You are on page 1of 10

NEURAL PLASTICITY VOLUME 8, NOS.

1-2, 2001

Exercise and Training to Optimize Functional Motor


Performance in Stroke: Driving Neural Reorganization?
Roberta B. Shepherd

School ofPhysiotherapy, Faculty ofHealth Sciences, The University ofSydney, Australia

SUMMARY cognitive engagement and practice, aiming to


increase strength, control, skill, endurance,
Neurorehabilitation is increasingly taking fitness, and social readjustment. Rehabilitation
account of scientific findings. Research areas services remain slow to make the changes
directing stroke rehabilitation are neuro- necessary to upgrade environments, attitudes,
physiology; adaptability to use and activity; and rehabilitation methodologies to those
biomechanics; skill learning; and exercise shown to be more scientifically rational and for
science (task, context specificity). Understanding which there is evidence of effectiveness.
impairments and adaptations enables a
reappraisal of interventions---for example,
changes in motor control resulting from KEYWORDS
impairments (decreased descending inputs,
reduced motor unit synchronization), secondary CVA, physiotherapy, task-specificity, exercise,
soft tissue changes (muscle length and stiffness training, brain reorganization
changes) are adaptations to lesion and disuse.
Changes in interventions include increasing
emphasis on active exercise and task-specific INTRODUCTION
training, active and passive methods of
preserving muscle extensibility. Training has This paper briefly describes a perspective in
the potential to drive brain reorganization and movement rehabilitation following brain lesion
to optimize functional performance. Research which has been in development over the past 15
drives the development of training programs, years (e.g., Carr & Shepherd, 1998; 2000). It is a
and therapists are relying less on one-to-one, perspective to which many have contributed since
hands-on service delivery, making use of circuit it has developed out of investigations in the fields
training and group exercise and of technological of motor control, motor learning; biomechanics;
advances (interactive computerized systems, cognitive, behavioral, and environmental psychology;
treadmills) which increase time spent in active neural plasticity; and neuropathology. It is based
practice. Emphasis is on skill training, stressing on the view that the methods used in movement
rehabilitation should be based in science (particularly
in the sciences related to human movement),
*Mailing address: updated as scientific understanding advances and
22 Albion Street, Waverley based on evidence of effectiveness. It remains the
NSW 2024 AUSTRALIA
tax: 61 2 9386 5386 case, however, that much of what is currently done
e-mail: R.Shepherd@cchs.usyd.edu.au in the name of movement rehabilitation still does

(C) Freund & Pettman, U.K., 2001 121


122 R.B. SHEPHERD

not meet these requirements but is based on and negative, the positive referring to exaggerations
unproved, untested concepts, and/or the personal of normal phenomena, the negative to features such
preferences of therapists and physicians. There as impairments in muscle activation and motor
seems a reluctance in some centers to push for the control. A major negative feature, weakness, is due
major changes which need to be made, both to the to loss of motor unit activation, changes in
process of neurorehabilitation and to the environment recruitment ordering, and changes in firing rates
in which it is carried out, if neurorehabilitation is (Tang & Rymer, 1981; Dietz et al., 1986). Weakness
to be optimally restorative and if it is to be time from these sources is compounded by changes in
and cost efficient. the properties of motor units and in morphological
There is increasing evidence on the effective- and mechanical changes in the muscles which
ness of many newer methods of intervention, occur adaptively as a consequence of denervation,
developed out of recent scientific investigations but also of decreased physical activity and disuse
and focusing particularly on task-specific exercise (e.g., Farmer et al., 1993; McComas, 1993). Muscle
and training. There is also evidence that training weakness and disordered motor control combine to
methods designed to stimulate motor leaming can cause functional movement disability.
have positive effects on brain reorganization after a This division still has explanatory value for clinical
neural lesion. In this paper it is argued that there are practice, although current research suggests the
at least five major areas of scientific research, the classification may be an oversimplification.
recent findings of which are driving these more However, working within this framework, it is useful
effective rehabilitation methods: to include a third set of characteristics called
Mechanisms of primary impairments under- adaptive (Carr & Shepherd, 1998; 2000). It appears
lying the neural lesion. likely that some of the features which have been
Adaptive nature of the neuromuscular systems considered positive (e.g., hypertonus and abnormal
in response to use/activity and experience. movement patterns) are more likely to be the result
Biomechanics and neural control of human of the adaptation of neural system, muscles, and soft
movement. tissues to the primary impairments (Fig. 1).
Mechanisms of motor skill leaming and the Inclusion of this additional characteristic is
critical importance of practice. useful because clarification of the mechanisms
Exercise science: task and context specificity underlying functional deficits is crucial to the
of neuromuscular action and therefore of development of rehabilitation methods and the
exercise and training. planning of rehabilitation environments. Some of
the confusion in clinical practice is to due to the
use of confusing terminology. The term spasticity
PRIMARY IMPAIRMENTS AND ADAPTATIONS is used generically to cover both neural and muscle
AFTER STROKE changes, despite the fact that it was defined at a
neurological consensus conference in the 1980s as
It is common in stroke for there to be velocity-dependent hyperactivity of tonic stretch/
involvement of the cortically-originating motor proprioceptive reflexes (Lance, 1980; 1990).
systemthe upper motor neuron (UMN), its path- Similarly, the term hypertonus (evaluated by
ways, and connections. Since Hughlings Jackson, the degree of resistance to passive movement)
it has been typical to consider the impairments that suggests an underlying neural origin, yet it appears
are associated with the UMN syndrome as positive that the resistance is largely due to changes in
EXERCISE AND TRAINING IN STROKE 123

Hyperreflexia
Positive features (spasticity)

Muscle + connective tissue changes


UMNL---- Adaptive features (altered mechanical and functional properties)
Hypertonus (resistance to passive movement)
Altered motor patterns

Weakness
Negative features Loss of dexterity

Fig. 1: The positive, negative and adaptive features following UMN lesion

muscle and connective tissue (increased stiffness and The functional significance of spasticity (as
other length and disuse-associated changes), with the hyperreflexia) remains equivocal following stroke.
contribution of hyperreflexia remaining equivocal. Indeed, from studies so far it seems likely that
Clinical tests in common use for spasticity are reflex hyperactivity may make a relatively minor
largely tests which do not discriminate between contribution to functional disability in many
the contribution of stretch reflexes and that of individuals following stroke (ODwyer et al., 1996).
altered muscle mechanics (e.g., pendulum test and Nevertheless, it remains typical for spasticity to be
the Ashworth Scale; Fowler et al., 1997). Muscle considered the major impairment following stroke.
co-contraction and stiffening of a limb can be Understanding the contribution of adaptive
taken as a sign of spasticity, but it might instead structural and functional changes in muscles and
reflect a response to fear of falling (poor balance) or knowing that these changes occur in response to
to lower limb collapse (weak lower limb muscles) muscle paralysis and weakness, compounded by
and lack of skill. Similarly, an abnormal movement disuse and physical inactivity, enables the
pattern may not reflect spasticity but arise from development of strategies (such as active exercise,
muscle imbalance caused by the preferential use of passive stretching, and orthoses) to decrease
stronger muscles and weakness or paralysis of muscle stiffness and preserve the functional
others. extensibility of muscles. At the same time, task-
124 R.B. SHEPHERD

specific training (i.e., specific training of or negatively, brain reorganization and neuro-
functional actions, such as walking, reaching, muscular responses, is driving some
standing up) stimulates the regaining of motor neurorehabilitation professionals to find the most
control by training muscles to generate and time effective interventions. A recent paper by Stefan et
force at the necessary length and the appropriate al. (2000) summarizes studies which have
relationship to each other for specific actions. demonstrated the capability of the brain (e.g., at
In some rehabilitation facilities, however, sensorimotor cortex and subcortical levels) to
there is still a lack of acknowledgment of the reorganize in response to injury. These studies
profound effects on functional performance of focused on limb amputation, nerve transection,
muscle paralysis/weakness and physical and mental focal brain lesions; motor skill acquisition-motor
inactivity and, consequently, of the need for learning; and repetition of simple movements---e.g.,
intensive exercise. In such facilities, individuals thumb movements. The authors point out that
following stroke may have little or no opportunity understanding the underlying mechanisms (and of
to practice muscle-strengthening exercises, develop course what drives them) is a necessary
cardiovascular fitness and endurance, or train requirement for the development of strategies to
specifically for the motor actions they need to promote recovery following brain damage.
regain. It can still be typical for such patients to In summary, the changes that take place at neuro-
spend long periods of the day inactive in a passive motor, cognitive-perceptual, muscular, connective
and unehallenging environment (Maekey et al., tissue, and cardiorespiratory levels are evidenced by
1996). It is interesting to note a recent paper (Maeko Neural reorganization in response to lesion,
et al., 1997) which demonstrated, after a post-stroke use, experience, and activity (Kolb, 1995).
exercise program, an improvement not only in Muscle changes, including increased muscle
aerobic capacity (cardiovascular responses) but stiffness and length-associated changes (Thil-
also in functional motor performance. Many other mann et al., 1991; Carey & Burghardt, 1993).
studies point to the improved fitness gained from Connective tissue changes such as contracture
an active exercise program (Potempa et al., 1996). of joint capsule, ligaments (Dietz et al., 1991).
Following a lesion, physiological changes At the behavioral or motor performance
which could be called reparative take place in level---adaptive motor patterns reflecting
direct response to the lesion and the cellular muscle weakness/paralysis and resultant muscle
damage incurred. In addition, the system begins to imbalance (Delp et al., 1999).
make adaptations to its altered state, and it is Decreased cardiovascular fitness and energy
evident that these are driven by what the individual levels (Potempa et al., 1996; Macko et al., 1997).
does, thinks, and experiences; i.e., use and experience Depression, anxiety, helplessness
may drive reorganizational and adaptive processes
as they do in able-bodied individuals (Jenkins &
Merzenich, 1987; Kolb, 1995; Nudo et al., 1997;
Liepert et al., 1998). If use and experience drive BIOMECHANICS, EXERCISE, AND THE
neural reorganization, so also do their converse LEARNING OF MOTOR SKILL
disuse, inactivity/immobility, and lack of meaningful
experience (Nudo & Grenda, 1992). The probability Research findings in biomechanics, exercise
that what an individual does in rehabilitation after science, and motor-skill learning inform clinical
an acute brain lesion might affect, either positively practice by providing the knowledge necessary for
EXERCISE AND TRAINING IN STROKE 125

planning the coment of training and exercise effectiveness of performance, and performance can
programs and the measurement of performance. be tested using complex tools, such as forceplates
Increased understanding of the biomechanics of and motion analysis systems, and simple ones,
everyday actions has enabled the development of such as distance walked, time taken, stride length,
models of skilled motor performance which can grip strength, and distance reached in standing.
guide movement analysis and the planning of To regain skillful performance requires not
intervention. The scientific study of skill acquisition, only the ability to generate muscle forces but also
once largely the work of psychologists, overlaps the ability to time muscle activations to control
into physiology and biomechanics as experimenters complex musculoskeletal linkages. Both bio-
begin to focus on the neural mechanisms under- mechanical and muscle studies consistently report
pinning motor learning and on the mechanical movement patterns which are specific not only to
changes taking place as motor performance becomes the task being performed but also to the context in
more skilled, i.e. more effective. Research into the which the action is being carried out (e.g.,
physiology and mechanics of exercise examines Rutherford, 1988). These findings are consistent
the specificity of exercise and training, the effects even in studies of complex postural adjustments
of exercise on muscle and cardiovascular fitness. (balance) (e.g., Nardone & Schieppati, 1988). It is
Biomechanics tells us how able-bodied subjects logical, therefore, to train individuals with movement
perform an action in a consistent, effective, and disability by giving them the opportunity to
efficient manner. It provides, therefore, information practice these actions in the relevant contexts.
about essential spatio-temporal components of an However, individuals with extreme weakness
action (i.e., muscle forces, angular displacements, and lack of motor control may not be able to
and velocities), those critical components without practice if the muscles critical to that activity are
which the action cannot be performed effectively. unable to produce and time the necessary force.
Studies of walking, stair walking, standing up and There is evidence from work by Buchner et al.
sitting down, reaching, and manipulation provide (1996) suggesting that, with marked weakness, the
objective data about these actions against which a type of strengthening exercise given may not
patients performance can be compared. matter, provided it improves a muscles force-
The body of knowledge currently available is generation. However, beyond a certain threshold
driving the development of biomechanical models of strength, exercise needs to be specific to the
of significant actions like walking, sit-to-stand, action being trained. In other words, when muscles
and reaching, which allow the development and are weak, methods such as electrical stimulation,
testing of training and exercise protocols and weight-resisted open chain exercise, isometric
guidelines (Dean et al., 1997, 2000; Texeira-Salmela contractions, and machine-assisted exercises can be
et al., 1999). Science- and evidence-based protocols given in the early stages as a means of improving
and guidelines will soon be more widely used in the muscles ability to contract. However, once
clinical practice as minimum criteria, affording the muscle strength reaches a certain threshold, exercises
opportunity for multicenter trials to find the best should be biomechanically similar to actions being
practice. trained.
Biomechanical measurement tools are Lets say that we want to train a person to
increasingly being used to test the effects of stand up and sit down after a stroke. This action
intervention. Note that the aim of exercise and requires lower limb extensor muscles which can
training is not normalization as such, but optimum lift over three times body mass and muscles which
126 R.B. SHEPHERD

can cooperate with each other to control the forces pattems of coordination through practice of the
produced. When muscles are very weak, exercises action, that is to say, motor learning. Active exercises
for quadriceps and other lower limb extensors are also decrease muscle stiffness (Hagbarth et al., 1985)
necessary to increase the force-generating ability and reflex hyperactivity, if it is present (Butefisch et
of the muscles to a certain threshold. However, for al., 1995).
transferring into improved performance of sit-to- This perspective in rehabilitation, which we
stand, exercises probably need to be closed-chain, first raised in 1982, is increasingly being seen to
produce sufficient resistance, and require a similar be critical where individuals must regain the
pattern of movement. Step-up exercises, being ability to move effectively, i.e., to regair/skill, in
closed-chain (i.e., with a fixed distal segment, in everyday actions. With stroke disability, however,
this case with the foot on the step), enable practice the actions initially learned by the individual, in
of using lower limb extensor muscles to raise the the sheltered environment of hospital and
body mass. In practice, such exercises are performed rehabilitation center, may not be appropriate for life
in a manner known to increase strength, e.g. 3 sets of outside the institution. Once the acute phase of
10 maximum repetitions. Sit-to-stand can itself be stroke is complete, the individual starts to move
performed as a strengthening exercise, with seat about as well as possible given the distribution of
height raised to make the action possible in an muscle weakness and any soft tissue adaptations
individual with muscle weakness and then lowered which may have taken place. One way in which the
to increase resistance as strength and control improve. subsequent restorative process can be viewed is as a
It is biomechanical studies of sit-to-stand which process of learning which commences as soon as the
provide the information on which training is based. person attempts an action. If the movement pattem
We know, for example, is reasonably effective, it will be repeated and
a) the optimal foot placement for mechanical leamed. If it is ineffective, alternative ways may
efficiency (Shepherd & Koh, 1996), be found (e.g., use the other hand) or the person
b) that raising seat height decreases the muscle may give up that action (e.g., replacing walking
force requirements (Rodosky et al., 1987) and with wheelchair locomotion). Moving effectively
c) that rotating the trunk/upper body forward at in the non-demanding hospital environment is not,
the hips potentiates lower limb extension (Pai however, the same as moving about in the outside
& Rogers, 1991; Shepherd & Gentile, 1994). world. Walking slowly using a 4-point cane or
It is becoming evident that transfer to actions propelling oneself in a one-arm drive wheelchair
which are dynamically similar can occur. For may be relatively effective in hospital, but, once
example, exercises which strengthen lower limb discharged home, the individual needs the ability
extensor muscles can transfer not only to improved to stand up from different chairs, walk the
sit-to-stand but also to improved speed of walking. necessary distances, cross the road at traffic lights,
The latter effect may be due to enhanced capacity and so on. If this is not possible, less and less
to bear weight through stance phase (using ground walking will be done, and there is evidence that
reaction forces) and to propel the body mass some individuals deteriorate in functional abilities
forward at push off. after they are discharged (Wade et al., 1992).
Strengthening exercises appear to have their Although the action being attempted, walking
effects by improving motor unit recruitment, the for example, is one in which the individual was
muscles force-generating capacity, the timing of previously skilled, regaining the ability to walk
peak forces, and through developing neuromotor again in the presence of considerable alteration to
EXERCISE AND TRAINING IN STROKE 127

the motor control system is probably akin to learning and timing of muscle activations and cardio-
a new action and developing skill. Rosenbaum vascular fitness and training to gain optimal skill
(1991) has pointed out that movement becomes in functional actions. The methods used are driven
more skilled with learning, and this is probably by current knowledge in many fields, many of
due to improvements in timing, tuning, and which are outside the traditional knowledge of
coordinating muscle activations. Training walking rehabilitation professionals. Clinical and experi-
should, therefore, include exercises to strengthen mental liaisons are being formed, not only between
weak muscles, to preserve muscle length, plus the physiotherapists and physicians but also with
practice of walking, if necessary with an aid such biomechanists, physiologists, psychologists, exercise
as mobile walking machine with harness to support physiologists, and computer scientists.
some body weight or to prevent a fall. Walking on However, major changes still need to take
a treadmill may be effective in forcing the place in clinical practice to take account of the
reciprocal action of lower limbs, hip extension, patients needs as an active learner and the need to
and ankle dorsiflexion at the end of stance phase, increase practice opportunity and time spent in
and in potentiating hip flexion and ankle plantar- exercising to optimize muscle strength and in
flexion. A harness (taking 30% body weight) may training. Therapists are beginning to move away
be necessary early in training when lower limb from reliance on the one-to-one, hands-on form of
muscles are too weak to support 100% body weight therapy delivery and are making use of circuit
(Hesse et al., 1995). However, intensive exercise and training and group exercise and training programs.
electrical stimulation to improve the activation of More use is being made of technological advances,
weak or paralyzed lower limb muscles may also be such as interactive computerized systems, exercise
critical in the early stages. machines giving motivational feedback, supportive
We do not yet know enough about what is walking systems, and treadmills (Hesse et al., 1995;
learned, what takes place at the neural level, and Shepherd & Carr, 1999). Conceptual advances such
how best to drive learning in disabled individuals. as the use of forms of constraint to force the
However, we do know a great deal about how able- required muscle action are being shown to be
bodied individuals learn to perform effectively and effective (Taub et al., 1993). Exercise and training
to acquire skill in a particular motor action (Magill, sessions are being carried out throughout the day,
1998; Gentile, 2000), and we can use these methods thereby increasing the time spent in practice. In
in rehabilitation. It is well known, for example, these programs, emphasis is placed on physical
that motor leaming and developing skill require training and exercise and on skill training,
practice with concrete goals and objective stressing cognitive engagement and practice,
feedback about effectiveness. The learner must gaining strength, control, and fitness. There is
have the opportunity to practice actively and to increasing evidence that such methods can be
understand the importance of frequent repetitions. effective in improving functional performance in
elderly individuals, including those with stroke
(e.g., Sherrington & Lord, 1997; Dean et al., 2000).
CONCLUSION Some health professionals, however, remain locked
into old-fashioned methods and are reluctant or
Rehabilitation to improve functional motor unable to change. The continuing dominance of
performance is increasingly becoming focused on Bobath therapy (e.g., Davies, 1990) and the
exercise and training-exercise to improve strength acceptance of this by physicians for over half a
128 R.B. SHEPHERD

century, despite lack of an up-to-date scientific paretic hand. J Neurol Sci 130: 59-68.
rationale and evidence of effective functional Carey JR, Burghardt TP. 1993. Movement dysfunction
outcomes, is hard to understand given the relevance following central nervous lesions: A problem of
neurologic or muscular impairment. Phys Ther 73"
of modem scientific knowledge to neuro- 538-547.
rehabilitation and the number of published studies Carr JH, Shepherd RB. 1998. Neurological Rehabilita-
reporting positive effects of methods based on such tion. Optimizing Motor Performance, Oxford, UK:
knowledge. Butterworth Heinemann; 350.
Since it is evident that task-specific training Carr JH, Shepherd RB. 2000. A motor learning model
for rehabilitation. In: Carr JH, Shepherd RB, eds,
has the potential to drive brain reorganization
Movement Science. Foundations for Physical
toward more optimal functional performance, it is Therapy in Rehabilitation, 2nd ed. Gaithersburg,
critical to utilize training methods most likely to Maryland, USA: Aspen Publishers; 33-110.
have a positive impact on this process and shown Davies P. 1990. Right in the Middle. Selective Trtmk
to be effective. In reviewing the literature, a sense Activity in the Treatment of Adult Hemiplegia,
of optimism comes the from the evidence presented Berlin-Heidelberg-New York: Springer-Verlag; 514.
Dean C, Shepherd RB. 1997. Task-related training
in many recent studies. These studies illustrate the
improves performance of seated reaching tasks
potential for improved outcomes with more modem following stroke: A randomised controlled trial.
active and performance-oriented methodologies. Of Stroke 28: 722-728.
major interest to neurorehabilitation will be the Dean C, Richards CL, Malouin F. In press. Task-
results of research in which training method.s are related circuit training improves performance of
tested for their effects on functional performance locomotor tasks in chronic stroke. A randomized
controlled pilot trial. Arch Phys Med Rehab.
by measurements of biomechanical change, Delp SL, Hess WE, Hungerford DS, Jones LC. 1999.
measurements of organizational changes in the Variation of rotation moment arms with hip
brain and spinal cord, post-discharge motor flexion. J Biomechanics 32:493-501.
effectiveness, and patient satisfaction. Dietz V, Ketelson UP, Berger SC. 1986. Motor unit
involvement in spastic paresis: Relationship
between leg muscle activation and histochemistry.
J Neurol Sci 75: 89-103.
ACKNOWLEDGEMENT Dietz V Trippel M, Berger W. 1991. Reflex activity
and muscle tone during elbow movements in patients
The author wishes to acknowledge the with spastic paresis. Ann Neuro130: 767-779.
contribution of Dr Janet Carr to this paper, which Farmer SF, Swash M, Ingram DA, Stephens JA. 1993.
represents theoretical work carried out in joint Changes in motor unit synchronization following
collaboration. central nervous lesions in man. J Neurophysiol
(London) 463: 83-105.
Fowler V, Canning CG, Carr JH, Shepherd RB. 1997.
The effect of muscle length on the pendulum test.
Arch Phys Med Rehab 79:169-171.
REFERENCES Gentile AM. 2000. Skill acquisition: Action, movement
and neuromotor processes. In: Carr JH, Shepherd
Buchner DM, Larson EB, Wagner EH, Koepsell TD, RB, eds, Movement Science. Foundations for
de Lateur BJ. 1996. Evidence for a non-linear Physical Therapy in Rehabilitation. Gaithersburg,
relationship between leg strength and gait speed. Age Maryland, USA: Aspen Publishers, Inc.; 111-188.
Ageing 25" 386-391. Hagbarth K-E, Hagglund JV, Norkin M. 1985.
Butefisch C, Hummelsheim H, Mauritz K-H. 1995. Thixotropic behaviour of human finger flexor
Repetitive training of isolated movements improves muscles with accompanying changes in spindle and
the outcome of motor rehabilitation of the centrally reflex responses to stretch. J Physiol 368" 323-342.
EXERCISE AND TRAINING IN STROKE 129

Hesse S, Bertelt C, Jahnke MT, Schaffrin A, Baake P, 1737-1749.


Malezic M, et al. 1995. Treadmill training with Pai Y, Rogers MW. 1991. Segmental contribution to
partial body weight support compared with total body momentuna in sit-to-stand. Med Sci
physiotherapy in non-ambulatory hemiparetic Sports Exercise 23" 225-230.
stroke patients. Stroke 26:976-981. Potempa K, Braun LT, Tinknell T, Popovich J. 1996.
Jenkins WM, Merzenich MM. 1987. Reorganisation Benefits of aerobic exercise after stroke. Sports
of neocortical representations after brain injury: A Med 21: 337-346.
neurophysiological model of the bases of recovery Rodosky MV, Andriacchi TP, Andersson GBJ. 1989. The
from stroke In: Seil FJ, Herbert E, Carlson, BM, influence of chair height on lower limb mechanics
eds, Progress in Brain Research, vol. 71. New during rising. J Orthoped Res 7:266-271.
York, NY, USA: Elsevier Science; 249-266. Rosenbaum DA. 1991. Human Motor Control. New
Kolb B. 1995. Brain, Plasticity and Behavior. Mahwah, York, NY, USA: Academic Press; 411.
New Jersey, USA: Lawrence Erlbaum; 194. Rutherford OM. 1988. Muscular coordination and
Lance JW. 1980. Symposium synopsis. In: Feldman strength training. Implications for injury rehabili-
RG, Young RR, Koella WP, eds, Spasticity tation. Sports Med 5" 196-202.
Disordered Motor Control. Chicago, Illinois, USA: Shepherd RB, Carr JH. 1999. Treadmill walking in
Year Book Medical Publishers; 485-495. neurorehabilitation. Neurorehab Neural Repair 13:
Lance JW. 1990. What is spasticity? [Letter] Lancet 171-173.
335: 606. Shepherd RB, Gentile AM. 1994. Sit-to-stand: Functional
Liepert J, Miltner WHR, Bauder H, Sommer M, relationships between upper body and lower limb
Dettmers C, Taub E, et al. 1998. Motor cortex segments. Human Movement Sci 13: 817-840.
plasticity during constraint-induced movement Shepherd RB, Koh HP. 1996. Some biomechanical
therapy in stroke patients. Neurosci Lett 250: 5-8. consequences of varying foot placement in sit-to-
Macko RF, DeSouza CA, Tretter BS, Silver KH, stand in young women. Scandinavian J Rehab Med
Smith GV, Anderson PA, et al. 1997. Treadmill 28: 79-88.
aerobic exercise training reduces the energy Sherrington C, Lord SR. 1997. Home exercise to
expenditure and cardiovascular demands of hemi- improve strength and walking velocity after hip
paretic gait in chronic stroke patients. Stroke 28: fracture: A randomized controlled trial. Arch Phys
326-330. Med Rehab 78: 208-212.
Mackey F, Ada L, Heard R, Adams R. 1996. Stroke Stefan K, Kunesch E, Cohen LG, Benecke R, Classen J.
rehabilitation: Are highly structured units more 2000. Induction of plasticity in the human motor
conducive to physical activity than less structured cortex by paired associative stimulation. Brain 123"
units? Arch Phys Med Rehab 77: 1066-1070. 572-584.
McComas AJ. 1993. Human neuromuscular adaptations Tang A, Rymer WZ. 1981. Abnormal force-EMG
that accompany changes in activity. Med Sci Sports relations in paretic limbs in hemiparetic human
Exercise 26:1498-1509. subjects. J Neurol Neurosurg Psychiatry 44:6906 98.
Magill RA. 1998. Motor Learning Concepts and App- Taub E, Miller NE, Novack TA, Cook EW, Fleming
lications. New York, NY, USA: McGraw-Hill; 326. WC, Nepomuceno CS, et al. 1993. Technique to
Nardone A, Schieppati M. 1988. Postural adjustments improve chronic motor deficit after stroke. Arch
associated with voluntary contraction of leg muscles Phys Med Rehab 74: 347-354.
in standing man. Exp Brain Res 30:13-24. Texeira-Salmela LF, Olney SJ, Nadeau S. 2000.
Nudo R, Grenda R. 1992. Reorganization of distal fore- Muscle strengthening and physical conditioning to
limb representations in primary motor cortex of reduce impairment and disability in chronic stroke
adult squirrel monkeys. Soc Neurosci Abstr 18:216. survivors. Arch Phys Med Rehab 80:1211-1218.
Nudo RJ, Wise BM, SiFuentes F, Milliken GW. 1997. Thilmann AF, Fellows SJ, Rose HF. 1991. Bio-
Neural substrates for the effects of rehabilitative mechanical changes at the ankle joint atter stroke.
training on motor recovery after ischaemic infarct. J Neurol Neurosurg Psychiatry 54: 134-139.
Neural Network [Comment] 1:121-126. Wade DT, Collen FM, Robb GF. 1992. Physiotherapy
ODwyer NJ, Ada L, Neilson PD. 1996. Spasticity and intervention late atter stroke and mobility. Br Med
muscle contracture following stroke. Brain 119: J 304:609-613.
Sleep Disorders
Stroke
Research and Treatment
International Journal of
Alzheimers Disease
Depression Research
and Treatment
Schizophrenia
Research and Treatment
Hindawi Publishing Corporation Hindawi Publishing Corporation Hindawi Publishing Corporation Hindawi Publishing Corporation Hindawi Publishing Corporation
http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014

International Journal of

Scientifica
Hindawi Publishing Corporation
Brain Science
Hindawi Publishing Corporation
http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014

Submit your manuscripts at


http://www.hindawi.com

Autism
Research and Treatment Neural Plasticity
Hindawi Publishing Corporation Hindawi Publishing Corporation
http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014

Computational and
Mathematical Methods Neurology The Scientific Epilepsy Research Cardiovascular Psychiatry
in Medicine
Hindawi Publishing Corporation
Research International
Hindawi Publishing Corporation
World Journal
Hindawi Publishing Corporation
and Treatment
Hindawi Publishing Corporation
and Neurology
Hindawi Publishing Corporation
http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014

Psychiatry Neuroscience Parkinsons


Journal Journal Disease

Journal of
Neurodegenerative BioMed
Diseases Research International
Hindawi Publishing Corporation Hindawi Publishing Corporation Hindawi Publishing Corporation Hindawi Publishing Corporation Hindawi Publishing Corporation
http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014

You might also like