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Motor compensation and its effects on neural reorganization after stroke

Key Points

  • The development of compensatory movement strategies is a reliable consequence of strokes that result in motor disabilities. Obvious forms of compensation for upper-limb disability after stroke include dominant reliance on the non-paretic upper limb and the use of trunk movements, in place of distal movements, to control the paretic upper limb.

  • Converging evidence from animal and clinical studies of stroke indicate that reliance on the obvious forms of compensation described above can limit the recovery of more-normal movements and more-functional use of the paretic upper limb. Their potential to do so can be expected to vary with impairment severity.

  • By contrast, the use of relatively subtle compensatory strategies to perform skilled motor tasks with the paretic upper limb can precede the recovery of more-normal movements on those tasks. The initial reliance on compensatory strategies that approximate normal movements may enable the task practice that is needed to support the recovery of those movements.

  • Both the effects of motor rehabilitative training focused on the paretic limb and the development of compensatory movement strategies depend on learning-related neural plasticity mechanisms that can be facilitated by their interaction with early post-stroke neuroregenerative responses. As compensation starts early after stroke, its neural plasticity mechanisms are probably normally facilitated by this interaction.

  • In rodent models of stroke, the neural plasticity involved in learning to compensate with the non-paretic upper limb can compete with the neural plasticity related to rehabilitative training of the paretic forelimb. This competitive plasticity is a putative mechanism by which compensatory strategies counter functional improvements in the paretic upper limb and exacerbate its disuse.

  • Compensation is not currently receiving the prominent attention in animal models of stroke that is warranted by its reliable clinical manifestation and its potential to either promote or impede recovery. A better understanding of the neural mechanisms, and adaptive and maladaptive consequences, of behavioural compensation has a strong potential to lead to new treatments that optimize functional outcome after stroke.

Abstract

Stroke instigates a dynamic process of repair and remodelling of remaining neural circuits, and this process is shaped by behavioural experiences. The onset of motor disability simultaneously creates a powerful incentive to develop new, compensatory ways of performing daily activities. Compensatory movement strategies that are developed in response to motor impairments can be a dominant force in shaping post-stroke neural remodelling responses and can have mixed effects on functional outcome. The possibility of selectively harnessing the effects of compensatory behaviour on neural reorganization is still an insufficiently explored route for optimizing functional outcome after stroke.

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Figure 1: The motor cortex and its descending projection pathways are often affected by strokes that result in upper-extremity impairments.
Figure 2: Illustrations of compensatory movement strategies for upper-limb hemiparesis.
Figure 3: Different trajectories of cortical reorganization depending on forelimb behavioural experiences after motor cortical infarcts in rodent models.

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Acknowledgements

The author is supported by NS056839 and NS078791. The author thanks the Bergeron Family Foundation (Vermont, USA) for enabling experiences at the Georgetown University (Washington DC, USA) and the US National Rehabilitation Hospital Center for Brain Plasticity and Recovery (Washington DC, USA) that informed the content of this Review, and S. K. Subramanian for helpful suggestions on figure 2a.

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Glossary

Callosotomy

The surgical procedure of severing the corpus callosum at the midline.

Non-paretic

Refers to the side of the body that is ipsilateral to the stroke.

Paretic

Showing weakness, ineptitude and partial loss of voluntary movement. Usually most severe on the side of the body that is contralateral to the stroke.

Rehabilitation

A treatment designed to improve functional capacities. It includes physical therapy for motor impairments.

Precision grip

Grasp between the tips of the thumb and a finger.

Motor skill learning

The practice-dependent refinement of novel movement sequences.

Action Research Arm Test

A test that measures the ability to perform various actions with the paretic upper limb, such as grasping differently sized objects and pouring water from a glass.

Homotopic

Describes an anatomical region corresponding to that of the other hemisphere or body side.

Movement representations

The territories in the motor cortex that control discrete movements, such as of the wrist or of a digit. They are usually defined on the basis of movements evoked by electrical stimulation and are also known as a 'motor map'.

Perforated synapses

Synapses with discontinuous postsynaptic densities that are on average larger and more potent in evoking postsynaptic depolarizations than are other synapses.

Multisynaptic boutons

(MSBs). Single boutons that form synapses with more than one postsynaptic dendritic surface.

Paired-pulse protocols

Tests for the facilitation or depression of a stimulation-evoked neural response due to a preceding stimulation.

Crossed collaterals

Branches of an axon that cross the midline to terminate in the hemisphere opposite to that of the originating axon.

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Jones, T. Motor compensation and its effects on neural reorganization after stroke. Nat Rev Neurosci 18, 267–280 (2017). https://doi.org/10.1038/nrn.2017.26

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