Cerebral Palsy: New Approaches to Therapy Marjorie A. Garvey, MD, Margot L. Giannetti, BA, Katharine E. Alter, MD, and Peter S. Lum, PhD
Corresponding author Marjorie A. Garvey, MD National Center for Cerebral Palsy and Related Disorders, National Rehabilitation Hospital, Neuroscience Research Center, 102 Irving Street, NW, Washington, DC 20010, USA. E-mail:
[email protected] Current Neurology and Neuroscience Reports 2007, 7:147–155 Current Medicine Group LLC ISSN 1528-4042 Copyright © 2007 by Current Medicine Group LLC
Cerebral palsy is the most common developmental disorder causing a physical disability arising from an injury to the central nervous system. The majority of pediatric neurologists remain minimally involved in the rehabilitation of these children. Recent advances in basic and clinical neuroscience give hope that effective rehabilitation strategies, based on motor learning science, can be developed for these children. The aim of this review is to alert pediatric neurologists to these advances.
Introduction Most pediatric neurologists are minimally involved in the rehabilitation of children with cerebral palsy, restricting their role to writing referrals for appointments with a physiatrist or prescriptions for physical and occupational therapy to prevent deterioration of their motor function. This relative absence of neurologists is partly the result of a widely accepted, long-standing belief that therapy aimed at achieving motor recovery in these children is an exercise in futility. However, recent advances in neuroscience and in clinical neurorehabilitation of upper extremity paresis have challenged this belief and provide the hope of developing more effective interventions. Until recently, it was thought that the brain was incapable of reorganizing itself once the normal course of development was complete. However, converging lines of evidence from both basic and clinical neuroscience show that this capacity to reorganize is present throughout life. A common manifestation of brain reorganization occurs in the individual’s ability to learn new motor skills. Motor learning is a critical aspect of everyday life because virtually all behavior is expressed by means of some acquired motor skill [1]. The motor learning process
is accompanied by changes in the pattern of intracortical connectivity of the motor cortex [2••]. This capacity of the brain to acquire motor skills is one aspect of a phenomenon commonly referred to as neural plasticity. When motor learning is dysfunctional, as in children with cerebral palsy, learning to perform even simple tasks is difficult and may not occur because these children require much more practice to learn even simple motor skills than their nondisabled peers. Traditional therapeutic interventions focus on helping the child compensate for the lack of these motor skills rather than having an expectation of learning new skills [3]. Experimental work in animals and clinical neurophysiologic studies in adults post-stroke have shown that the brain retains the capacity for change (ie, plasticity) after an injury [4•,5,6]. For this reason, rehabilitation science has moved away from traditional therapeutic strategies towards those based on concepts of motor learning that aim to restore motor function [7]. A growing number of studies show that when treatment strategies based on motor learning theories are incorporated into a therapy program, clinically noticeable gains in motor function occur [8••]. Establishing the efficacy of these new therapies depends upon methods that can accurately examine their ability to improve motor function. Although standardized measures of motor performance and functional status are frequently used in studies to assess rehabilitation interventions in children with cerebral palsy, they suffer from serious shortcomings [9]. Quantitative measures of motor function such as electromyography (EMG) and kinematic analyses of reaching movements can overcome these shortcomings by directly assessing movement patterns before and after therapy; they can also provide insights into the mechanisms by which these improvements were achieved [10•]. The aim of this review is to inform pediatric neurologists of the advances in both experimental neuroscience and clinical neurorehabilitation so that they can be in a position to promote evidence-based and patient-specific approaches to rehabilitation. This discussion, therefore, provides 1) a brief overview of treatments presently used by therapists to treat children with cerebral palsy, including those based on motor learning concepts; 2) a review of the process of, and the neuroplasticity associated with,
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motor learning; and 3) an outline of the quantitative methods being developed to understand neuromuscular and mechanical processes involved in motor learning.
ing science [24]. Given the potential of these strategies to improve upper extremity motor function in children with cerebral palsy, a greater understanding and in-depth knowledge of the underlying concepts would allow clinicians to maximize therapeutic opportunities.
Cerebral Palsy and History of Treatments Cerebral palsy is the most common neurologic developmental disorder causing a physical disability. It receives comparatively little attention from researchers and policy makers compared with autism as measured in the relatively small amount of government research dollars assigned to the disorder ($1000 per person with the disorder compared with $80,000 per person with autism; Personal communication, Mindy Aisen, United Cerebral Palsy, Research and Educational Foundation). As a result, only a few randomized clinical trials have evaluated therapies for the upper extremity in children with cerebral palsy, and these have shown small treatment effects [11]. This, to some degree, may be due to an implicit nihilism about the ability of therapists to really effect a positive change in motor function in individuals with this disorder. The functional limitations associated with cerebral palsy are the result of the complex interaction of primary and acquired impairments such as spasticity, weakness, contractures, joint deformities, and somatosensory dysfunction. As for other physical disabilities, the goal of therapy in children with cerebral palsy is to reduce the impact of impairments and prevent acquired problems, improve function, decrease disability, and, ultimately, to provide avenues for increased participation in family events, school, the workforce, and society [12]. To date, there are limited data regarding the effectiveness of all available therapies, traditional or otherwise, to improve upper extremity function (Table 1) [11,13]. Comparing the benefits or efficacy of treatments is not easy primarily due to a lack of evidence, as there are very few randomized controlled studies.
Rehabilitation Interventions Based on Motor Learning Concepts Although traditional therapeutic approaches show only small treatment effects, interventions that are primarily based on motor learning theories (such as constraintinduced therapy) show noticeable gains in motor function (Table 2) [3,8••,14–23]. Key features distinguish these therapeutic approaches from the concepts behind traditional therapeutic strategies: 1) they view the individual with the disability as an active participant in the learning process; 2) they aim to restore function of the paretic limb rather than achieve “independence” based on compensatory strategies; and 3) they consider repetition of voluntary movements as an essential part of the therapy [7]. Interestingly, experienced therapists tend to base interventions on motor learning strategies even when they demonstrate only an implicit awareness of motor learn-
Motor Learning Overview When a person wishes to learn a motor skill, he or she must not only know what needs to be done, but must be able to translate this knowledge into action through practice [25]. At first movements are slow, irregular, and not very accurate. With practice, under normal circumstances, movements become more fluent and controlled and, gradually, the same motor task is performed with increasingly greater skill until it is “automatic.” Through this process, frequently performed motor tasks (such as those involved in the activities of daily living) can be completed quickly and without much attention. The role of motor learning in everyday life is typically taken for granted until it is dysfunctional, when even simple tasks, such as tying one’s shoe laces in the morning, require minutes of intense concentration [26]. This is the world of a child with cerebral palsy.
Motor skill versus motor adaptation learning When an individual acquires a new motor skill, two processes are necessary: the new skill needs to be learned (“motor skill learning”) and then adapted to new environmental constraints (“motor adaptation learning”). Although acquisition of most motor skills involves both types of learning, behavioral and neuroimaging studies have shown that these two components are distinct and dissociable [27,28]. Therefore, when an individual has difficulty learning a motor skill, this can arise due to a deficit of either motor skill or motor adaptation learning. For this reason, tests have been developed that primarily assess one or the other. Motor skill learning can be tested by examining the ability to learn a motor sequence (eg, serial reaction time task). These tests measure response times as a person practices a repeating sequence. Decreasing response times indicate the presence of motor skill learning [29,30]. Motor adaptation learning is assessed by examining the ability to adapt a familiar motor skill to new constraints (eg, adaptation to external perturbations from a force field during a limb movement or to lateral displacement of vision using prisms). In the force field paradigm a subject’s reaching movements are forced off target, causing them to be inaccurate. With practice, subjects adapt to the force field and produce accurate movements [31,32].
Temporal phases of motor learning During the first phase of motor learning, considerable improvement in performance occurs within a single training session with practice of the motor skill [33]. Practice
One case report showed increased shoulder girdle strength and mobility; all others focus on lower extremity
No studies examining strength training in children with cerebral palsy
Evidence
Promote independent function, self-help skills, and problem solving
Peto
Ayers
HBOT
Conductive education
Sensory integration
Hyperbaric oxygen
Increase oxygen delivery to damaged areas of the central nervous system
Improve sensory processing
Inhibition of primitive reflex patterns in order to restore normal motor control
NeuroBobath developmental therapy (NDT)
Kelly and Darah [81]
Winstein et al. [80]
Study
Studies use different levels of Ozer et al. [82], Scheker stimulation for varying time periods et al. [83], Wright and Granat [84]
Motor learning is more effective than strength training in adults after stroke
Comments
No effect in clinical randomized trial
One study showing increased sensory and motor function after treatment
Stiller et al. [87], Reddihough et al. [88]
Side effects of barotrauma to ear
Muller-Bolla et al. [90], Hardy et al. [91], Collet et al. [92]
Not compared with traditional therapy Bumin and Kayihan [89]
No clear advantage over equally Few studies and no randomized intensive therapies controlled trials
A number of studies examining Variation in training in NDT and the Fetters and Kluzik [69], NDT with or without other way NDT is incorporated into a Kerem et al. [85], modalities; all found little effect therapy session make it difficult Law et al. [86] of NDT to assess across studies
Neuromuscular Small amounts of current One open-label study of upper stimulation (NS) / applied using surface extremity FES; increased funcfunctional electrical stimulators to increase bulk tion (Jebsen and quantitative stimulation (FES) and strength wrist extension); one study combined NS with dynamic bracing showing increased wrist extension
Buoyancy and resistance to exercises performed under water, which increases strength and endurance
Aquatic exercise
Stimulation
Muscle strengthening, improved motor skills, cardiovascular conditioning, increased endurance
Strength training
Therapeutic exercise
Goals
Specific name
Therapy
Table 1. Therapeutic interventions currently used for children with cerebral palsy
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Evaluate effectiveness of CIT in 9 children aged 21–61 mo with hemi-CP
Modified CIMT vs conTherapy group: restraint glove for ventional therapy in 21 2 h/d for 2 mo children aged 18 mo to 4 y (20 controls)
Naylor and Bower [97] / 2005
Eliasson et al. [20] / 2005
No modifications to usual routine OT/PT visits
CIT study in 20 children Sling on less affected arm for 60 h aged 4–13 y with hemi CP (6 h/d; 10 of 12 d)
Gordon et al. [19] / 2006
Outcome
Post-therapy QUEST scores increased 2- to 17-fold compared with scores at baseline and follow-up
Play and skilled activities with repetitivetask practice and shaping
Modified CIMT model therapy intervention based on child’s motivation and activities that provided challenges and repetition
Intensive unimanual training led to gains in unimanual and bimanual tasks
Improved dexterity, coordination, precision, and manipulative abilities sustained at 5-mo follow-up
Motor learning principles used in play and CIT improved ability to use paretic motivational settings hand more than children in control group 2 mo after therapy
Verbal instruction to use affected UE; gentle restraint of unaffected arm
Therapy group acquired significant number of new motor skills; maintained gains over follow-up at 3 and 6 mo
Treatment group improved significantly compared with controls and had higher PDMS scores; casting effects remained at 6-mo follow-up
Intervention beneficial when compared with baseline prestudy
Children showed significant gains in UE function in ADL
ADL—activities of daily living; CIMT—constraint-induced movement therapy; CIT—constraint-induced therapy; CP—cerebral palsy; hemi—hemiplegia; IEP—individualized education program; OT—occupational therapy; PDMS—Peabody Developmental Motor Scales; PT—physical therapy; QUEST—Quality Upper Extremity Skills Test; RCT—randomized control trial; UE—upper extremity; WMFT—Wolf Motor Function Test.
Home exercise program: 1 h of practice in evening without restraint
CIMT in day camp setting in Therapy for 7 h/d; glove-like splint for 9 children aged 13 daily activities to 18 y
Bonnier et al. [96] / 2006
Control group: standard therapy
Therapy for 1 h twice weekly, structured activities with therapists and home program for nontherapy days
Control group: continued participation in previously established IEP and therapy routines
Therapy group: casted UE of less CIT with shaping; based on family’s goals impaired arm; therapy for 6 h/d for 21 d and movements that would promote greatest function improvement
RCT with 18 children aged 7–96 mo with hemi-CP
Taub et al. [14] / 2004
Open-label RCT with crossover into treatment group after 6 mo; children received no additional intervention
Forced use (cast) in 12 children aged 1–8 y with chronic hemi-CP
Willis et al. [95] / 2002
Case 2: permanent cast on UE; 4 wk of PT/OT for 2-h long sessions; extra practice of 1.5 h/d at home
Case studies of 2 children Case 1: removable splint to less affected Intensive shaping and movements with hemi-CP, ages 19 mo UE for 11 d; patient received 2 sessions and 38 mo of OT and PT directed practice for 9 d
Glover et al. [94] / 2002
Therapy Restraining mitt for therapy sessions and Improvements in UE found after home; structured play activities and home therapy and at 8-mo follow-up; exercise program were enforced; WMFT increased use of left UE at home used at baseline, after therapy, and at during ADL after therapy 8-mo follow-up
Pierce et al. [93] / 2002
Study design
Description / subjects
CIT case study of 12-y/o left CIT for 4 h/wk for 3 wk and home hemi-CP practice
Author / year
Table 2. Studies using various modified versions of constraint-induced therapy in children with cerebral palsy
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is also important in later stages of motor learning, where further gains in learning occur across several practice sessions [25]. With extended practice, the skilled behavior becomes durable and can be readily retrieved despite long periods without practice [28,34]. Between the early and late phases of motor learning, there is an intermediate “consolidation” phase during which a new, initially fragile motor memory is transformed into a robust and stable memory [35••]. Two different behavioral phenomena occur during this phase: “off-line” improvement of skills in between practice sessions and stabilization of motor memories. The improvement of skills “off-line” between practice sessions is the result of active neurophysiologic processes within the brain [35••,36]. For some skills, off-line improvements are sleep dependent, and for others improvements occur within hours of the practice session but do not depend on sleep. Both types of off-line learning can be blocked by learning a second skill before sleep, or, for time-dependent consolidation, within 6 hours after learning the first skill [35••]. Motor memories are fragile immediately after a practice session, becoming more stable in between practice sessions. This phenomenon is most clearly seen in motor adaptation learning when a subject is asked to learn two reaching tasks (using different force fields). When one is learned immediately after the other, memory of the first one is eradicated. The longer the time interval between the two tasks, the smaller is the disruptive influence of the second task (ie, subjects can make accurate movements in both force fields if the second task is learned at least 6 hours after the first) [34,35••,37].
Influence of practice scheduling on motor learning A complex relationship exists between the way a motor skill is learned and the long-term stability of the motor skill (as measured by its performance). Effective longterm motor learning is enhanced when the individual learning the skill is challenged from the start to learn the whole task [38•,39] in a variety of settings presented in a random way [40,41] and is given little feedback from the instructor regarding his/her performance [42]. These data suggest that the way a therapy session is organized is not arbitrary but has significant effects on the long-term stability of the motor memory.
Studies of motor learning in children with cerebral palsy Studies demonstrate that children with cerebral palsy can improve their ability to grasp objects of various sizes (motor adaptation learning) when given sufficient practice, but no one type of practice schedule appears to confer an advantage over the others [43–46]. A greater number of repetitions are required to show improvements in motor skills, and the children may not achieve the same level of performance as age-matched peers [46].
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Preliminary data regarding sequence learning (motor skill learning) in children with cerebral palsy from our laboratory indicate that, compared with typically developing, age-matched children, children with cerebral palsy also require more practice to demonstrate even a small degree of learning. In addition, these children require more practice to learn a motor sequence when using their paretic hand than when they learn a sequence with their less-affected hand. No studies have directly examined the various temporal phases of motor learning in children with cerebral palsy. However, children with cerebral palsy demonstrate a deterioration of their motor performance compared with age-matched peers who show the same, if not improved, motor performance when tested 24 hours after an initial practice session [45,46]. Thus, off-line learning is most probably absent or deficient in certain children with cerebral palsy.
Brain Plasticity Associated with Motor Learning Neuroplasticity is a capacity that allows the brain to organize (or reorganize) itself in response to different stimuli. Normal brain development (developmental plasticity), which continues from conception through the third decade of life, is the best example of this organizational capacity. The ability to learn new data, processes, or motor skills (plasticity of learning and memory) is also a manifestation of plasticity. In addition, the brain has the capacity to reorganize itself after an injury (plasticity of injury and repair). These types of neuroplasticity are distinct but inter-related facets of the same remarkable capacity of the brain to respond to many different circumstances throughout life [1,47,48].
Encoding motor skills in the motor cortex The ability to perform skilled movements persists long after the completion of training, suggesting that motor skills are encoded in a durable way within the network of motor areas of the central nervous system. The cellular mechanisms thought to be responsible for the encoding process are not completely understood but include “motor maps.” These movement representations are connected to each other via an extensive system of intracortical connections that is highly dynamic and capable of rapid reorganization [2••,49]. Novel muscle synergies, formed during skilled motor training, are associated with changes in the pattern of intracortical connectivity, which then result in alterations in neuronal firing patterns [50] and in the size of the motor map in such a way that those muscles involved in the trained movements occupy a larger proportion of the map [51,52]. However, motor map reorganization requires a sufficient amount of repetition of a skilled movement and does not occur after repetition of a nonskilled task. Thus, motor skill acquisition, or motor learning, appears
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to be a prerequisite factor in driving plasticity of learning and memory in the motor cortex [53,54] In humans, skill acquisition is also associated with changes in the motor map. Using transcranial magnetic stimulation, investigators have shown that motor maps enlarge and motor cortex excitability increases during the learning of a motor skill but not during increased use of the limb without specific skill training [55]. Improvement of the motor skill correlates with the degree of motor map enlargement [56,57]. Map enlargement can first be detected after 2 hours of practice and it continues to enlarge until the motor skill is over-learned by the subject [56]. Thus, motor map changes appear to be responsible for the consolidation of the motor skill such that it becomes resistant to decay in the absence of continued training.
Motor learning following an injury to the brain There is growing evidence from work with animal models that the adult central nervous system has an extraordinary capacity for anatomic rewiring after injury, both close to and at a distance from the initial injury, and that this rewiring may play an important role in recovery [5,58]. Ischemic stroke produces both cell death and a process of repair that may involve a reactivation of developmental programs in areas connected to the infarct. The axonal sprouting within intracortical and interhemispheric projections that occurs during the repair process resembles that seen in the developing brain during axonal elongation and synaptogenesis. These projections establish substantially new patterns of cortical connections with the damaged brain areas [47]. However, as with motor learning in the intact animal, the relative success of the repair process (both in terms of the reorganization and the recovery of motor function) appears to occur only when the animal performs repetitive, task-specific, motor training tasks [59]. Studies in adults after stroke have shown similar results. In these individuals, the motor map significantly increases in size immediately after a brief period of training but then decreases toward baseline unless the training is continued. The increase in map size is associated with improved dexterity of the paretic hand although there is no direct correlation between the amount of clinical improvement and the extent of change in map area [60]. In two studies the area of the motor map both enlarged and shifted its center, suggesting that the enlargement occurred as a result of recruitment of adjacent brain areas [6,61]. Studies using functional neuroimaging (positron emission tomography and MRI) demonstrate changes in activation patterns before and after therapy. Primarily, these changes consist in an increased efficiency of cortical function after therapy compared with baseline, seen as relative decrease in activation of motor areas while performing the task [22]. However, methodologic difficulties make functional imaging less useful as a tool to understand the effect of rehabilitation [62,63].
Quantitative Measures of Motor Learning Changes in performance that occur during motor learning are made possible, in part, by selecting the most appropriate muscle synergy for the task [50]. The resulting improved movement patterns occur with or without the subject’s conscious effort, depending on whether the subject is aware of the learning process (explicit learning) or not (procedural learning) [9,27]. Therefore, to understand motor learning, it is critical to understand the changes that occur in EMG patterns in the muscles used to perform the task. Kinematic patterns provide important information on the changes in the movement patterns produced by the new EMG patterns. These quantitative measures are also an important way to overcome the shortcomings of many standardized measures presently used to assess treatment-related changes in rehabilitation studies. By quantifying motor function before and after therapy, they provide a more accurate picture of the effect of therapy on the paretic hand than those measures that assess improvements in activities of daily living. Many of these latter measures assess improvement without regard to whether they are achieved by an improvement in motor function of the paretic hand or through compensatory mechanisms using the less affected hand. Because effective masking of treatments is not always possible in rehabilitation trials, quantitative measures can also provide an important adjunct for those measures that directly assess motor function but are dependent on observer ratings [9]. In addition to introducing a threat of bias, observer-dependent measures may not be as sensitive to small changes in performance [64,65].
Kinematics, movement deficits, and motor learning EMG and kinematic data are also a potentially rich source of information regarding the neuromuscular mechanisms associated with motor function improvement. Such information can provide a springboard for further development of improved treatments. A number of studies have examined kinematic measures of reaching in children with cerebral palsy using motion capture systems [66–70]. The most commonly used method of quantifying reaching is an analysis of the number of movement units in the movement: a smaller number of movement units is an indication of smoother movement trajectories. The number of movement units in a reaching movement decreases during development in typically developing children; a mature reaching movement is associated with a single movement unit with only one stop-start action [71]. Children with cerebral palsy show an increased number of movement units in reaching movements compared with age-matched controls [66,67], and the number of movement units appears to decrease with treatment [69]. These results are similar to those found in adults after stroke; as recovery progresses, movement units gradually “blend” into smaller numbers of units, resulting in smoother movements [72,73].
Cerebral Palsy: New Approaches to Therapy
Coupled analysis of kinematics and muscle activity can provide important information regarding range of motion and the muscle synergies active at the shoulder and elbow during multijoint reaching movements. For example, voluntary movements are often associated with bursts of EMG activity in the muscles that carry out the movement [74]. These bursts of EMG activity occur in a set temporal order and have an expected length of duration unless there is an abnormality of motor control [75]. Similar analysis in individuals after stroke, and in children with cerebral palsy, suggest that in these individuals, abnormalities of reaching are associated with atypical muscle synergies, abnormal temporal order of muscle activation, and altered duration of EMG activation [68,76–79]. These insights have allowed the development of promising new interventions that directly target abnormal coupling between shoulder abductors and elbow flexors [10•].
Conclusions To take full advantage of the concepts from motor learning science for developing effective, evidence-based rehabilitation for children with cerebral palsy, therapists require not only a much better insight into the deficits of motor learning in this population, but also knowledge of how practice schedules promote or limit the stability of long-term motor learning. These issues have practical implications for therapists as they develop newer, more effective interventions to improve upper extremity function and functional independence in children with cerebral palsy. EMG and kinematic analyses of reaching patterns offer an objective means of quantifying temporal patterns of movements and coordination of limbs during motor learning, including the relatively under-studied investigation into the effects of practice schedule on memory stabilization and offline learning.
Acknowledgments This work is supported, in part, by grants 1K22 NS04 268001A1 from the National Institutes of Neurological Disorders and Stroke and 5 M01-RR020359 from the General Clinical Research Center Program of the National Center for Research Resources, National Institute of Health. Dr. Alter can be contacted at the Mount Washington Pediatric Hospital at Prince George’s Hospital Center in Cheverly, MD. Dr. Lum can be contacted at the Catholic University of America in Washington, DC.
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