http://jneuroengrehab.biomedcentral.com/articles/10.1186/s12984-015-0039-z
- Belén Rubio BallesterEmail author,
- Jens Nirme,
- Esther Duarte,
- Ampar Cuxart,
- Susana Rodriguez,
- Paul Verschure and
- Armin Duff
Journal of NeuroEngineering and Rehabilitation201512:50
DOI: 10.1186/s12984-015-0039-z
© Rubio Ballester et al. 2015
Received: 5 February 2015
Accepted: 13 May 2015
Published: 9 June 2015
The Erratum to this article has been published in Journal of NeuroEngineering and Rehabilitation 2015 12:106
Abstract
Background
Stroke-induced impairments result from
both primary and secondary causes, i.e. damage to the brain and the
acquired non-use of the impaired limbs. Indeed, stroke patients often
under-utilize their paretic limb despite sufficient residual motor
function. We hypothesize that acquired non-use can be overcome by
reinforcement-based training strategies.
Methods
Hemiparetic stroke patients (n = 20, 11
males, 9 right-sided hemiparesis) were asked to reach targets appearing
in either the real world or in a virtual environment. Sessions were
divided into 3 phases: baseline, intervention and washout. During the
intervention the movement of the virtual representation of the patients’
paretic limb was amplified towards the target.
Results
We found that the probability of using
the paretic limb during washout was significantly higher in comparison
to baseline. Patients showed generalization of these results by
displaying a more substantial workspace in real world task. These gains
correlated with changes in effector selection patterns.
Conclusions
The amplification of the movement of the
paretic limb in a virtual environment promotes the use of the paretic
limb in stroke patients. Our findings indicate that reinforcement-based
therapies may be an effective approach for counteracting learned non-use
and may modulate motor performance in the real world.
Keywords
Stroke rehabilitation Hemiparesis Upper extremity Physical therapy Learned non-use Reinforcement-based motor therapyIntroduction
Following
stroke, a loss of neural tissue induces drastic neurophysiological
changes that often result in cognitive and motor impairments, such as
hemiparesis. In order to counteract these deficits patients often
introduce compensatory movements (e.g. overutilizing their non-paretic
limb). Although these compensatory strategies may immediately improve
functional motor performance in activities of daily living (ADLs) or
reduce the burden of using the paretic limb, a long period of non-use of
the affected limb can lead to further reversible loss of neural and
behavioral function [1].
This so-called learned non-use has been associated with a reduced
quality of life. Hence, methods must be found to reduce the impact of
acquired non-use.
A
possible treatment for learned non-use is Constraint Induced Movement
Therapy (CIMT), which forces the patient to use the paretic limb by
constraining the movement of the non-paretic limb. This technique has
been shown to be effective in mitigating the effects of learned non-use [2, 3, 4].
However, due to the high intensity and long duration of CIMT protocols,
which can range from 1 to 6 hours of training per session [5],
they may reduce quality of life, affect the patient’s adherence to
therapy, be prohibitively expensive and even inconvenient for those
patients with severe motor or cognitive deficits [6].
Moreover, it remains unclear whether the standard CIMT protocols are
more beneficial than bimanual functional rehabilitation [7].
The success rate of the standard CIMT protocols may depend on the
severity of upper limb paresis and latency of intervention post-stroke.
Consequently, its application remains restricted to subacute patients,
with no severe cognitive impairments, and mild hemiparesis. These very
stringent inclusion criteria only account for about 15 % of stroke cases
[8].
Hence, in light of these limitations it seems opportune to develop
rehabilitation techniques that build on the positive aspects of CIMT,
i.e. enhanced use of the paretic limb, while mitigating the negative
ones.
CIMT
builds on the emergence of compensatory movements post-stroke. Such
movements can be acquired and retained through the involvement of the
mirror neuron system (MNS) [9].
For instance, it has been proposed that a successful action outcome
might reinforce not only the intended action but also any movement that
drives the MNS during the course of its execution [10, 11, 12]. Action selection may depend on both the action’s executability and desirability [13].
In this case, the executability of an action is modulated by the MNS
and indicates the action’s expected biomechanical error, while the
desirability of an action is modulated by its outcome and can be
reinforced by accidental success. Desirability of action was
demonstrated in a recent study exploring handedness bias, suggesting
that performance asymmetries between limbs may influence the choices
that individuals make about which hand to use [14].
A recent study on hemiparetic stroke patients proposed that increasing
the patient’s confidence in using the paretic arm for a given level of
function may be critical for recovering non-pathological hand selection
patterns [15].
In this vein, Stoloff and colleagues showed that modulating reward
rates during a reaching task can increase the use of the non-dominant
hand in healthy subjects [16].
In order to ensure a high performance level the authors used a variable
ratio staircase procedure to adjust the size of a virtual target when
users selected their non-dominant limb to perform the action. The visual
representation of the target remained fixed. Note however, that this
reinforcement strategy exposes the user to an incomplete visuomotor
feedback of the reaching action when performed using the dominant limb.
This is because, due to the changing size of the virtual target, the
movements executed with the non-dominant limb were inferior in extent
and accuracy when compared to the dominant limb. We hypothesize that
exposing a user to the complete visual feedback of an intended action
may lead to reinforcement and thus will modulate hand selection
patterns.
The
approach we take towards stroke rehabilitation is based on the
Distributed Adaptive Control (DAC) theory of mind and brain, which
proposes that the disruption of the sensorimotor contingencies leads to a
reduction of activity in the motor cortical pathways and interconnected
sensorimotor areas. This reduction of activity leads to a reduced drive
in neural plasticity and thus to an impairment of recovery in case of a
lesion to the brain. Consequently, restoring these sensorimotor
contingencies through external manipulation of sensory and/or motor
modalities during the execution of goal-oriented actions might increase
the activation of the MNS and its interconnected motor areas, thus
driving plasticity and recovery [17].
On this basis, Virtual Reality (VR)-based protocols have proved
beneficial in the clinical context, since they can provide multimodal
feedback in safe and ecologically valid training environments. Indeed,
we have demonstrated this using the so called Rehabilitation Gaming
System (RGS) [18, 19] and provided direct evidence for the involvement of the MNS in these VR-based manipulations [20].
The
aim of this study is to explore to what extent goal-oriented movement
amplification in VR can induce beneficial changes in a patient’s hand
selection patterns, namely, effectively reinforcing the use of the
paretic limb, reversing learned non-use, and promoting motor recovery.
To realize this, we instructed stroke patients to perform a reaching
task in the first person VR RGS environment and a pointing task in the
real world. We included in the RGS protocol movement amplification of
the paretic limb. Results show that visual amplification of the movement
of the virtual counterpart of the paretic limb may induce improvements
in use of the affected arm and modulate performance in the real world.
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