± 178 ms, P \ 0.004); Chedoke-McMaster scale scores (spherical r = -0.59;
cylindrical grasp: P1 (control: 284 ± 45 ms, stroke: cylindrical r = -0.90) indicating that stroke survivors
482 ± 117 ms, P \ 0.001), P2 (control: 364 ± 184 ms, with better hand function took less time to complete the
stroke: 767 ± 345 ms, P \ 0.006), and P3 (control: tasks. This was also true for each phase of the reaching
281 ± 73 ms, stroke: 704 ± 342 ms, P \ 0.002)], Fig. 6a. task, especially for the cylindrical object with correlations
When the two tasks were compared within groups, the ranging from -0.71 to -0.91 for Chedoke scores vs. times
control group took longer to complete P3 (P \ 0.04) in the spent in phases 1–3 and from -0.53 to -0.71 for Purdue
cylindrical grasp as compared to the spherical grasp. The Pegboard Scores) versus each phase.
stroke patients, however, took longer to complete the pre-
shaping (P2: control: 364 ± 184 ms, stroke: 767 ± Proximal interphalangeal (PIP)
345 ms, P \ 0.01) and the contact shaping phases (P3: and metacarpo-phalangeal (MCP) joint linearity
control: 281 ± 73 ms, stroke: 704 ± 342 ms, P \ 0.053),
see Fig. 6b, particularly for the cylindrical grasp type. To better characterize hand-related deficits due to stroke,
Patients who had relatively high hand function scores (C5 aside from palmar modulation, finger joint coordination
on Chedoke-McMaster Scale and close to normal hand was also investigated by examining phase-wise linearity

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66 Exp Brain Res (2009) 199:59–70

Fig. 5 a Phase-wise thenar and (A)


hypothenar contribution for Contact shaping (P3) Pre-shaping (P2) Transport shaping (P1)
each grasp type and respective
error bars. A smaller angle Control Stroke
200
indicates greater palmar
concavity and the stars indicate

Arch modulation (°)


phases in which the differences 150
between groups were significant
(P \ 0.01). Phase-wise
interaction in thenar (top panels) 100
and hypothenar (bottom panels)
contribution for b spherical and,
c cylindrical grasp type. In the 50
spherical grasp, there was more
thenar contribution to palmar
concavity formation during P2 0

thenar

hypothenar

thenar

hypothenar

thenar

hypothenar

thenar

hypothenar
and P3 and, more hypothenar
contribution during P3. In the
cylindrical grasp, there was
more thenar contribution only Spherical grasp Spherical grasp
Cylindrical grasp Cylindrical grasp
during P3, while hypothenar
contribution was the same (B) Spherical grasp (C) Cylindrical grasp
across all phases
Control
Estimated marginal means (°)

72 72
Patients
68 68
64 64
60 60
56 56
52 52
48 48
44 44
Thenar Thenar
40 40
1 2 3 1 2 3
Estimated marginal means (°)

72 72
68 68
64 64
60 60
56 56
52 52
48 48
44 44
40 Hypothenar 40 Hypothenar

1 2 3 1 2 3
Phase Phase

between MCP and PIP joints in the index and middle fin- The same pattern was not observed for the cylindrical grasp
gers. Although there were no overall phase-wise differ- (Fig. 7b). While there was still a tendency for the most
ences between groups in the correlation between the linearity to occur in P1 and the least linearly to occur in P2
linearity of PIP and MCP movement, there were distinct in the control group, there was only a significant difference
PIP–MCP interaction effects (F2,14 = 4.763, P \ 0.05) between groups in P2 for the middle finger.
between the two groups for each grasp type (Fig. 7a, b).
For the spherical grasp (Fig. 7a), the pattern of index and
middle PIP–MCP movement was more linear in P1 in the Discussion
control subjects compared to the patient group. In addition,
the linearity was greater in the patient group at P2 for the Most studies of reach-to-grasp movements have high-
index and in the control group at P3 for the middle finger. lighted differences in reaching and grasping movement

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Exp Brain Res (2009) 199:59–70 67

2500 descriptions, the relationship between these deficits and the


(A)
Cylindrical grasp decreased use of the post-stroke upper limb, even in well-
2000
recovered patients remains elusive (Lai et al. 2002; Mayo
Spherical grasp
1500 p<0.001
et al. 2002). This relationship may be more completely
Time (ms)

p<0.004 understood by including the description of the biome-


1000 p<0.006 chanical limitations in the ability of the hand to conform to
the object to be grasped. To better understand how post-
500 p<0.02 p<0.002
stroke hemiparesis impacts hand movement, we formulated
0 a measure to quantify palmar arch modulation and identi-
Control Stroke Control Stroke
2500
fied three phases characterizing prehensile movement. Our
(B) earlier studies validated these methods in healthy individ-
Stroke
2000 uals with no history of hand dysfunction (Sangole and
Control p<0.053 Levin 2007, 2008a, b). In this article, we extended the same
Time (ms)

1500
methods to characterize modulations in hand movement
1000 p<0.04
p<0.01
during functional reaching tasks in individuals following
stroke.
500 Our findings showed that both groups exhibited com-
parable performance in phase-wise absolute palmar arch
0
Spherical Cylindrical Spherical Cylindrical modulation for the spherical grasp. However, for cylin-
grasp grasp grasp grasp
drical grasping there were differences during the preshap-
Contact shaping (P3) Pre-shaping (P2) Transport shaping (P1)
ing (phase 2: establishing object contact) and contact
Fig. 6 The time (ms) to complete each phase of the reaching shaping phases (phase 3: making fine adjustments to the
movement and the total reaching time a for the same grasp type grip at object manipulation). These differences may be
between groups; b for the two grasp types within each group attributed to the fact that in a spherical grasp, there are
support reaction elements that stabilize the object as the
patterns between stroke survivors and healthy subjects with hand establishes contact with it. For example, the direction
a main focus on hand aperture and grip forces (for a recent of the hand movement while establishing contact with the
review, see Nowak 2008). Yet, despite detailed spherical object is normal to the supporting surface
Fig. 7 Group interaction in (A) (B)
phase-wise PIP–MCP linearity a
spherical grasp (left panels) and 1.0 1.0 Control
Estimated marginal means

b cylindrical grasp (right Patients


0.9 0.9
panels). The y-axis is the linear
regression coefficient value 0.8 0.8

0.7 0.7

0.6 0.6
p<0.05
0.5 0.5
E

0.4 Indexfinger 0.4 Indexfinger


1 2 3 1 2 3

1.0 1.0
Estimated marginal means

0.9 0.9
08
0.8 0.8
0.7 0.7
0.6 0.6
0.5 p<0.05
0.5
0.4 p<0.05 0.4
0.3 0 3 Middle finger
0.3
Middle finger

1 2 3 1 2 3
Phase Phase

123
68 Exp Brain Res (2009) 199:59–70

whereas this is not so for the cylindrical object. While The phase-wise PIP–MCP linearity pattern revealed an
grasping a spherical object does not necessitate object interaction between the groups (see Fig. 6). The interaction
stabilization, a cylindrical object may tip over if the hand is effect in the spherical grasp may be attributed to PIP–MCP
not aligned appropriately. Tipping of the object is often linearity during transport shaping and preshaping (phases 1
avoided by using the other hand for stabilization. In the and 2). The PIP–MCP linear relationship explains the rel-
current experimental protocol, however, subjects could not ative coordination between the two finger joints. If they are
avail themselves of assistance from the unaffected side. synchronous with each other, then both PIP and MCP joint
Furthermore, cylindrical grasping requires a re-orientation angles during a grasping phase are either extending or
of the hand at the wrist joint. These aspects impact the flexing together. If they are not synchronous then one fin-
hand–object dynamics, particularly when object interaction ger is extending while the other is flexing or vice versa.
occurs which requires grip adjustment for overall prehen- The interaction effect in Fig. 6a suggests that the stroke
sile stability during object manipulation (phases 2 and 3). survivors exhibit different, perhaps opposite, characteris-
The results thus suggest that although both grip types are tics of PIP–MCP phase-wise linearity during hand opening
power grasps, grasping a cylindrical object requires addi- and closing compared to the healthy individuals thus
tional hand re-orientation at the time of establishing object reflecting an altered finger-joint coordination pattern. This
contact and adjustment of the grip for overall prehensile would impact their ability to use the hand for fine manip-
stability during object manipulation. This explains why ulative tasks and provides a more detailed level of
upper limb assistive technology efforts in the design of description of the hand impairment. Further studies of more
doorknobs, utensils etc. minimize the need to re-orient the complex grasping tasks primarily focusing on finger joint
hand. Assistive technology is essentially designed to angular excursions are required to examine the PIP–MCP
maximize the use of gravity or body weight in order to coordination for other grasping tasks.
manipulate objects. For example, using a lever-shaped
doorknob (e.g., LeveronÒ handle door knob adaptors), door
opening can be done by leaning on the knob with the arm Conclusions
or hand instead of supinating the hand which is required to
turn a standard spherical doorknob. Previous studies of reaching and grasping in subjects with
In the healthy subjects, most of hand shape modulation post-stroke hemiparesis have focused on arm movement to
was accomplished during transport shaping (P1), with fine explain hand-related deficits by characterizing hand ori-
adjustments occurring during the P2 and P3 phases. Thus, entation relative to the arm and grip aperture scaling. What
hand shape modulation was accomplished early in the is not clear from studies of arm motor compensations
reach-to-grasp task. In contrast, the stroke patients started during reach to grasp tasks is whether the compensations
with a much flatter hand (greater palmar arch angle) and are related to deficits in arm trajectory formation per se or
thus required more arch modulation during the three pha- to deficits in the ability of the hand and fingers to conform
ses. They exhibited relatively more arch modulation during to the object and develop a stable grasp. This study is the
P2 and P3 as compared to the healthy subjects. This not first to demonstrate that deficits in palmar shape modula-
only reflects the temporal concurrency between the three tion occur concurrently with deficits in coordinated finger
phases (Sangole and Levin 2008b) but also suggests a movement. This new information about palmar shape
spatial concurrency. Phase-wise times differed in the stroke modulation may help to explain why even patients who are
subjects and were related to hand motor impairment and considered to be well-recovered on standard clinical testing
function scores (Chedoke-McMaster Hand Scale, Perdue still have deficits in performing activities of daily living
Pegboard). The only moderate correlation between the (Mayo et al. 2002).
times and the Chedoke-McMaster scores may be attributed Our findings provide additional insights into how stroke
to a ceiling effect of the scale for fine hand control. impacts hand configuration during the performance of
From a motor control standpoint, our findings show that functional hand tasks. Palmar arch modulation was most
modulation of hand shaping at the level of the palm occurs affected in latter segments of the prehensile movement, i.e.,
at the same time as changes in the finger aperture during phases 2 and 3, which involve hand–object contact and fine
reach-to-grasp tasks. This suggests that the nervous system grip adjustment. This indicates that discrete parameters
controls these actions together in an anticipatory way prior such as maximal grip aperture cannot characterize hand-
to object contact which is likely an important feature of related deficits because maximal grip aperture is already
successful grasping. Hand functional retraining in patients attained by the time of phase 2. Although both of the tasks
with post-stroke hand paresis may be more successful if studied (spherical and cylindrical grasps) are power grips,
focused on the coordination of these two elements of hand our findings showed that stroke survivors with mild hand
preshaping. impairment had more difficulty with the cylindrical grasp

123
Exp Brain Res (2009) 199:59–70 69

possibly because the stability of the grip is threatened Desmurget M, Prablanc C, Rossetti Y, Arzi M, Paulignan Y, Urquizar
during hand–object interaction. If the same task were to be C, Mignot JC (1995) Postural and synergic control for three-
dimensional movements of reaching and grasping. J Neurophys-
executed using a bimanual strategy, wherein the other hand iol 74:905–910
stabilizes the object during contact, we presume that the Desmurget M, Prablanc C, Arzi M, Rossetti Y, Paulignan Y,
performance would be comparable to the hand–object Urquizar C (1996) Integrated control of hand transport and
dynamics during a spherical grasp. orientation during prehension movements. Exp Brain Res
110:265–278
Interpretation of the findings is limited by the small Desmurget M, Grea H, Prablanc C (1998) Final posture of the upper
sample size and the fact that a majority of the patients had limb depends on the initial position of the hand during
relatively moderate hand function capabilities. Neverthe- prehension movements. Exp Brain Res 119(4):511–516
less, the findings reveal distinct differences of how hand Feldman AG, Goussev V, Sangole AP, Levin MF (2007) Threshold
position control and the principle of minimal interaction in motor
configuration is affected by stroke. Our findings suggest actions. Exp Brain Res 165:267–281
that combined with other measures of hand function such Fries W, Danek A, Scheidtmann K, Hamburger C (1993) Motor
as grip forces during object manipulation (e.g., Nowak recovery following capsular stroke. Brain 116:369–382
2008), hand shape modulation may form the basis of a Gentilucci M, Caselli L, Secchi C (2003) Finger control in the tripod
grasp. Exp Brain Res 149:351–360
standardized assessment of deficient manual dexterity for Gowland C, Stratford P, Ward M, Moreland J, Torresin W, Van
better diagnosis and rehabilitation of the hand post-stroke. Hullenaar S et al (1993) Measuring physical impairment and
In particular, rehabilitation interventions for patients with disability with the Chedoke-McMaster Stroke Assessment.
grasping deficits stressing anticipatory hand preshaping in Stroke 24(1):58–63
Jeannerod M (1984) The timing of natural prehension movements.
addition to wrist and finger joint movement may result in J Mot Behav 16:235–254
better outcomes. Jeannerod M (1999) Visuomotor channels: their integration in goal-
directed prehension. Hum Mov Science 18:201–218
Acknowledgments APS was supported by a Fonds de la Recherche Kamper DG, Cruz EG, Siegel MP (2003) Stereotypical fingertip
en Santé du Quebec (FRSQ) fellowship. The research was conducted trajectories during grasp. J Neurophysiol 90(6):3702–3710
at the Jewish Rehabilitation Hospital, during her postdoctoral term at Kapandji IA (1982) Physiology of the joints—upper extremities, vol
McGill University. The authors express sincere gratitude to the par- 1. Churchill Livingstone, New York
ticipants, to the students—Liza Azeff, Mi Yun, Olivier Vourantonis, Lai SM, Studenski S, Duncan PW, Perera S (2002) Persisting
and Luis Alberto Knaut who assisted on various aspects of data consequences of stroke measured by the Stroke Impact Scale.
recording as well as to Dr. Valeri Goussev for his assistance with data Stroke 33:1840–1844
analysis. MFL holds a Canada Research Chair in Motor Recovery and Landsmeer JMF (1962) Power grip and precision handling. Ann
Rehabilitation. Rheum Dis 21:164–170
Levangie PK, Norkin CC (2001) The wrist and hand complex. In:
Davis FA Joint structure and function, 3rd edn. Philadelphia,
pp 251–289
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