Motor compensation and its effects on neural reorganization
after stroke
Theresa A. Jones
Department of Psychology and Institute for Neuroscience, University of Texas at Austin, Texas
78712, USA.
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.
Behavioural compensation refers to alternative behavioural strategies that circumvent
impairments to enable the performance of tasks and the attainment of goals. The
development of compensatory strategies after CNS damage is observed across diverse
impairment modalities. For example, patients who have undergone callosotomy (and who
are referred to as ‘split-brain’ individuals) develop peripheral self-cuing strategies to
compensate for impaired interhemispheric communication
1
. People with partial visual field
loss use compensatory head and eye movements to help to fill in the field
2
. Those with
agrammatic aphasia compensate for impaired syntax comprehension by relying on semantics
to understand speech
3
.
The compensatory strategies for stroke-induced motor disability are a prevalent category
owing to the overwhelming prevalence of stroke. As of 2013, there were more than 25
million stroke survivors worldwide
4
, and this population is predicted to reach 70 million by
2030 (REF. 5). Up to 85% of stroke survivors have hemiparesis that affects the upper
extremity (hand and arm) of one side
6
. Humans use both hands together most of the time
7
,
and the loss of the function of either hand requires major adjustments to our interactions
with the physical world. A common response to this loss after stroke is to learn
compensatory ways of relying on the better-functioning, non-paretic hand
8,9
. There are also
compensatory changes in the coordination of movements of both hands and of the paretic
forearm with the trunk, as explained below.
tj@austin.utexas.edu.
Competing interests statement
The author declares no competing interests.
HHS Public Access
Author manuscript
Nat Rev Neurosci
. Author manuscript; available in PMC 2018 December 11.
Published in final edited form as:
Nat Rev Neurosci
. 2017 May ; 18(5): 267–280. doi:10.1038/nrn.2017.26.
Author Manuscript Author Manuscript Author Manuscript Author Manuscript
Compensation is often mistaken for recovery (BOX 1). One goal of this Review is to
highlight the importance of distinguishing between the two in research on the neural
mechanisms of recovery. Motor recovery is defined as the return of more-normal movement,
or reductions in movement impairment. Some forms of compensation are obvious, but others
are subtle enough to go undetected in the absence of sensitive behavioural measures, making
them easily confused with recovery
10
. If not for the clever assays developed by Gazzaniga
and colleagues
1
, the use of self-cuing strategies in patients who have undergone callosotomy
would be easy to miss and could be interpreted as support for the idea that these patients
recovered interhemispheric communication without a key anatomical pathway for it. The
failure to recognize compensatory strategies has a strong potential to confuse our
understanding of the neural mechanisms of functional improvement after brain injury and to
hamper the usefulness of basic neuroscience research for guiding treatment.
Another reason to attend to compensation is that it is both a mechanism for improved
function and a contributor to persisting impairment after CNS injury
8,10,11
. There is
currently much interest in the potential to optimize functional outcome after CNS damage by
capitalizing on early endogenous mechanisms of neural repair and remodelling after stroke,
which are sensitive to behavioural manipulation and could facilitate the efficacy of motor
rehabilitation
12–15
. Behavioural compensation is often a major contributor to the functional
improvements that result from motor rehabilitative training
16,17
. Compensatory behaviours
are also self-taught. As they are developed early and are well practised
7
, these selftaught
behaviours may normally be a dominant force in shaping post-stroke brain reorganization;
however, they may do so in suboptimal, or even maladaptive, ways.
From the perspective of a researcher of rodent models of chronic stroke, this Review first
attempts to jointly summarize findings from human and animal studies on the nature of
motor compensation after strokes that impair upper-limb function. I describe findings from
animal models on the influence of motor compensation on neural reorganization after stroke
and its maladaptive consequences, and briefly consider the potential impact of motor
compensation on the role of the contralesional hemisphere in functional outcome.
Compensatory movement strategies
Stroke damage and its effects on movement.
The high prevalence of motor impairments after stroke may be due to the propensity for
strokes to damage motor regions of cortex, the subcortical projection pathways of these
regions or both
18,19
, thus disrupting the cortical control of movement (FIG. 1). Post-stroke
motor impairments are characterized by weakness, diminished muscle activation, abnormal
muscle co-activation and other abnormalities that diminish movement capacity and disrupt
the spatiotemporal coordination of movements
20–23
. There is often abnormal coupling of
shoulder and elbow movements (muscle synergies) — for example, the elbow may bend as
the arm is lifted
20,21,24
. Reduced wrist stability, diminished finger and grasp control, and
impaired grasp release all impair hand dexterity
25–27
. Movements are slower and more
variable
27,28
, reach trajectories are less direct
29
, and more-extraneous movements occur
30
in
stroke survivors than in healthy controls. Although the movements of both the left and the
right hands are typically impaired after unilateral stroke, the non-paretic side is less severely
Jones
Page 2
Nat Rev Neurosci
. Author manuscript; available in PMC 2018 December 11.
Author Manuscript Author Manuscript Author Manuscript Author Manuscript
so
31–34
. Spasticity due to hyperexcitability of the stretch reflex can develop after stroke
35
,
and its severity is correlated with the severity of motor impairments
36
. Motor impairments
co-occur to varying degrees with impaired somatosensation
37,38
, which is associated with
damage to ascending somatosensory pathways
39
.
Movement adaptations after stroke.
There are normally many different ways (or degrees of freedom) in which individual joint
movements can be combined to perform a task, and this diversity allows for adaptation to
changing environmental conditions and movement constraints. Motor impairments after
stroke can demand adaptation for a greatly diminished repertoire of movement
combinations
20,40,41
. Some of the compensatory movements that have been observed in
stroke survivors or in animal models of stroke are described in TABLE 1. To perform
reaching or pointing tasks with the paretic upper limb in laboratory settings, stroke survivors
compensate for limited arm extension and stability using movements of the trunk and
scapula
42–45
(FIG. 2). The aim and orientation of the hand tend to be controlled more
proximally by trunk and scapular movements, with elbow and hand positions fixed
46,47
, a
strategy that may reduce the complexity of movement control and increase stability
42,48,49
.
To grasp an object, stroke survivors use an excess of forward movements when reaching
towards it
50
and use the resistance of the object to wind their fingers around it
25
, presumably
to compensate for impairments in opening the fingers to grasp. Those with milder
impairments reach for differently sized objects using greater-than-normal adjustment at
proximal, in place of distal, finger joints and make these adjustments later in the reach than
normal, possibly reflecting a greater reliance on visual feedback to compensate for impaired
feedforward control
51
. Those with milder impairments open the hand excessively to grasp
objects and hold them with excessive grip force
31,52,53
, which may help to ensure a
successful grasp and hold in the presence of diminished hand control
53
.
In the laboratory, stroke survivors who are not told which hand to use will typically perform
unimanual tasks with the non-paretic hand
54,55
. Outside of the laboratory, increased reliance
on the non-paretic hand is a dominant strategy
9
. Based on data recorded with movement
monitors worn on the wrists, healthy controls perform most daily activities using both
hands
7,56
. After strokes affecting the dominant body side, bilateral hand use is diminished,
and sole use of the formerly non-dominant hand is increased in these patients relative to
healthy controls
7,56
. After strokes affecting the non-dominant side, use of only the dominant
hand predominates
7,56,57
. The non-paretic side is also used to help to move the paretic leg
during walking, via amplified swinging movements with the non-paretic arm and leg
48
.
Compensatory movement strategies are likely to be mediated by CNS regions that are less
severely affected by the injury. Relying on the better-functioning hand puts the relatively
intact circuitry of the contralesional hemisphere mostly in charge of task completion. In
healthy individuals, there is more bilateral control of trunk, relative to limb, movements
58,59
,
and trunk movements are also used to reach for objects outside of arm’s reach
60
; thus, trunk
movements may offer a ready solution for impaired arm extension after stroke.
Jones
Page 3
Nat Rev Neurosci
. Author manuscript; available in PMC 2018 December 11.
Author Manuscript Author Manuscript Author Manuscript Author Manuscript
Movement adaptations in animal models.
There are remarkable homologies in the movement patterns used by rodents and humans to
perform reach-to-grasp tasks
61,62
. There is also resemblance in the impairments and
compensatory movement patterns that result from unilateral motor system damage
63–66
(FIG. 2d–f). Slower, more-variable and more-extraneous movements are observed in the
paretic forelimb of rodents after motor system damage than in intact animals
65,67,68
. To
reach for food rewards with the paretic forelimb, rodents use compensatory rotational
movements of the trunk to extend and control paw position, and use compensatory trunk and
head movements to bring the mouth to the paw
16,63,69
. If not constrained, the non-paretic
limb is often used to assist paretic limb movements — for example, to support the paretic
forelimb during its extension (FIG. 2f) or to help to open its digits so that food can be
released into the mouth13,16. In addition, rats rely more on the non-paretic forelimb for
activities such as food handling
70,71
and postural support during exploration
72
.
Impairments in fine manual dexterity have been characterized in monkeys after focal motor
system damage
73,74
— for example, in tasks in which food rewards are most efficiently
retrieved using a precision grip. After ischaemic lesions of the digit region of the primary
motor cortex (M1)
75,76
or of the posterior limb of internal capsule
77
, macaques compensate
for impairments in precision grip by scooping food rewards with one or more digits towards
the palm or proximal thumb. However, these movement strategies can change with task
practice, as described below.
Learning to compensate
Compensation is likely to begin whenever a stroke survivor first attempts to perform an
activity with the paretic body side in the normal way that they did before the stroke, at which
point it becomes evident that the normal way no longer works. That is, compensation can be
expected to begin with the resumption of movement very early after stroke, but the process
of becoming adept in the new ways of moving involves motor skill learning, which is
practice dependent
78
. A right-hander can manage to eat and dress using only the left hand,
but the speed and efficiency in doing so is likely to improve over time with practice. Even
long after stroke, new compensatory movement patterns can be developed in response to
motor training
10
.
Learned non-use.
The counterpart of the compensatory strategy of relying mostly on the non-paretic hand is
disuse of the paretic upper limb. This disuse has been proposed to result from ‘learned non-
use’, whereby repeated experience with the weakness and ineptitude of stroke-impaired
functions encourages their disuse
8
. This idea was originally based on observations in
macaque monkeys with peripheral sensory deafferentation of one arm, which the monkeys
continued to disuse even after its capacity to move returned
79
. Findings in rats suggest that
paretic limb disuse develops with repeated experiences in attempting to use it. Most rats
have a strong preference for performing unimanual skilled reaching tasks with one limb. If
this limb becomes paretic owing to large motor cortical or mixed cortical–subcortical
lesions, rats continue to attempt to retrieve food rewards with it at first
80
. However, after
Jones
Page 4
Nat Rev Neurosci
. Author manuscript; available in PMC 2018 December 11.
Author Manuscript Author Manuscript Author Manuscript Author Manuscript
repeated failures, they start attempting to retrieve rewards with the other limb. With
continued practice, most rats with substantial injuries completely switch ‘handedness’ for
reaching
80,81
. Even rats that are not allowed to switch limbs (FIG. 2) transiently reduce their
attempts to retrieve food rewards with the paretic limb after initial attempts are
unsuccessful
82
.
In people who have survived stroke, the reliance on the trunk and scapula to control the
position of the paretic hand can also encourage the disuse of more-distal movements of the
paretic upper limb. Stroke survivors with moderate impairments who practise a reaching task
with the paretic upper limb while the trunk is restrained regain more-normal elbow
movement during arm extension, whereas those who do so without trunk restraint increase
their reliance on compensatory trunk movements instead
83
.
Training-induced compensation.
The compensatory movement patterns that develop after stroke can be self-taught or
encouraged by interventions. Stroke rehabilitation is focused on improving functional
abilities, and this improvement can be achieved through either the development of new
compensatory strategies or the recovery of more-normal function. The relative contribution
of the two varies with impairment level, with compensation making a larger contribution in
those with more severe impairment
42,84
, and with different rehabilitation approaches — for
example, depending on the extent of guided movement and the restriction of compensatory
strategies
83,85,86
. However, most motor rehabilitation approaches are focused on successful
task completion, which is permissive of compensation. In fact, some interventions encourage
reliance on the non-paretic hand to perform basic daily tasks, such as dressing
87,88
.
Rehabilitation efficacy can depend on compensation even when use of the non-paretic arm is
restricted. Constraint-induced movement therapy (CIMT) involves constraint of the non-
paretic arm during most waking hours while the paretic side undergoes intense task-oriented
practice. CIMT has mostly been studied in stroke survivors who have some residual capacity
to move the wrist and fingers. In one such study
89
, CIMT improved performance on the
Action Research Arm Test (which does not discriminate between recovery and
compensation) but led to no notable improvements in measures of movement quality and
impairment recovery. Several studies have found that CIMT improves the speed, efficiency
and smoothness of paretic arm movements
90–92
, but one of these studies
92
found that it does
so without diminishing reliance on compensatory trunk movements; in fact, reliance on such
movements was increased after CIMT. Together, these findings suggest that CIMT may
promote the refinement of compensatory movement strategies that improve the functional
capacity of the paretic arm.
Several studies in rodent models of stroke have found that a few weeks of daily training of
the paretic forelimb in skilled reaching tasks can improve performance (as measured by the
successful retrieval of food rewards), even when abnormalities in the paretic limb
movements that are used to perform the task persist, suggesting that the improvements result
from compensatory strategies
68,69,93,94
. In rats with substantial motor cortical infarcts, the
performance improvements were greatly diminished if the non-paretic forelimb was kept in
a sling during daily training, indicating that assistive movements of this limb probably
Jones
Page 5
Nat Rev Neurosci
. Author manuscript; available in PMC 2018 December 11.
Author Manuscript Author Manuscript Author Manuscript Author Manuscript