# Bimanual training in stroke: How do coupling and symmetry-breaking matter?

Rita Sleimen-Malkoun, Jean-Jacques Temprado, Laurent Thefenne, Eric Berton

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Rita Sleimen-Malkoun, Jean-Jacques Temprado, Laurent Thefenne, Eric Berton. Bimanual training in stroke: How do coupling and symmetry-breaking matter?. BMC Neurology, 2011, 11 (1), pp.11. hal-01450707

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# Bimanual training in stroke: How do coupling and symmetry-breaking matter?

Rita Sleimen-Malkoun¹, Jean-Jacques Temprado¹*, Laurent Thefenne², Eric Berton¹

**Abstract**

**Background:** The dramatic consequences of stroke on patient autonomy in daily living activities urged the need for new reliable therapeutic strategies. Recently, bimanual training has emerged as a promising tool to improve the functional recovery of upper-limbs in stroke patients. However, who could benefit from bimanual therapy and how it could be used as a part of a more complete rehabilitation protocol remain largely unknown. A possible reason explaining this situation is that coupling and symmetry-breaking mechanisms, two fundamental principles governing bimanual behaviour, have been largely under-explored in both research and rehabilitation in stroke.

**Discussion:** Bimanual coordination emerges as an active, task-specific assembling process where the limbs are constrained to act as a single unit by virtue of mutual coupling. Consequently, exploring, assessing, re-establishing and exploiting functional bimanual synergies following stroke, require moving beyond the classical characterization of performance of each limb in separate and isolated fashion, to study coupling signatures at both neural and behavioural levels. Grounded on the conceptual framework of the dynamic system approach to bimanual coordination, we debated on two main assumptions: 1) stroke-induced impairment of bimanual coordination might be anticipated/understood by comparing, in join protocols, changes in coupling strength and asymmetry of bimanual discrete movements observed in healthy people and those observed in stroke; 2) understanding/ predicting behavioural manifestations of decrease in bimanual coupling strength and/or increase in interlimb asymmetry might constitute an operational prerequisite to adapt therapy and better target training at the specific needs of each patient. We believe that these statements draw new directions for experimental and clinical studies and contribute in promoting bimanual training as an efficient and adequate tool to facilitate the paretic upper-limb recovery and to restore spontaneous bimanual synergies.

**Summary:** Since bimanual control deficits have scarcely been systematically investigated, the eventual benefits of bimanual coordination practice in stroke rehabilitation remains poorly understood. In the present paper we argued that a better understanding of coupling and symmetry-breaking mechanisms in both the undamaged and stroke-lesioned neuro-behavioral system should provide a better understanding of stroke-related alterations of bimanual synergies, and help clinicians to adapt therapy in order to maximize rehabilitation benefits.

**Background**

Stroke is a major cause of functional disabilities and decrease in quality of life of people living in industrialized countries [1,2]. For instance, it is well established that mono-hemispheric cerebral vascular accident (CVA) results, among other diseases, in important chronic limitations of upper-limb use and manual

dexterity [3,4] even after several months of rehabilitation [5,6]. In particular, it has been shown that CVA-induced spasticity [7,8] leads to significant slowing-down of unimanual movements, alteration of multijoint coordination [9], decrease in smoothness [10,11] and segmentation (multiple peak velocity) of reaching and grasping movements [12]. Moreover, diminished dexterity [13,14], decrease in muscular strength [15] and slowing [16] have also been observed in the (presumably intact) ipsi-lesional limb.

As most of our daily living activities require the use of both hands [17], disruptions of bimanual coordination

<footnote>* Correspondence: jean-jacques.temprado@univmed.fr
¹UMR 6233 Institut des Sciences du Mouvement E.J. Marey, CNRS & Université de la Méditerranée, 163 Avenue de Luminy, CP 910, 13288 Marseille, France
Full list of author information is available at the end of the article</footnote>
induced by CVA lesions constitute an additional han-
dicap for stroke patients. Thus, re-acquiring bimanual
coordination is essential for making progress toward
autonomy and should constitute a necessary objective
for neuro-rehabilitation of upper-limb extremities [18].
However, in spite of well-identified neuro-physiological
dependencies between limbs (e.g., [19,20]), for a long
time, clinicians considered bimanual coordination as a
simple addition of two uni-manual movements [21,22]
and treated stroke-related alterations of bimanual
synergies as the result of impaired capacities of the
paretic limb. Thus, as noticed by McCombe Waller
and Whitall [18], studies investigating CVA-induced
impairment of bimanual coordination aimed primarily
at analyzing movement kinematics and performance of
the paretic limb (e.g., motor scores, dexterity index,
qualitative functional tests) rather than between-limbs
coordination.

Recently, bimanual movement training (BMT) has
emerged as a complementary tool in neuro-rehabilitation
of the paretic upper-limb. BMT is a general term which
includes multiple bilateral training techniques all of
them requiring the simultaneous use of both upper-
limbs in rehabilitation (see [23] for a review). Advanced
justifications for BMT were grounded on the three main
arguments: 1) the existence neurally-mediatted depen-
dencies between limbs (see [19] for a review); 2) interhe-
mispheric interactions along with the occurrence of
bimanually triggered activation of similar neural distrib-
uted networks in both hemispheres [24-27]; and 3) evi-
dence of training-related plasticity of the brain (e.g.,
[28-30]). The primary aim of BMT strategies has been
to facilitate and enhance the recovery of the paretic
limb. An additional argument was that bimanual train-
ing is closer than unimanual practice to every day tasks,
which frequently requires coordinated use of both hands
[18]. Accordingly, BMT is expected to maximize func-
tional recovery through re-establishing both paretic limb
control and bimanual control. However, in spite of the
expected benefits, consistent findings regarding BMT's
functional efficacy are still lacking and contradictory
results have even been identified in the literature
[18,23,26]. Thus, who could benefit from BMT and how
it could be practically used in rehabilitation protocols
remain largely unknown.

McCombe Waller and Whitall [18] suggested that
more randomized controlled trials and neuro-physiologi-
cal studies are still necessary to firmly confirm the effi-
cacy of BMT for functional recovery of upper limb
extremities in stroke patients. They hypothesized that
inconsistent results observed in past studies on biman-
ual training could be attributed to the inadequate
matching of protocols with baseline characteristics of
the patients and the lack of functional assessment,

which includes bimanual coordination tasks. In line with
these statements, we suggest that the inadequate match-
ing of BMT protocols with severity level of CVA lesions
resulted mainly from: 1) the lack of evidence on how
the mono-hemispheric lesion might perturb neurally-
mediated dependencies between the limbs (which would
alter inter-limb coupling strength, direction and signa-
tures), 2) insufficient use of a variety of task constraints
to account for patients' differences in neurally-mediated
coupling between-limbs and symmetry breaking
mechanisms. Indeed, quite similar bilateral tasks were
used in all BMT protocols, independently of the specific
characteristics of patients (see [23] for a review).
Numerous studies carried out in the undamaged neuro-
musculo-skeletal system (NMSS) have however demon-
strated that bimanual synergies emerge by virtue of
mutual coupling as an active, task-specific assembling
process where the limbs are spontaneously or intention-
ally constrained to act as a single unit (e.g., [31,32]).
Accordingly, exploring, assessing, re-acquiring and
exploiting functional bimanual synergies following
stroke require, as prerequisite, a deeper understanding
of how the coalition of various constraints (i.e., neural,
muscular, spatial, temporal, attentional,...) may facilitate/
inhibit expressions of bimanual coupling at both neural
and behavioural levels, as a function of the severity of
CVA lesions. So, in order to adequately choose/adapt
the bimanual rehabilitation protocol, one must take into
account two fundamental variables: 1) the persistence
(or not) of bimanual coupling following CVA, 2) the
degree of the lesion-induced interlimb asymmetry. The
degree of alteration of inter-limb coupling would deter-
mine whether the patient-specific BMT strategy should
be directed toward mutual coupling rehabilitation (if
altered) or whether the ipsi-lesional limb could be used
as a "trainer" for the paretic one (via the persisting cou-
pling). On the other hand, the degree of inter-limb
asymmetry would determine how external constraints
(task, environment) should be adapted in order to bal-
ance internal ones (lesion-induced), which will facilitate
both the production of adaptive coordinated behaviour
and the expression of the "positive" entrainment of the
paretic limb by the "healthy" one.

In the present paper, we put the debate on the above
rationale. Inspired by the conceptual framework of the
dynamic system approach to bimanual coordination, we
argue that neuro-behavioural manifestations of stroke-
induced alterations of coupling and between-limb sym-
metry should be the cornerstone of both research and
rehabilitation interventions. Accordingly, we draw two
new directions for future experimental and clinical stu-
dies in the perspective of assessment and rehabilitation
of upper-limbs in stroke patients: 1) behavioural conse-
quences of CVA-induced impairment of bimanual
coordination could be (at least in part) fruitfully
explored by comparing, in join protocols, task-induced
changes in coupling strength and asymmetry of biman-
ual discrete movements observed in both healthy people
and stroke patients; 2) intervention protocols elaborated
for restoring spontaneous bimanual coordination pat-
terns that characterize the unimpaired NMSS (or aiming
to exploit them) should be based on individual adapta-
tion of task constraints in order to attenuate the stroke-
related effects of decrease in bimanual coupling strength
and/or increase in interlimb asymmetry.

Discussion

Coupling as a fundamental mechanism of bimanual
coordination

In the undamaged NMSS, the motion of the limbs can
be coordinated with seemingly unlimited temporal and
spatial relationships, in either discrete or cyclical move-
ments. Some of these patterns are spontaneously pro-
duced, while others require learning and intensive
practice to be performed skilfully. For instance, in rhyth-
mic movements, synchronized or alternated movements
of limb components have been indentified as sponta-
neous coordination patterns [33-35]. In addition, it has
been shown that spatial assimilation and synchroniza-
tion tendencies between the two limbs can be intention-
ally overcome to perform bimanual coordination tasks
with different (spatial and/or temporal) requirements
[36-39]. Thus, both spontaneous and intentional/learned
coordination patterns are the hallmark of the intact
NMSS. Conversely, disruption of spontaneous coordina-
tion patterns of the bimanual repertoire can be consid-
ered as a signature of stroke-induced impairments in
the NMSS.

During the last twenty years, theoretical foundations
for a basic understanding of coordination principles and
their neural basis have begun to emerge, thanks to the
convergent contributions of nonlinear dynamic systems
(e.g., [31,40]) and neural crosstalk (e.g., [30,41]) frame-
works. In particular, research on interlimb coordination
has shown that spontaneous coordination patterns
emerge as the result of neurally-mediated cross-talks
that occur at different levels of the central nervous sys-
tem (CNS) facing internal (proper to the system) and
external (environmental) constraints [31]. Mutual inter-
actions between limb motions are captured by the
abstract notion of coupling. Coupling may be thought as
an informational flow substantiated through various
substrates (neural, musculo-skeletal, spatial,... [42]), that
links limb components. As the result of coupling, kine-
matic features of each hand motion are found in the tra-
jectory of the other hand. For instance, when trying
simultaneously to tap the head with one hand while
rubbing the stomach with the other hand, each hand

movement is reciprocally attracted to the other so that
their trajectories become spatially and/or temporally
coupled. Neural processes that mediate interlimb inter-
actions can be accounted for by informational exchanges
at the different levels of the CNS, resulting in neural
crosstalk and finally, in kinematic coupling of limb tra-
jectories [19,41,43,44]. For instance, as a result of neural
crosstalk, activation of the muscles of one limb may
affect muscle activity in the contralateral limb and then
favour a specific and stable spatio-temporal relationship
between limb motions [35,45]. In addition, coupling
may be asymmetric, thereby leading to unequal influ-
ence of one limb to the other.

The most illustrative model system of this conceptual
framework has been the study of phase transitions in
bimanual, cyclical movement tasks [33-35]. In this
situation, two spontaneous patterns were identified, cor-
responding to 0° and 180° of relative phase and then
so-called "in-phase" and "anti-phase", respectively [35].
In the case of limb motion in the horizontal plane, the
in-phase pattern involves symmetric motion of the
hands in opposite directions, due to the simultaneous
activation of homologous muscles, whereas the anti-
phase pattern involves motion in the same direction,
with simultaneous activity of antagonist muscles. The
analysis of between limb coordination through the use
of relative phase variability revealed different stability of
the two patterns: The in-phase pattern proved to be
more stable than the anti-phase pattern. Moreover, an
unavoidable switch (transition) occurred from the latter
to the former (i.e. a phase transition) when oscillation
frequency increases beyond a given critical threshold.
This behavioural picture of bimanual coordination has
been called "spontaneous coordination dynamics"
[31,33]. It depends essentially upon neural cooperation
that expresses, at the behavioural level, the results of
two competing forces within the CNS that would other-
wise remain invisible. On the one hand, a tendency for
limb components to adopt a specific, persisting beha-
viour (as a result of their intrinsic neuro-mechanical
properties e.g. eigenfrequency), and on the other hand, a
tendency for each limb component to be attracted
toward the other (by virtue of coupling). Finally, when
moving together in a bimanual task, limbs are con-
strained to operate as a single functional synergy, which
is the observable outcome of a continuous struggle
between maintenance and attraction within the NMSS.

One can easily figure out that if one or the two com-
peting forces is/are modified as the result of internal
(e.g., CVA lesion, mechanical factors), environmental
(e.g., metronome) and/or task (e.g., movement fre-
quency) constraints, both the bimanual repertoire and
the transient capacity of assembling a task-specific rela-
tionship between limbs will be affected. Numerous
works have confirmed this prediction in the undamaged neuro-behavioural system. For instance, it has been suggested that increase in movement frequency decreased coupling strength, giving rise to loss of stability of the actual pattern and, finally, to a switch toward a more attractive phase relation (e.g., [33]). Conversely, atten- tional focus has been shown to increase coupling strength, thereby stabilizing the actual pattern and delaying the occurrence of phase transition from anti- phase to in-phase [46,47]. At the individual component level, a change in natural movement frequency resulting from a modification of neuro-mechanical properties of one of the oscillating segment has been shown to create a difference between the two components, which offset the attraction toward perfect synchronization between them (e.g., [31,48]). To our knowledge, this conceptual framework has never been applied to stroke-related impairments of bimanual coordination (but see [49] for an introduction).

Coupling mechanisms and limitations of the CNS in
mastering interlimb coordination were also revealed in
discrete bimanual tasks (e.g., [39,50,51]). In this context,
spontaneous tendencies to spatio-temporel synchroniza-
tion of both limbs reflect what are the most easily
potentiated pathways and neural cross-talk in the ner-
vous system. For instance, when trying to draw a line
and a circle simultaneously, one with each hand, ampli-
tudes and directions tend to be similar so that the line
is attracted toward the circle (it becomes elliptic) and,
conversely, the circle is compressed and tend toward a
line. This so-called spatial assimilation reflects, at a
behavioural level, the effects of underlying neural cou-
pling mechanisms. Similarly, drawing orthogonal lines
in front of the body is more difficult than drawing par-
allels, thereby revealing underlying neural interference
giving rise to directional coupling (see [30] for an
overview).

For clinicians, a major implication of these findings is
that the observed coordination patterns provide a win-
dow into underlying coupling mechanisms in the NMSS.
Accordingly, stroke-induced alterations in bimanual
coordination must be assessed through impairments of
the relationship between limbs rather than through
changes in the kinematics of individual limb components
[18]. Evidence exists of CVA-induced impairment of
bimanual control but knowledge about the alterations of
neural coupling and how it can be influenced by task
constraints in stoke patients remain limited.

Limited knowledge is available about stroke-induced
alterations of bimanual coupling

Cyclic bimanual movement tasks

Since Mudie & Matyas's seminal work [52,53], subsequent studies have explored inter-limb interactions in

stroke patients and the effectiveness of bilateral arm
training for rehabilitation of upper limb extremity (see
[18,54] for reviews). It has been shown that stroke
patients with severe lesions usually encounter great diffi-
culties to perform cyclic movements even at a relatively
low frequency [55]. Consequently, assessment of biman-
ual coordination dynamics is not practical with severely
impaired patients. Studies carried out with mild
impaired stroke patients showed that, as compared to
healthy adults, patients were less stable and less accurate
both in in-phase and in anti-phase coordination patterns
(e.g. [56-58]). In continuous temporally symmetric
movement Rice and Newell [58] showed that, in post-
stroke individuals, the non-paretic limb was constrained
to the slower paretic limb frequency and, consequently,
was unable to achieve its unimanual natural frequency.
Lewis and Byblow [56] examined interlimb temporal
and spatial coordination in a continuous circle-drawing
task in post-stroke hemiparetic individuals. Their results
showed that the paretic limb influenced the behaviour
of the non-paretic limb and no improvements in the
paretic one were elicited with the continuous bimanual
task. Ustinova et al. [59] investigated how the bilateral
coordination pattern was regained after external pertur-
bations of either the paretic and non-paretic limbs.
Results showed that the relaxation time toward the
initial anti-phase pattern was longer for stroke patients
than for control participants (2 cycles versus 1 cycle,
respectively). These findings suggested that coupling
strength was altered, though weakly, in mildly impaired
stroke patients.

Discrete bimanual movement tasks

Inconsistent results have been observed in the literature
with respect to CVA effects on coupling in bimanual
discrete coordination tasks. Some studies did not find
kinematic signatures of coupling in either the paretic or
non-paretic limb kinematics during bimanual move-
ments (e.g., [60]). On the other hand, other experiments
succeeded in demonstrating the persistence of sym-
metric coupling after CVA. In a group of moderately
impaired patients, Harris-Love et al. [61] observed sym-
metric coupling interference on movement time (MT),
peak velocity (PV), and peak acceleration (PA) of both
arm trajectories, as well as on symmetry ratios for each
variable (i.e. the value of the paretic arm divided by
non-paretic one). Messier et al. [62] reported a similar
pattern for elbow joint motion during simultaneous par-
allel bilateral movements. These results indicated the
persistence of a symmetric coupling as usually observed
in healthy participants. Finally, several studies showed
an increase in asymmetric coupling after CVA. For
instance, Dickstein et al. [63], investigating unilateral
and bilateral arm movements resulting from elbow-joint
mobilization, reported a prolonged movement time for
the non-paretic limb during bilateral elbow flexion compared to the unilateral condition. Temporal asymmetrical coupling, in which the paretic limb slowed the non-paretic one, has also been reported in other studies [55,56,61,62,64,65]. On the other hand, Cunningham et al. [66] showed some facilitation of the paretic limb that is a smoother elbow extension velocity profile during bimanual movements.

Thus, though a number of studies confirmed that bimanual movements are disrupted in stroke patients, the above reviewed literature showed inconsistent results with respect to the stroke-induced alterations of bimanual coupling. A possible explanation is that in the different studies, bilateral movement tasks were proposed quite independently of the severity of CVA lesion and, consequently, might have sometimes hidden behavioural expression of interlimb coupling. This hypothesis is grounded on the theoretical premise that bimanual coordination in stroke results from the struggle between two competing forces: mutual attraction between limbs (depending on the strength of neural coupling) and symmetry-breaking (resulting from difference in neuro-mechanical properties of the limbs), which are both affected by CVA lesion. However, the balance of these two competing forces can also be modulated by task constraints.

## Bimanual coordination in stroke as an expression of the balance between coupling strength and symmetry-breaking between limbs

An attractive hypothesis concerning bimanual coordination stroke patients is that CVA lesion modifies both the coupling scheme within the neuro-behavioral system and the neuro-mechanical characteristics of individual limb components (i.e., the paretic and non paretic limbs). Evidence exists in the literature on the undamaged NMSS, that the balance between coupling strength and differences in neuro-mechanical limb properties determines interlimb (de)synchronization in discrete bimanual coordination tasks. The resulting symmetry-breaking refers to the offset of spatial and temporal synchronization of hand motions, A main source of symmetry-breaking in bimanual coordination tasks has been reported first by Kelso, Delcolle and Schöner ([67]; but see also [68]). It lies in intrinsic differences between limb properties, such as the difference in movement times or natural frequency of each limbs, and may lead to a variety of coordinative phenomena: From moderate shifts in relative timing between limbs, which perturbs the bimanual coordination and manifests either by a (more or less large) shift in between-limbs relationship or even by "relative coordination" in which limb movements are no longer (or only transiently) attracted to a stable coordination pattern.

Schöner [51] proposed a model to capture the synchronization/de-synchronization tendencies observed in discrete bimanual coordination in the undamaged neuro-behavioral system (see [49] for details). In this framework, relative timing between limbs expresses the underlying coordinative activity of the CNS. Accordingly, one predicts that depending on the magnitude of neuro-mechanical differences between limbs, bimanual coordination may (or not) be dominated by symmetry-breaking and coupling may (or not) be strong enough to lead to synchronization tendency. Thus, depending on the importance of decrease in coupling strength relative to the magnitude of difference between neuro-mechanical limb properties, patterns characterized by sequential initiation of discrete movements (i.e. initiation time, IT) and/or differences in movement time (MT) will be observed. This prediction accounted for experimental (and supposedly clinical) conditions in which the two limbs differed individually in their amplitude and/or movement duration [39,50,69,70]. An elegant illustration can be found in Kelso et al.'s study [39,50], where the authors manipulated task difficulty in unimanual and bimanual aiming tasks by varying both width and distance of the target. In unimanual conditions, as predicted by Fitts's law [71,72], MT increased with the index of difficulty (ID). In the bimanual conditions, task difficulty was manipulated either symmetrically (i.e. same ID for both hands) or asymmetrically (i.e. a different ID for each hand). Results showed that, when confronted to dissimilar movement task constraints, the fast hand slowed down to move synchronously with the slower hand, which was weakly affected by the faster one. These results suggest that there is a strong tendency for limbs to be synchronized even under conditions of disparate difficulty. However, Marteniuk et al. [69] and Corcos [70] also showed a tendency to a breakdown of synchronization when the intrinsic movement times (reflecting task demands) become too dissimilar, which means that coupling was not strong enough to maintain a synchronized bimanual synergy. Riek et al. [73] observed that increasing asymmetry between limbs also increased sequential initiation of movements: The hand performing the longer amplitude started before the hand performing the shorter amplitude but the two hands arrived on the target simultaneously.

This theoretical framework provides new insight to assess stroke-induced alterations of bimanual coordination and might help to define principles of therapeutic interventions dedicated to functional recovery of coordinated behaviour. These hypotheses rest however on the assumption that: 1) the NMSS becomes internally constrained in an asymmetrical manner by CVA lesions at both the level of coupling and individual components (e.g., spasticity), and that 2) a parallel can be drawn
between symmetry breaking of bimanual coordination in healthy people and stroke-related alterations of coupling strength and limb properties. In the following section, we discuss how the study of the interplay between coupling and symmetry-breaking mechanisms could help researchers and clinicians to better understand bimanual coordination impairments in stroke patients and correspondingly better individually adapt their interventions in respect to the patient characteristics.

## Join protocols to study symmetry-breaking of bimanual coordination in the undamaged and in CVA-lesioned neuro-behavioral systems

Our main assumption is that, in a bilateral coordination task, shifts in relative timing between limbs express the results of counteracting effects of attraction and symmetry-breaking factors. These factors may originate in stroke-induced weakness of neural coupling between limbs and/or in difference in neuro-muscular stiffness between the paretic and non-paretic limbs (e.g., spasticity), respectively. Their effects on bimanual coordination can be experimentally investigated in both healthy and stroke patients. In this aim, a possible experimental strategy consists of the comparison of the observed behaviours of both populations in similar experimental paradigms and tasks conditions, though adapted to baseline characteristics of stroke patients. Kelso et al.'s experimental paradigm [39] might be a valuable a model system in this respect.

By using bimanual Fitts's task paradigm, temporal asymmetry between limbs can progressively scaled by changing either biomechanical (loading, muscular co-contraction) or tasks/informational constraints (e.g., Fitts's ID) applied to each limbs. Neural coupling can also be modulated by changing attentional focus directed to the task [47] or to a limb [74], or even by removing vision. According to loss of coupling and symmetry-breaking predictions, when increasing asymmetry between limbs, one should observe a progressive de-synchronization of IT and/or MT and finally, when temporal asymmetry between limbs goes beyond a critical threshold, an abrupt transition from synchronized movements to a desynchronized pattern. In the undamaged neuro-behavioral system, transitions should be preceded by an increase in variability of the difference in movement times between limbs. One also predict that, for a given magnitude of temporal asymmetry between limbs, if coupling strength is increased, one should observe: (a) a better synchronization for larger interlimb temporal asymmetries, and (b) a higher stability of synchronized patterns and less transition for higher magnitude of temporal asymmetry between limbs. These predictions are in large part deduced from disparate experimental facts (e.g., [39,50,69,73,75]), but to our knowledge they have never been tested systematically.

In doing so, one could establish a reference frame for further analyzing bimanual asymmetries resulting from CVA lesions. Indeed, an important question is whether and in what conditions comparable behaviours will be observed in stroke patients and healthy people with respect to the effects of asymmetry between limbs, be it caused by mechanical, informational or attentional factors.

Following the same logic in stroke patients, bimanual asymmetry could be attenuated by manipulating movement time of the non-paretic arm, while keeping constant the difficulty of the task for the paretic arm. By doing so, one makes bilateral movements more symmetric, thereby increasing the effect of neural coupling and improving synchronization. Participants could also be instructed to focus their attention on the bimanual task or to the paretic limb to increase bimanual coupling and then to facilitate synchronization. Thus, one could determine whether (more or less severely impaired) stroke patients perform more synchronized bimanual patterns when asymmetry between limbs is attenuated by specific manipulations of constraints on either the non-paretic (e.g. progressive loading, manipulation of ID) or the paretic arm (focus of attention, reduction of spasticity). Moreover, it can be anticipated that transient loss of coordination between limbs, characterized by a complete independence of each limb at a given level of dissimilarity between limbs (i.e., relative coordination), could be more frequently observed in stroke patients. In this respect, the effects of reducing spasticity of the paretic limb on bimanual coordination will also be of particular interest to distinguish the respective effects of neuromuscular factors and neural coupling on the occurrence of relative coordination. For instance, a crucial question is whether entrainment and synchronization can be gained or whether de-synchronization can be delayed after reducing limb spasticity. Finally, one can hypothesize that, on the basis of this experimental paradigm, it could be possible to determine whether behavioural expressions of asymmetries and relative coordination caused by CVA lesions depend on the location in the dominant/non dominant hemisphere of the lesion, the age of the patient, the constraints of the task, etc.... To our knowledge, these predictions have never been empirically tested for discrete movement tasks in both healthy and stroke participants.

In addition to research studies, further application of the above "loss of coupling" and "symmetry-breaking" hypotheses to stroke rehabilitation could also be envisaged by introducing a patient-specific constraint-adapted BMT.

## Implications of coupling and symmetry-breaking for BMT in stroke

Following the same aforementioned reasoning, in order to facilitate the expression of neuro-behavioral coupling
and make use of it in rehabilitation, it is necessary to
adapt bimanual protocols to patient baseline characteris-
tics. It can be done, in particular, by modulating task-
constraints to be applied to non-paretic limb during
bimanual rehabilitation. This recommendation is
grounded on the above-mentioned coordination princi-
ples established in the undamaged NMSS. It could be
however further explored in clinical studies on BMT.

As a preliminary consideration, it is necessary to clar-
ify what the notion of coupling means in the context of
bimanual rehabilitation. Commonly, since bilateral train-
ing is often used as a tool to help recover the paretic
limb control, the bimanual coupling is considered as
functional only when it permits to create a “positive”
entrainment effect that is, when temporal and/or spatial
features of the non-paretic arm trajectory interfere with
the paretic arm trajectory. In other words, a main
expectation in BMT is that the non-paretic limb would
“entrain” the impaired one thereby improving its perfor-
mance. As a result, in two-handed conditions, the pare-
tic limb movement is expected to be faster, more
accurate, and smoother then in one-handed ones. Not
surprisingly, such prediction has rarely been verified in
the experimental studies. From the theoretical point of
view, coupling exists as long as there are spatial and
temporal interferences between the limbs no matter the
direction (i.e. from the paretic to the non-paretic and/or
from the non-paretic to the paretic). Actually, even an
asymmetric influence of the paretic limb toward the
non-paretic indicates the persistence of bimanual cou-
pling. Furthermore, results observed in both healthy
(e.g. [70,75]) and stroke participants [55,56,61,62,64,65]
rather suggest that a predominant asymmetric coupling
effect, from the slower (i.e. paretic) to the faster (i.e.
non paretic) limb, should be expected. Therapeutic
interventions should then wisely choose the appropriate
settings of bimanual training tasks in order to counter-
balance the neuro-mechanical asymmetries between
limbs thereby facilitate the expression of a more mutual
inter-limb entrainment and to optimize the recovery of
bimanual coordination by increasing coupling strength.

Presumably, both “abstract” training tasks (i.e.
BATRAC®, [24]) and functional daily-living-inspired
tasks could be successfully used in BMT protocols as
long as the coupling and symmetry-breaking principles
are correctly taken into account. The cornerstone for
therapeutic interventions lies in the identification,
appropriate setting and adequate manipulation of differ-
ent external constraints (environmental and task-
related). This could be made, for instance, by: (a) adapt-
ing mean movement time, (b) reducing effective asym-
metry between limbs (e.g. by loading the arm, reducing
spasticity,...), (c) balancing asymmetry through manipu-
lating accuracy constraints, (d) changing attentional

conditions either by instructing participants to allocate
more attention to the paretic arm or by re-organizing
the starting point and targets locations (see [73,76]).
One can speculate that these modulations of external
constraints will improve plastic changes at the different
levels of the CNS. Therapists may expect to obtain both
short-term and delayed effects on coordinated behaviour
by conjugating: (a) scaling of control parameters of the
coordination pattern (e.g. movement speed, physical
support,...), (b) augmented behavioural information (e.g.
instruction on movement goal, auditory or visual feed-
back, guiding metronome...) and (c) practicing single or
multiple coordination task across multiple training ses-
sions. Short-term effects would result from transient,
intentional forcing of bimanual synergy to adapt to task
constraints, while long-term effects would result from
stabilized CNS adaptations (brain plasticity) incurred by
repetitive practice in specific conditions.

To sum up, the important message for clinicians is
that, for a given coordination pattern, inappropriate
scaling of task constraints may preclude or, conversely,
facilitate the production of an adaptive coordinated
behaviour. In this respect, the attention of therapists
should be drawn on several important points: (a) asses-
sing the persistence of the basic repertoire of bimanual
movements may be considered as a preliminary step
indicating specific dysfunctions in the neuro-behavioral
system; (b) gains in bimanual coordination do not auto-
matically arise from progress of unimanual movements,
instead, they must be trained as specific synergies, not
as the sum of two single limbs; (c) restoring the default
mode of coupling may be indicative of an ongoing re-
learning process, which is of potential benefit for stroke
patients; and (d) bilateral training is beneficial for the
paretic limb only when bimanual coupling is unimpaired
and inter-limb asymmetry is small (surmountable or
partially compensated).

Summary

Even after a long rehabilitation period, stroke patients
continue to suffer from long-term impairments in their
daily living activities. If properly conducted BMT could
be an efficient approach to significantly reduce such
handicap and accelerate the recovery of the upper-limbs
function. In spite that bilateral therapy was classically
used as an additional approach to restore the paretic
limb control it should above all be looked at as predilec-
tion strategy to train bimanual behaviour. Since biman-
ual control deficits have scarcely been systematically
investigated in the context of stroke, many uncertainties
remain on the adequate prescription and the true value
of BMT. Clearly, researchers and clinicians should pay a
lot more interest to bimanual coordination assessment
and rehabilitation. In the quest for evidence and
guidelines concerning the appropriate use and settings
of BMT protocols, “coupling” and “symmetry-breaking”
are very promising concepts to guide researchers (ran-
domized controlled research studies) and therapists
(individualized rehabilitation protocols). New directions
for research and intervention are put into debate in the
present paper. However, only the results of future
research and clinical studies will determine the evi-
dence-based recommendation for therapy. Finally, one
can argue that BMT might be a promising tool for
neuro-rehabilitation, under the reserve that both
researchers and clinicians develop specific approaches to
assess, restore and exploit bimanual coupling and sym-
metry breaking phenomena.

Author details

¹UMR 6233 Institut des Sciences du Mouvement E.J. Marey, CNRS & Université de la Méditerranée, 163 Avenue de Luminy, CP 910, 13288 Marseille, France. ²HIA Laveran, Service de Réhabilitation Fonctionnelle, 13 Boulevard Laveran, 13013 Marseille, France.

Authors’ contributions

RSM elaborated the general structure of the manuscript and drafted it. JJT and LT critically revised the draft. EB supervises the research program. All authors have read and approved the final version of the manuscript.

Authors’ information

RSM: She is physiotherapists and PhD student in the Institute of Movement Science in Marseille. She has a long experience of classical upper-limb rehabilitation strategies. Her PhD research program aims at exploring CVA-induced alterations of coupling processes and neuro-mechanical properties of paretic and non-paretic limbs by comparing healthy people and stroke patients in both assessment and rehabilitation protocols.

JJT: He is full professor at the Institute of Movement Science at the University of the Mediterranean. He is a well-recognized specialist of the dynamical systems approach to bimanual coordination. During the last 10 years, he has published a number a paper exploring the role of the coalition of various constraints (muscular, directional, attentional...) on bimanual coordination dynamics in the undamaged neuro-musculo-skeletal system. In particular, he published reference papers on attention and bimanual coordination in the framework of the theory of dynamical systems (Monno et al., 2000, Temprado et al., 1999; for a review Monno et al., 2002).

LT: He is medical doctor in physical medicine and rehabilitation. He is head of the department of functional rehabilitation in Laveran hospital. He supervises the rehabilitation protocol elaborated and tested by the authors in a currently on-going research program on bimanual rehabilitation, coupling and symmetry breaking.

LT: He is medical doctor in physical medicine and rehabilitation. He is head of the department of functional rehabilitation in Laveran hospital. He supervises the rehabilitation protocol elaborated and tested by the authors in a currently on-going research program on bimanual rehabilitation, coupling and symmetry breaking.

EB: He is a specialist of movement biomechanics. He is the head director of the Institute of Movement Sciences where the research program is undertaken.

Competing interests

The authors declare that they have no competing interests.

Received: 11 November 2010 Accepted: 25 January 2011

Published: 25 January 2011

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Pre-publication history

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http://www.biomedcentral.com/1471-2377/11/11/prepub

doi:10.1186/1471-2377-11-11

Cite this article as: Sleimen-Malkoun et al.: Bimanual training in stroke: How do coupling and symmetry-breaking matter? *BMC Neurology* 2011 **11**:11.