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Opportunities for Early Intervention Based on Theory, Basic Neuroscience, and Clinical Science

Beverly D. Ulrich
DOI: 10.2522/ptj.20100040 Published 1 December 2010
Beverly D. Ulrich
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Abstract

Therapeutic approaches in the pediatric population have generally been less aggressive than those implemented for younger and older adults. Several factors contribute to this, starting with the challenge of engaging infants in the “goal” of therapy, their resistance to initiating behaviors that are uncomfortable or fatiguing, the desire to make therapy as functionally relevant as possible when many functional skills have yet to emerge, and residual history of outdated theoretical concepts. On the practical side of who will pay for this more aggressive approach, there is limited empirical evidence based on randomized controlled trials to convince third-party payers to fund more extensive services. This article outlines a theoretical perspective prominent in developmental science that argues not only for the importance of frequent bouts of functionally relevant activity on the self-organization of behavioral patterns, but also for the impact that should be expected from the use of rigorous interventions on underlying subsystems, such as neural organization, that support these outcomes. In order to propose some future opportunities for clinical research and application, examples from recent activity-based clinical studies are presented, along with theoretical principles, neuroscience, and other tissue science data concerning mechanisms that contribute to behavioral changes. One such opportunity is to increase the structured engagement of caregivers, guided by therapists, in administering well-defined activity intervention programs focused on the development of specific functional skills. Such an approach may be one of the few financially feasible options for generating sufficient therapy that adheres to principles for optimizing development of neuromotor control.

This is such an exciting time! Health care systems are intensely focused on the need to be efficient and cost-effective in treatments, coverage for everyone is a central goal of the US president's administration, and theory and data support the importance of early and aggressive intervention to reduce long-term costs and improve outcomes. The question is, can we capitalize on this moment in time to expand support for early intervention for infants and young children, thus leading them to a future in which they optimize their own development and functional outcomes? I believe efforts such as this, using the power of the American Physical Therapy Association's media to speak to so many readers, is a critical and important step in that process. However, the message also must reach legislators, funding agencies, and the grassroots support of families to promote both the quality-of-life value to citizens and the economic efficiencies of early, sustained, and aggressive therapeutic interventions.

One important goal in the overall plan to improve health and curb medical costs is to decrease obesity and inactivity. Activity-based protocols also are core to therapy for motor disabilities to improve neuromotor control, muscle strength (force-generating capacity) and endurance, and cardiovascular function. In the following pages, I highlight the importance of significant levels of activity very early in life for optimizing behavioral outcomes. I outline contemporary theoretical explanations for change, discuss research on change in some specific mechanisms that are important to optimizing motor behavior, and highlight clinical studies focused on changing motor behavior via increased activity. From this foundation, I propose some opportunities for future developmental neuromotor control research and clinical interventions.

Theoretical Foundation

Finding an agreed-upon name for a unified theory to explain the emergence of, and change in, motor skills over time is more difficult today than it was a decade ago. In 2000, I would have selected easily the term “dynamic systems theory,” although even then “theories” (plural) would have been more appropriate, given the diversity of disciplines from which the core principles emerged.1,2 Today, terms used more frequently that embrace similar underlying concepts and expand to include the growing body of neuromotor data include “developmental systems approach,”3–5 “probabilistic epigenesis,”6 and “neuroconstructivism.”7–9 To avoid the confusion of adding another term to the mix, I suggest that the material that follows may cluster under the more inclusive of these options: developmental systems.

One of the most important conclusions scientists examining and developing these approaches, including dynamic systems, support is that the extant body of data moves us beyond relevance in continuing to accept or debate a nature-nurture dichotomy with regard to the causes underlying emergence of and changes in patterns of behavior over time. This conclusion holds, whether we examine change early in life or later, at all levels, from subcellular entities to human organisms and populations. Replacing this is focus on processes—the ways in which many components in a system interact, sometimes including those with no obvious relevance, causing change among each other and in behavior. Smith eloquently laid out such an approach during a speech delivered at the International Conference on Infant Studies in 1998 and subsequently in publication.10 Spencer and colleagues updated this argument recently in a target article in Child Development Perspectives.3 Their point is that attributing behaviors, even those as persistent across intact humans as the emergence of walking, to an a priori genetic code for primacy is neither defensible empirically nor helpful in terms of facilitating the emergence or recovery of this functional skill. Genes, to quote Spencer et al, “do not create anything…. Genes participate in the production of proteins and in the regulation of other genes. The building of brains, bodies, and flexibility involves a cascading developmental process in which genes and their products interact within their local environment to create the substrates for further development.”11(p104) Nor does this argument accept that humans or their brains are blank slates, on which organization and behavior are created exclusively by a process of learning or exploration of the world around them. However, development is a process of self-organization, among multiple factors, within the organism and without, driven by interactions and experiences. For description alone, one might ignore processes that drive change; to have an impact on change in a system, we must understand the history, context, and interactions that constructed the current state in order to facilitate subsequent adaptations.

That behavior is dynamic and adaptive may be illustrated by a series of studies that addressed historical observations of an inverted U in the development of stepping in infants, part of the traditional sequence of motor milestones in infancy. Maturationist and some neurophysiological approaches proposed that neonatal stepping is a reflex, the essence of which resides in a central pattern generator (CPG), that is innately prescribed, located in the spinal cord, and, ultimately, is the core component for, later in life, walking.12,13 Sensory stimuli, provided by holding newborns upright and moving them forward over a firm surface, activate the neural program and cause stepping. By 2 to 3 months of age, this behavior disappears, to reappear between 8 and 11 months of age when infants cruise and walk. The argument was that as the nervous system matures, higher levels of the central nervous system inhibit the free-running action of the CPG, then restructure in subsequent months to drive the onset of walking.14,15

Thelen and Ulrich16,17 illustrated the dynamic and plastic nature of infant stepping by showing that intralimb and interlimb temporal and kinematic characteristics of newborn steps persisted in other postures, such as supine kicking, and that stepping displayed its own trajectory of interlimb coordination patterns when the context was shifted and infants were supported upright on a motorized treadmill. Even when stepping was supposed to be inhibited by higher brain centers, the behavior was easily elicited when infants were supported in water,18 and given practice, stepping never disappeared at all.19,20 Furthermore, the behaviors infants generate when supported on a treadmill are not stereotypic. Several researchers17,21–23 have shown that when babies step on a treadmill, their leg movements are highly variable, yet adaptive. Early in life, the treadmill elicits a variety of interlimb couplings (alternating, single, parallel, and double steps), and infants produce lots of nonstepping leg movements, then settle into alternation over time, without directed practice.17,22 They used multiple foot postures to contact the support surface at the end of swing, including heel-strike, which was not deemed available based on maturationists' arguments, until several months after walking onset.12,24 When the treadmill belt was split down the middle and one side moved twice as fast as the other, infants adapted spontaneously by modulating the “fast” leg to a slower frequency and increasing the frequency on the “slow” leg to maintain a steady interlimb coordination.17,25

Yet, underlying these overt alternating kinematic patterns on the treadmill were muscle activations that only began to show signs of consistency or rhythmicity late in the first year. While the many muscles and joints in the legs and pelvis converged to produce the net effect of patterned behaviors, the underlying neuromotor system vascillated among many of the possible combinations of muscle activity to respond to this context (unpublished research).26 Just as toddlers explore their many options for which muscles to use, including the timing of their onset and duration, to control upright locomotion before they settle into a stable activation pattern,27,28 infants demonstrate similarly on a treadmill the dynamic and adaptive responses possible to produce this kinematic pattern of globally rhythmic leg flexions and extensions.

The implication of these data is not that organized populations of neurons in the spinal cord and brain do not play critical roles in the emergence of stepping and walking, but rather that the essence of walking does not reside in any of these neural modules. Stepping behaviors, like other patterns of movement, are dynamic, fluid, and adaptive; their essence is in the convergence of many innate and external factors, including the context and goal of the performer. Furthermore, populations of neurons in the spinal cord are themselves dynamic, affected by the process of perceiving and acting, of changes in the periphery and centrally, like other populations of neurons throughout the nervous system.

Research also has shown that humans, including infants and young children, have multiple, redundant pathways for achieving the same functional goal. Variability in individual behaviors was a hallmark of the earliest descriptions of motor patterns observed by developmentalists such as McGraw,29,30 Gesell,31 and Shirley.32 Collapsing their many observations into normative age means and categories seems to have obscured the fact that infants who are typically and atypically developing skip common milestones, revert to earlier patterns after more complex ones emerge, and produce their own unique patterns under varied environmental contexts and their own performance goals. To be clear, these early scientists themselves correlated their developmental sequences and progressions with underlying neural maturation. Yet, as McGraw30 concluded in later writings, attempts to uncover unique neural substrates that drove these maturational outcomes had largely failed.

For a vivid illustration of the flaws in attributing motor outcomes to single causes, such as neural substrates, we can draw from populations such as children and others with Down syndrome (DS), in which multiple factors play a more visible role. One lovely example is in the solution such infants tend to discover for shifting posture from prone to seated. Like infants with typical development, they begin the transition by pushing their chests off the surface with their arms, but there the similarity ends. Infants with typical development swing their legs together around to one side and forward; infants with DS slide their legs first in opposite directions into abduction (doing a split) and then forward.33 Given the extreme laxity in their hip joints, this pattern is the path of least resistance for accomplishing their goal. Not directed by a prescribed neural plan for their actions, infants with DS, like their peers without DS, are opportunistic, discovering through exploration and practice actions that accomplish their goal, given their current state of subsystem characteristics and the context. Infants with DS can shift to producing more typical patterns for this transition if extrinsic constraints are imposed, such as placing therapeutic bands around the legs, making parallel leg movements the path of least resistance.

Similarly, children who are healthy with relatively shallow hip joints may discover that scooting on their bottoms provides better overall stability, yet allows a more upright trunk during locomotion than creeping on their hands and knees. Both patterns may occur less frequently in the population at large than the mean pattern, but they reflect similar processes in their emergence. That is, each new behavior builds on the foundation of previous experiences and solutions discovered, the functional repertoire, and subsystem strengths to allow discovery of subsequent patterns of movement that accomplish the ever-changing and expanding goals of curious and active young humans.

That history matters at all levels of interacting subsystems, and the outcome of these interactions may appear close to or well downstream of their initial convergence, has been emphasized in developmental work recently and referred to as “cascading effects.” Karmiloff-Smith8 described a sequence of behaviors that illustrate this effect in which motor and cognitive factors intertwine in ways that might not be obvious without close longitudinal examination. Early in development, infants born with Williams syndrome show impaired planning of saccadic eye movements. This impairment leads to decreased ability to follow finger-pointing actions, which results in diminished capacity to use referential pointing in parents' normal efforts to help their babies connect objects to vocabulary words. This diminished capacity fosters atypical trajectories and delay in language acquisition, although, ultimately, fairly functional language skills emerge. In an example more central to the motor domain, Holt and colleagues34,35 conducted a series of experiments with children with cerebral palsy (CP). Their results led them to argue that the high stiffness seen in these children is due, at least in part, to their early muscle weakness and emerges as a solution to generate sufficient force for locomotion. They created a mechanical model of the actual walking patterns for each leg in children with spastic hemiplegic CP. Data showed that these children generate more force with the less-affected limb than a child with typical development. They use this force to project their center of mass forward, but upward too, with each step. This movement enables them to use the stiffened, affected (and weaker) leg as a stiff vertical spring. When the body drops down onto this foot, a pogo stick–style rebound is created, propelling the system forward. These data and theoretical arguments suggest the next question to be asked is, could very early efforts to improve leg strength reduce secondary levels of high tone and stiffness in this population?

One hallmark of complex systems—open, thermodynamic systems, such as those in humans—is that they seek higher levels of complexity.36 This fact fits both the behaviors we observe in early postnatal life, in which infants continually explore and discover new actions, each a bit more demanding than those that led up to them, and our explanation for them. Empirical studies show that even the youngest babies create adaptive, goal-directed movements and demonstrate systematic learning from their experiences,37–39 and we know that existing neuromotor strength and control form the scaffolding that supports each subsequent level of construction. As newborns use their available eye muscle strength and control to attend to objects or people moving through their space, they push their systems, bit by bit, to go farther, to see more and longer. These repeated cycles of moving and perceiving the consequences lead, over time, to sufficient control of head and neck muscles to lift the head and eyes upward, leading to new, interesting things to explore. Their efforts have cascading effects, enabling more and longer movements through greater distances, toward objects, people, and sounds that attract them. Bit by bit, the foundation takes shape and expands for discovering new concepts, consistencies, and motor control. A predesign for this sequence is not necessary, or likely, given individual differences within infants who are healthy, as well as infants with atypical neurophysiological and biomechanical constraints. Yet, probabilistically, the similarities in sequential progressions follow, given the similarities in goals, substrates, and contexts they have to work with.

That rigorous practice—repeated cycles of perceiving and acting—affects recovery of neuromotor function via distinct changes within areas of the brain in children and adults is commonly accepted.40,41 The same processes are less often acknowledged in the very early foundational organization among neurons. In 1987, Edelman42 published a detailed account of early brain development based on what was known about neuroembryology, neuroanatomy, and principles of physics acting at molecular and cellular levels. Together, the system's biochemical and physical properties and environment interact prenatally to produce cell proliferation, migration, adhesion, differential growth, and the formation of vast numbers of connections. The impact of the organism's own movements and environment contribute both to the typical organization of areas of cortical specialization and to individual variations in connectivity. Labeling his proposals the theory of neuronal group selection,42,43 Edelman argued that the primary repertoire of broad patterns of network connections established before birth becomes ever more organized as the interaction with increasing numbers of sensory inputs and history of experiences grows after birth. Stated simply, through repeated cycles of perceiving and acting, synapses among populations of neurons within local areas of the brain, as well as globally, become strengthened to work together synergetically in their contributions to patterns of behavior. This process shapes the behavioral repertoire of the organism, according to what is of adaptive value in its eco-niche.

Whether the vast overpopulation of neurons and connections that emerges prenatally and the cell death that begins early to accompany the emergent synaptic organizations are sculpted or constructed continues to be debated. However, the significant role of the baby's own activity in facilitating these changes is not at issue.44,45 Karmiloff-Smith and colleagues argued that very small differences in emergent properties of areas in the brain make them somewhat more relevant to processing certain types of input than others. However, it is time and through the repeated processing of information that some become more proficient than others and more actively involved in processing particular inputs. Although plasticity in early brain development is not totally unconstrained, it seems evolution has resulted in increasing flexibility for humans, rather than increasing complexity of built-in, domain-specific constraints.8 Rather than activity being able to invoke neural plasticity only in recovery from neural damage, plasticity underlies the process of development in infants who are healthy, as well as in infants with atypical development.46–51

To summarize principles from this brief discussion of a developmental systems perspective, I offer the following principles:

  1. Behavior patterns and changes in patterns emerge via self-organized interactions among many subsystems, intrinsic and extrinsic to the organism, within a context, and the performer's goals.

  2. Behavior is dynamic and adaptive, changing in response to repeated cycles of perceiving and acting and to variations in the contextual demands or intrinsic capacities of the system.

  3. There are multiple, redundant pathways to achieving the same functional goal.

  4. History matters; factors that may not have obvious relevance to a particular outcome may have a profound, cascading impact.

  5. Organization and change at the level of the nervous system are significantly affected by repeated cycles of perceiving and acting.

Critical Subsystems: Neural, Bone, Muscle, and Adipose Tissues

Early Development of the Nervous System

Theoretical approaches to the organization of and early changes in the nervous system derive very clearly from empirical data, including studies of humans and lower animals, as well as the impact of lesions occurring naturally and induced. My goal here is not to provide a comprehensive review of what is known about the developing nervous system, but to draw attention to interactive processes and changes at many levels that engage the nervous system. Particular emphasis is on the critical role of activity in optimizing the outcome of these processes.

When human babies who are healthy are born, they are in the midst of enormous change in their nervous systems. However, their unique neural history and makeup began nearly 9 months earlier and were influenced along the way by many converging subsystems, from the biochemistry of their genes to the nutrition, exercise, and external sensory environment experienced by the mother and their changing fit and comfort with the space within which they existed. Their embryonic neural tube gave rise before birth to the vast majority of neurons they will have throughout their lifetime, and they have begun already to lose neural cells. The intricate interplay among complex cascades of gene expression interacting with influences of activity and ever-expanding local and more-distant environmental stimuli results in cells migrating to regions and creation of tiny differences in type, density, and orientation, neurotransmitters, ratio of white matter to gray matter, and so on. Changes in connection strengths begin to take hold via repeated cycles of perceiving and acting, and competition leads some local areas to settle into more specialized responsiveness to some input versus others.8,48,49

Learning, in the neurophysiological sense of biochemical changes and the neuromuscular system's attraction to some patterns of movement over others, is already in evidence. Fetuses show distinct arm and leg patterns that are repeated, yet change over the prenatal months. They emerge and disappear with an average sequential order and with waxing and waning frequencies.52,53 Numerous studies have shown that auditory inputs, such as particular types of music played in the home or the mother's voice, lead to soothing or aversive responses to these same sensory stimuli after birth.54 Even some areas of the visual cortex have been shown, via animal studies and models of early human development, to rely on specific stimuli, although not visual, to drive prenatal organization.55

Birth marks a significant event on the nervous system's developmental continuum. The frequency, amplitude, and variety of sensations, actions, and contexts increase dramatically. New functional stresses impose on the system to thermoregulate, actively ingest nourishment, perceive the differences between wet and dry diapers and between light and dark rooms, and distinguish shapes and movements floating all around them. These converging forces bring a flood of exploration—of perceiving novelties and consistencies, acting, and discovering consequences. Dendritic arborization, axonal growth, and strengthened synaptic connections proliferate and become increasingly complex, continuing at an increasing rate through the first few years after birth. Many cortical regions initially process all incoming inputs and become more specialized to specific types of input through repeated cycles of perceiving and acting. However, their function plays out in concert with multiple areas of the brain to produce behaviors in early life and in adulthood.8,42 Stiles50 stated that development of the nervous system, from the very beginning, engages “both inherited and environmental factors and rel[ies] upon their continuous interaction.”50(p196)

When neural development is interrupted, when developmental or acute lesions occur in the brain or spinal cord, we turn to basic principles for optimizing neural outcomes. Dobkin56 identified 3 ways in which neural recovery can occur: (1) new cell growth, (2) regrowth of connections, and (3) retraining of existing connectivity. The opportunities for each of these vary by area of the nervous system affected, extent of damage (eg, cell loss, amount and type of nerve loss, availability of sensory motor linkages), and timing of the insult. Regardless of the specific mechanism of neural recovery to be affected, some things are clear. Research shows that copious amounts of activity and specificity of training are critical for maximizing neuromotor control and functional outcomes.57,58

Both angiogenesis and increases in circulating levels of neurotrophins in the brain and spinal cord are mechanisms known to respond to bouts of motor activity in animals. The improvements in functional outcomes emerging from significant repetitions of motor behaviors in humans may be strongly supported by these neurophysiological responses. Angiogenesis has been demonstrated to occur in the motor cortex and cerebellum.59,60 In particular, in animals with central and peripheral nervous system damage, researchers have shown that neurotrophins, particularly brain-derived neurotrophic factor, increase in the spinal cord, hippocampus, and other brain regions.61,62

Issues of optimal timing of interventions must be considered in terms of efficiency for specific tasks, stability of vital functions, risk of infection, postsurgical interventions, and so on. This is true across developmental time and warrants scrutiny with regard to intervention at earlier ages. That aggressive therapy has recently and publicly been championed for older children and adults with spinal cord and brain lesions was brought to prominence by the sustained efforts of scientists who used basic science knowledge and dared to push the system, and some visibility has been brought by celebrity (eg, Christopher Reeve).63–65 Many research groups and significant research funding are currently devoted to these issues in order to create more basic and clinical evidence intended to aid in recovery of neuromotor control. Early intervention needs to catch up to the level of research and intervention effort dedicated to supporting development and recovery in “older” neuromotor systems.

Impact of Activity on Bone, Muscle, and Adipose Tissue

Tissues other than neural tissues are affected by early activity, but they often are given less focused research attention, at least by neuromotor control specialists. Understanding the multilayered interactions that are involved in the emergence and control of behavior compels us to examine the reciprocal interactions that emerge among neural, bone, muscle, and adipose tissues directly under conditions of aggressive neuromotor activity prescriptions during early development. Bone and muscle, in particular, respond to the “form follows function” principle. The importance of muscle tissue strength seems obvious for its role in opposing gravity, moving body parts, and maintaining upright postures and gait. Yet, how much activity is optimal for pediatric populations, particularly those with disabilities, is not clearly defined via research.

Deformities of bones, and joints in particular, tend to be seen as malleable, via external interventions, such as surgeries, castings, positioning bars, and orthoses. However, how activity itself can contribute to better joint alignments is relatively unexplored. Excessive adipose tissue can strain joints and vital organs that may already be compromised; being overweight can cause fatigue and make balance difficult for locomotion. These issues may be raised by medical professionals with patients and parents of infants and young children with disabilities. However, discussions tend to focus on nutrition and genetic influences. Infrequently has research, and thus recommendations, focused on the potential benefits of increasing activity very early in life to improve status on this aspect of development of body fat and motor behavior.

During the first few years of life, the histochemical properties of muscle and bone tissue change dramatically. Babies' bones are dominated by cartilage. Cartilage is softer, more pliable, and less dense than ossified bone, and cartilage cells are gradually replaced with minerals that add stiffness and length. The ends of long bones, and the shape of short bones as well, mold to fit function, with changes in shape and density occurring in response to the tensions placed on them. For example, babies' hip sockets are relatively flat at birth, the head of the femur being stabilized with the pelvis by tendons and ligaments.

As infants begin to bear weight on their limbs, to creep and walk, the acetabulum deepens from the forces transmitted through the head of the femur to its contact surface. Babies for whom weight bearing is delayed, such as those with CP or spina bifida, have more-porous bones and are more prone to breaking a hip or leg when they fall during locomotion.66 Increasing weight-bearing activity has been shown to enhance bone density in children with CP,67 and infants with spina bifida who walk earlier also have denser bones than later walkers.68 Bone growth also requires activity to optimize its length. Recently, Teulier et al23 showed that infants with the most common form of spina bifida, myelomeningocele, “lose ground” in the growth of their lower legs compared with infants with typical development over the first postnatal year. At birth, shank lengths were not different. In utero, babies with spina bifida have been shown to be as active as their peers with typical development. After birth, leg activity is less rigorous and active.69–71 By 1 year after birth, the slower rate of growth for babies with myelomeningocele revealed a significantly shorter limb segment. Although this relationship does not prove cause, the fact that this pattern emerged over time and selectively, at least by this point, points to inactivity and lack of weight bearing as a potential cause.

Therapists know the impact of repetition and overload for increasing muscle strength. Yet, how to translate these principles developed for adults and children into baby therapy is not obvious. Overload training involves determining maximum capacities, followed by multiple repetitions of submaximal resistance, repeated over at least 3 days per week, with progressive increases in the resistance used. No such guidelines appear in the literature for infants and toddlers, nor do valid and quantifiable strength measures. Early in life, muscle tissue has different biochemical characteristics than those of adults. They are more watery and have lower peptide levels, and fiber types are not well differentiated.72,73 Yet, change in these characteristics are linked to the activity and stresses placed on them, generally through the seemingly incessant activity self-generated by babies who are healthy and who are eager to move and to challenge their bodies to ever more interesting opportunities.74

The worldwide trend for humans to be overweight continues to rise, extending into childhood, with concerns now being voiced more strongly for infancy. Evidence increasingly highlights the importance of the pattern of adipose tissue growth during the postnatal period and the possibility that these patterns may interact with subsequent lifestyle factors to cause obesity and metabolic syndrome.75 Numerous studies have shown correlations between infant growth in weight and body mass index and childhood and early adulthood adipose tissue levels, particularly in industrialized nations.75–77 Chomtho and colleagues77 found, specifically, that greater weight gain during the first 6 months of infancy was most strongly associated with greater fat mass in childhood, whereas the second half of infancy did not relate significantly to any of the body composition measures they assessed. Some of the rate of gain in body fat may clearly be attributed to feeding practices and some to genetics, although this relationship is poorly understood and genetics studies have not focused on infancy. However, it is clear that the most basic explanation for the current epidemic of obesity and overweight humans is excessive energy intake and physical inactivity. Although pediatricians attend well to issues of the need for fat in babies' diets for proper brain growth and encourage parents to discuss babies' weight with them regularly, little mention is made of babies' activity levels as a piece of the equation for balancing healthy intake with overall healthy body composition and weight. For populations with motor disabilities that are prone to difficulties moving and weight gain, this is a factor we can no longer ignore.

To summarize this section, the nervous system—central and peripheral—is not passive, static, or prescribed in detail. Failure to engage infants and young children with motor disabilities in the energetic, exploratory, and focused efforts to move and control their bodies that infants with typical development experience means not only missing opportunities to help them find functional solutions but failing to prevent cascades of secondary and tertiary problems, including, but not limited to, negative consequences to bone, muscle, and adipose tissue.

Clinical Challenges and Opportunities

Contemporary theoretical approaches and developmental neuroscience demand a greater emphasis on rigorous and early activity intervention for infants and young children with motor disabilities. The call for early intervention is not new, but new technologies have advanced, enabling scientists to demonstrate empirically the link between babies' physical activity and normal developmental processes. The mandate is clear that for infants and young children with diminished capacity to optimize their own developmental outcomes, the focus must be not only on very early but also on aggressive and functionally relevant activity protocols. Functionally relevant protocols emphasize activities of daily living, engaging infants in actively moving their limbs and bodies through space and responding to realistic perturbations as they show the capacity to adapt appropriately. Delaying interventions until motor milestones are missed or waiting until they have appeared and then trying to fix what looks “wrong” is to lose ground, perhaps irreparably in some cases. Although plasticity is more the rule than the exception, we must remind ourselves that time marches on. Each infant, child, adult, and geriatric system builds on a history of accumulated experiences. Our delay may mean lost opportunities for a child that in some cases may never be fully recovered, such as lost bone length or the joint's capacity to reshape on its own without surgical intervention, or it may allow the emergence of a compensatory neuromotor strategy for control and force that increases stiffness and tone and that may never be overcome.

Very early and aggressive interventions have become increasingly common in surgical and pharmaceutical treatments for disabilities. For example, babies born with DS who have a heart defect are likely, today, to receive cardiac surgery within months of birth. Cardiac muscle recovers quickly, and babies improve cardiorespiratory function, becoming more active, alert, and stronger overall. These improvements create a better physiological basis for development of other subsystems as well. In 2003, the National Institutes of Health began funding a major clinical trial to determine empirically the potential benefits and negative consequences of in utero surgery to protect the spinal cord of fetuses with myelomeningocele: the Management of Myelomeningocele Study (MOMS).78 The hypothesized outcomes include decreased shunt-dependent hydrocephalus and possibly improvement in leg function, among other things. Yet, activity therapy for these same babies, those with DS and myelomeningocele, and those with many other motor disabilities, tends to lag. Physical activity therapy for babies and very young children tends to be: (1) less aggressive than prescribed for older children and adults, (2) less focused on functional skills (tending toward precursors, control of specific postures, or joint range of motion), and (3) delayed months beyond onset of disability, which would not be the strategy followed for older children and adults. These efforts may help, but they are not likely sufficient to promote optimal development of neuromotor control.

Multiple factors contribute to these disparities. Perhaps the most salient to therapists is the unwillingness, too often, of third-party payers to fund the onset of therapy until milestones are missed and to pay for the amount of time a therapist needs in order to take an aggressive approach with patients. Unfortunately, a second factor supporting the third-party payers' stance is a dearth of empirical results that show, via well-controlled and generalizable samples, the: (1) functional benefits (behavioral as well as in underlying mechanisms), especially over the long term, and (2) the cost:benefit ratio. Although we have strong theoretical and basic science arguments for the functional and long-term cost benefits of aggressive activity interventions for both younger and older adults, the data are not as conclusive for early interventions. Third, the remnants of old theoretical models, such as the maturationist approach, hinder a broader, more comprehensive approach that includes infants and young children in models designed for older people. Waiting for a skill to appear on its own, then fixing aspects that look “wrong”79 ignores the enormous weight of developmental science showing that the processes and activities and contexts in which the infant engages lead to both the quality and rate at which patterns emerge. A fourth factor is the challenge of finding ways to motivate infants to engage in the therapies we design. Motivating adults can be challenging, even when they understand the advantages to their focused efforts. Infants' motivations are quite different from ours, and their reticence to repeat actions that are not fun or comfortable can be compelling.

Dynamic systems/developmental systems theory pushes us to think out of the box about ways, from the psychological to the physical and contextual, to engage pediatric populations in self-generated repetitions of activity. “Self-generated” implies that children engage in generating muscle activations in order to adapt to the dynamic context we create for them or to explore or pursue their own goals. This process builds the subsystems necessary for new and more effective functional patterns to emerge. Basic neuroscience identifies real mechanisms, such as neural transmitters, dendritic arborization, synaptic strengths, and brain activation patterns, that are dynamic and change in response to physically active engagement, even in, or perhaps particularly in, very young children. Muscle, bone, and adipose tissue mechanisms also show similarly positive responses. Dynamic systems/developmental systems theory addresses the processes by which these mechanisms change, affecting each other in an integrated manner and converging to allow new patterns of behavior and stronger bodies to emerge. Together, the groundwork is in place to support the goals of those who need to provide and guide intervention, but more needs to be done to expand the empirical database to design protocols for implementing these goals.

Funding may always be the bane of our health care existence when it comes to providing the level of therapy required to optimize outcomes in the short term and long term. Current funding for nonacute phases of long-term problems averages 1 hour biweekly of one-to-one service with a medical professional. We know this is, alone, not sufficient to change anything. Yet, how much therapy we need to fund, how much repetition is needed, remains open to question. A mountain of research evidence has accumulated for adults, allowing some consensus and guidelines that at least 3 to 4 times per week of intense repetition and progressive overload training will increase motor strength and control, although for focused neural control therapy, the amount of time needed to optimize outcomes is much more.80,81 No one really knows the frequency and intensity of therapy required to enable infants and toddlers to significantly improve their muscle strength and neural control. Adolph and colleagues82 reported that toddlers take about 9,000 steps per day and travel the distance of more than 29 football fields when practicing their new walking skill. Yet, improvements in their gait parameters, while showing the typical negatively accelerating learning curve seen in motor learning studies of adults, require between 3 and 6 months for the rate of improvement to asymptote.83 The necessary and sufficient frequency of treatment may be less than 9,000 repetitions per day, but do we approach this in practice?

One option for overcoming the cost of direct services problem and increasing practice repetitions is to devise therapies and develop technologies that can be administered in the home by caregivers and directed by therapists or other professionals. In a series of studies, my colleagues and I designed a portable pediatric treadmill and protocol for caregivers to facilitate the development of trunk and leg control and strength needed to reduce the significant delay in walking onset experienced by infants born with DS. As multiple studies have now shown, infants are not passive when supported on a treadmill; rather, they engage in active exploration of muscle activation patterns, adapt muscle activity to perturbations, and show residual (real-time) and more sustained (over developmental time) learning effects.21,84,85

In one study, we gave parents of babies in the experimental group a treadmill and prescribed durations of practice and number of days per week.86 Caregivers supported their infants upright, on the mini-treadmill, 8 minutes a day, 5 days per week. By their own reports, parents enjoyed both their dedicated “face time” spent in social interaction with their babies and the clear boundaries we prescribed for their efforts, and they expressed optimism that they were contributing in a tangible way to the health and development of their infants. Both experimental and control group infants also received traditional physical therapy sessions biweekly. The mean advance in walking onset was 3 months for the experimental group, which was gratefully embraced by families. Although this lag may not seem large to some people, it seems the design was a step in the right direction. Our intervention provided a maximum of 960 steps per training session, 5 times per week, which did not approach the step frequency Adolph and colleagues82 indicated toddlers who are healthy use in their normal “work” of practicing their control of walking.

The next step was to build on these baseline data. We designed the original protocol with no data to guide us on how many days per week or how long practice should persist. We did not know what parents as well as their babies would tolerate without fatigue or frustration. Post hoc, we believed we could be more aggressive. Ulrich and Angulo-Barroso and colleagues87,88 subsequently replicated this study but tailored the intervention to each child's rate of progress, increasing the treadmill belt speed and adding small weights to the shank to build on the strength and control improvements each child demonstrated along the way. These modifications led to greater behavioral gains, resulting in an average 5-month advancement in walking onset compared with controls. Furthermore, toddlers, after training, showed significantly greater spontaneous activity levels, as monitored by actigraphs.

This secondary impact, greater spontaneous activity levels, was not the initial target outcome, and it may not be the only one. However, it was a relevant subsystem and one particularly meaningful today, given the global recognition of the need to increase activity and reduce adipose tissue levels to improve health. Their results illustrate the need in clinical research to design studies more clearly aligned with developmental systems theory.87,88 Multiple factors affect and are affected by motor activity and patterns. In recent studies of infants born with myelomeningocele, my laboratory group has shown that throughout the first year after birth, these babies will respond to the treadmill context by producing some steps, although at a reduced rate compared with babies with typical development and with minimal improvement (without training) over the first 6 to 9 months.23 When supported on the moving belt of the treadmill, even when not stepping, babies with myelomeningocele moved their legs in other ways, more frequently than when simply held upright on a stable surface. The population with myelomeningocele is known to show osteoporosis, reduced rate of bone growth, asymmetrical peripheral sensory and motor neural loss, and reduced frequency of spontaneous leg activity.23,69,89 To address this set of factors and the facilitation of walking onset, my colleagues and I are designing an early treadmill intervention study that will include assessment of changes in several levels of subsystems that we hypothesize will be affected by this rigorous activity, as well as monitoring external factors that could affect outcomes, such as nutrition, medical history, and so on.

Other encouraging examples of research that shows the impact of intense, activity-based therapy on increased neuromotor function are growing. Mattern-Baxter and colleagues90 showed significant improvements in standing and walking skills in children with CP as young as 2.5 years following only 4 weeks of intensive treadmill training (1 hour, 3 times per week). These laboratory-measured improvements were reflected in increased independence and reduced reliance on caregivers for functional mobility. Research documenting the effectiveness of constraint-induced movement therapy (CIMT) for upper-limb function in children with hemiplegic CP has grown substantially in the past few years.91–93 Huang et al93 concluded that among the most rigorous of these studies, the one significant outcome they had in common was increased frequency of use. In 2009, Coker and colleagues94 demonstrated that modified CIMT can be effective, even when the child is under 1 year of age.

More new, creative approaches that can be adapted for home-based, parent-administered use also are within reach. For example, Needham and colleagues95,96 created “sticky mittens” to improve pre-reaching infants' experiences in reaching for objects as a vehicle to investigate how they develop an understanding of the intentions of others. To build their experiences perceiving and acting with objects, they placed mittens dotted with Velcro* on the hands of 3-month-old infants and provided them with 2 weeks of daily practice interacting with toys that also wore Velcro patches. This intervention led infants who were healthy to explore objects more (visually and manually) and to increased arm activity, especially swipes toward objects, even when not wearing the mittens. This clever, yet simple, idea could be modified for use with infants with disabilities who need assistance building strength and control of their upper limbs. Mobiles hanging above babies' cribs were shown years ago by Rovee-Collier and Gekoski97 to elicit significant increases in leg activity in 3-month-old infants who were healthy when their ankles were tied to the mobile with a ribbon. Very recently, movement scientists have begun to study how this simple, yet elegant, perception-action contingency can be harnessed to help babies with DS and those with white matter injury improve neuromotor control.98,99

A developmental science and activity-driven process approach to facilitating change pushes us to think more critically than ever about the effects, pro and con, of the use of passive devices, such as parapodiums, serial castings, orthoses, and Dennis Brown bars, in intervention therapy. We must take seriously other options, including engaging the child in repeated cycles of activity to stretch ligaments, engage the child in accepting weight on his or her limbs, and aligning joints properly via guided movement through functional ranges of motion. Certainly, the rationales for these static positioning devices are well reasoned, and the empirical data may show generally positive outcomes. However, are these outcomes at the expense of other aspects of development of active neural control of movement, motivation to move (spontaneously), and movement through normal ranges of motion? Decreases in muscle mass and strength and loss of bone density also are outcomes of casting that have been documented in adults, as well as reductions in the cortical motor area responsible for activating muscles surrounding the affected joint.100 The demands on caregivers' and therapists' time are high, and the physical strength required to assist children as they grow in practicing functional tasks grows with them; overall, the plan for optimizing the child's development must be balanced. However, without well-controlled, aggressive, and multifaceted empirical studies, we fail to provide professionals and caregivers with optimal information from which to make choices and to promote via the health care financial system better support for building strong and, ultimately, cost-effective foundations.

Summary

To date, the idea of very early and aggressive activity-based intervention for babies has, I would argue, suffered from a concern that babies are not able to withstand rigorous efforts to perform repetitions of their own body segments designed specifically to effect change in their subsystems, from neural to ligamentous tissues. A growing body of basic and clinical science results suggest we are missing the boat on opportunities for infants with motor disabilities if we do not develop more empirically based protocols to use very early in life in order to optimize developmental outcomes. Fundamentally, I hope this article encourages more empirical studies that build on theory and basic science to test the impact, at multiple levels, of well-controlled and assertive activity-based intervention programs, the short- and long-term effects, and especially interventions that can be administered by caregivers with professional guidance. Without greater opportunities for early treatment, the costs associated with health care needs in subsequent years will be higher, but the real cost is to those affected with early-onset neuromotor disabilities.

Footnotes

  • Dr Ulrich thanks Beth Smith, Annette Pantall, Jennifer Sansom, and Sandy Saavedra for their very helpful feedback on early drafts of the manuscript.

  • This work was funded by the National Institute of Child Health and Human Development (grant RO1HD047567).

  • ↵* Velcro USA Inc, PO Box 5218, 406 Brown Ave, Manchester, NH 03103.

  • Received January 29, 2010.
  • Accepted May 23, 2010.
  • © 2010 American Physical Therapy Association

References

  1. ↵
    1. Kelso JAS
    . Dynamic Patterns: The Self-Organization of Brain and Behavior. Cambridge, MA: MIT Press; 1995.
  2. ↵
    1. Thelen E,
    2. Smith L
    . A Dynamic Systems Approach to the Development of Cognition and Action. Cambridge, MA: MIT Press; 1994.
  3. ↵
    1. Spencer JP,
    2. Blumberg JS,
    3. McMurray B,
    4. et al
    . Short arms and talking eggs: why we should no longer abide the nativist-empiricist debate. Child Dev Perspect. 2009;3:79–87.
    OpenUrlCrossRefPubMedWeb of Science
  4. ↵
    1. Adolph KE,
    2. Robinson SR
    . In defense of change processes. Child Dev. 2008;79:1648–1653.
    OpenUrlCrossRefPubMedWeb of Science
  5. ↵
    1. Oyama S,
    2. Griffith PE,
    3. Gray RD
    . Cycles of Contingency: Developmental Systems and Evolution. Cambridge, MA: MIT Press; 2001.
  6. ↵
    1. Gottlieb G
    . Probabilistic epigenesis. Dev Sci. 2007;10:1–11.
    OpenUrlCrossRefPubMedWeb of Science
  7. ↵
    1. Karmiloff-Smith A
    . The tortuous route from genes to behaviour: a neuroconstructivist approach. Cogn Affect Behav Neurosci. 2006;6:9–17.
    OpenUrlCrossRefPubMedWeb of Science
  8. ↵
    1. Karmiloff-Smith A
    . Preaching to the converted: from constructivism to neuroconstructivism. Child Dev Perspect. 2009;3:99–102.
    OpenUrlCrossRefWeb of Science
  9. ↵
    1. Mareschal D,
    2. Johnson MH,
    3. Sirois S,
    4. et al
    . Neuroconstructivism, Vol 1: How the Brain Constructs Cognition. Oxford, United Kingdom: Oxford University Press; 2007.
  10. ↵
    1. Smith LB
    . Do infants possess innate knowledge structures: the con side. Dev Sci. 1999;2:133–144.
    OpenUrlCrossRefWeb of Science
  11. ↵
    1. Spencer JP,
    2. Samuelson LK,
    3. Blumberg MS,
    4. et al
    . Seeing the world through a third eye: developmental systems theory looks beyond the nativist-empiricist debate. Child Dev Perspect. 2009;3:103–105.
    OpenUrlCrossRefPubMedWeb of Science
  12. ↵
    1. Forssberg H
    . Ontogeny of human locomotor control, I: infant stepping, supported locomotion and transition to independent locomotion. Exp Brain Res. 1985;57:480–493.
    OpenUrlPubMedWeb of Science
  13. ↵
    1. Lamb T,
    2. Yang JF
    . Could different directions of infant stepping be controlled by the same locomotor central pattern generator? J Neurophysiol. 2000;83:2814–2824.
    OpenUrlAbstract/FREE Full Text
  14. ↵
    1. Connolly KJ,
    2. Forssberg H
    1. Forssberg H,
    2. Dietz V
    . Neurobiology of normal and impaired locomotor development. In: Connolly KJ, Forssberg H eds. Neurophysiology and Neuropsychology of Motor Development. London, United Kingdom: MacKeith Press; 1997:78–100.
  15. ↵
    1. Grillner S,
    2. Wallen P
    . Innate versus learned movements: a false dichotomy? Prog Brain Res. 2004;143:3–12.
    OpenUrlPubMedWeb of Science
  16. ↵
    1. Thelen E
    . Developmental origins of motor coordination: leg movements in human infants. Dev Psychobiol. 1985;18:1–22.
    OpenUrlCrossRefPubMedWeb of Science
  17. ↵
    1. Thelen E,
    2. Ulrich BD
    . Hidden skills: a dynamic systems analysis of treadmill stepping during the first year. Monogr Soc Res Child Dev. 1991;56:1–98.
    OpenUrlPubMed
  18. ↵
    1. Thelen E,
    2. Fisher D,
    3. Ridley-Johnson R
    . The relationship between physical growth and a newborn reflex. Infant Behav Dev. 1984;7:479–493.
    OpenUrlCrossRefWeb of Science
  19. ↵
    1. Super CM
    . Environmental effects on motor development: the case of “African infant precocity.” Dev Med Child Neurol. 1976;18:561–567.
    OpenUrlPubMedWeb of Science
  20. ↵
    1. Zelazo PR,
    2. Zelazo NA,
    3. Kolb S
    . “Walking” in the newborn. Science. 1972;176:314–315.
    OpenUrlAbstract/FREE Full Text
  21. ↵
    1. Pang MY,
    2. Lam T,
    3. Yang JF
    . Infants adapt their stepping to repeated trip-inducing stimuli. J Neurophysiol. 2003;90:2731–2740.
    OpenUrlAbstract/FREE Full Text
  22. ↵
    1. Ulrich BD,
    2. Ulrich DA,
    3. Collier D,
    4. Cole E
    . Developmental shifts in the ability of infants with Down syndrome to produce treadmill steps. Phys Ther. 1995;75:14–23.
    OpenUrlAbstract/FREE Full Text
  23. ↵
    1. Teulier C,
    2. Smith BA,
    3. Kubo M,
    4. et al
    . Stepping responses of infants with myelomeningocele when supported on a motorized treadmill. Phys Ther. 2009;89:60–72.
    OpenUrlAbstract/FREE Full Text
  24. ↵
    1. Sutherland DH,
    2. Olshen R,
    3. Cooper L,
    4. Woo S
    . The development of mature gait. J Bone Joint Surg Am. 1980;62:336–353.
    OpenUrlPubMedWeb of Science
  25. ↵
    1. Thelen E,
    2. Ulrich BD,
    3. Niles D
    . Bilateral coordination in human infants: stepping on a split-belt treadmill. J Exp Psychol Hum Percept Perform. 1987;13:405–410.
    OpenUrlCrossRefPubMedWeb of Science
  26. ↵
    1. Jensen JL,
    2. Schneider K,
    3. Ulrich BD,
    4. et al
    . Adaptive dynamics of the leg movement patterns of human infants, II: treadmill stepping in infants and adults. J Mot Behav. 1994;26:313–324.
    OpenUrlCrossRefPubMedWeb of Science
  27. ↵
    1. Chang C-L,
    2. Kubo M,
    3. Buzzi U,
    4. Ulrich B
    . Early changes in muscle activation patterns of toddlers during walking. Infant Behav Dev. 2006;29:175–188.
    OpenUrlCrossRefPubMedWeb of Science
  28. ↵
    1. Chang C-L,
    2. Kubo M,
    3. Ulrich BD
    . Emergence of neuromuscular patterns during walking in toddlers with typical development and with Down syndrome. Hum Mov Sci. 2009;28:283–296.
    OpenUrlCrossRefPubMedWeb of Science
  29. ↵
    1. McGraw M
    . Growth: A Study of Johnny and Jimmy. New York, NY: Appleton-Century; 1935.
  30. ↵
    1. McGraw M
    . The Neuromuscular Maturation of the Human Infant. New York, NY: Columbia University Press; 1962.
  31. ↵
    1. Carmichael L
    1. Gesell A
    . The ontogenesis of infant behavior. In: Carmichael L ed. Manual of Child Psychology. New York, NY: Wiley; 1946:295–331.
  32. ↵
    1. Shirley MM
    . The First 2 Years: A Study of Twenty-five Babies. Minneapolis, MN: University of Minnesota Press; 1931.
  33. ↵
    1. Lydic JS,
    2. Steele C
    . Assessment of the quality of sitting and gait patterns in children with Down's syndrome. Phys Ther. 1979;59:1489–1494.
    OpenUrlPubMedWeb of Science
  34. ↵
    1. Holt KG,
    2. Fonseca ST,
    3. LaFiandra ME
    . The dynamics of gait in children with spastic hemiplegic cerebral palsy: theoretical and clinical implications. Hum Mov Sci. 2000;19:375–405.
    OpenUrlCrossRefWeb of Science
  35. ↵
    1. Fonseca ST,
    2. Holt KG,
    3. Saltzman E,
    4. Fetters L
    . A dynamical model of locomotion in spastic hemiplegic cerebral palsy: influence of walking speed. Clin Biomech (Bristol, Avon). 2001;16:793–805.
    OpenUrlCrossRefPubMed
  36. ↵
    1. Prigogine I,
    2. Stengers I
    . Order Out of Chaos: Man's New Dialogue With Nature. New York, NY: Bantam; 1984.
  37. ↵
    1. Craig CM,
    2. Lee DN
    . Neonatal control of nutritive sucking pressure: evidence for an intrinsic tau-guide. Exp Brain Res. 1999;124:371–382.
    OpenUrlCrossRefPubMedWeb of Science
  38. ↵
    1. van der Meer AL,
    2. van der Weel FR,
    3. Lee DN
    . Lifting weights in neonates: developing visual control of reaching. Scand J Psychol. 1996;37:424–436.
    OpenUrlCrossRefPubMedWeb of Science
  39. ↵
    1. von Hofsten C
    . Eye-hand coordination in newborns. Dev Psychol. 1982;18:450–461.
    OpenUrlCrossRefWeb of Science
  40. ↵
    1. Kleim JA,
    2. Jones TA
    . Principles of experience-dependent neural plasticity: implications for rehabilitation after brain damage. J Speech Lang Hear Res. 2008;51:S225–S239.
    OpenUrlCrossRefPubMedWeb of Science
  41. ↵
    1. Lang CE,
    2. McDonald JR,
    3. Reisman DS,
    4. et al
    . Observation of amounts of movement practice provided during stroke rehabilitation. Arch Phys Med Rehabil. 2009;90:1692–1698.
    OpenUrlCrossRefPubMedWeb of Science
  42. ↵
    1. Edelman G
    . Neural Darwinism. New York, NY: Basic Books; 1987.
  43. ↵
    1. Sporns O,
    2. Edelman GM
    . Solving Bernstein's problem: a proposal for the development of coordinated movement by selection. Child Dev. 1993;64:960–981.
    OpenUrlCrossRefPubMedWeb of Science
  44. ↵
    1. Eyre JA
    . Corticospinal tract development and its plasticity after perinatal injury. Neurosci Biobehav Rev. 2007;31:1136–1149.
    OpenUrlCrossRefPubMedWeb of Science
  45. ↵
    1. Johnston MV
    . Plasticity in the developing brain: implications for rehabilitation. Dev Disabil Res Rev. 2009;15:94–101.
    OpenUrlCrossRefPubMedWeb of Science
  46. ↵
    1. Elman JL,
    2. Bates E,
    3. Johnson MH,
    4. et al
    . Rethinking Innateness: A Connectionist Perspective on Development. Cambridge, MA: MIT Press; 1996.
  47. ↵
    1. Huttenlocher PR,
    2. Dabholkar AS
    . Regional differences in synaptogenesis in human cerebral cortex. J Comp Neurol. 1997;387:167–178.
    OpenUrlCrossRefPubMedWeb of Science
  48. ↵
    1. Johnson MH
    . Functional brain development in humans. Nat Rev Neurosci. 2001;2:475–483.
    OpenUrlCrossRefPubMedWeb of Science
  49. ↵
    1. Stiles J
    . The Fundamentals of Brain Development: Integrating Nature and Nurture. Cambridge, MA: Harvard University Press; 2008.
  50. ↵
    1. Stiles J
    . On genes, brains, and behavior: why should developmental psychologists care about brain development? Child Dev Perspect. 2009;3:196–202.
    OpenUrlCrossRefWeb of Science
  51. ↵
    1. Karmiloff-Smith A,
    2. Thomas M
    . What can developmental disorders tell us about the neurocomputational constraints that shape development: the case of Williams syndrome. Dev Psychopathol. 2003;15:969–990.
    OpenUrlPubMedWeb of Science
  52. ↵
    1. deVries JL,
    2. Visser GH,
    3. Prechtl HF
    . The emergence of fetal behaviour, I: qualitative aspects. Early Hum Dev. 1982;7:301–322.
    OpenUrlCrossRefPubMedWeb of Science
  53. ↵
    1. Ianniruberto A,
    2. Tajani E
    . Ultrasonographic study of fetal movements. Semin Perinatol. 1981;5:175–181.
    OpenUrlPubMedWeb of Science
  54. ↵
    1. Lecanuet JP,
    2. Krasnegor NA,
    3. Fifer WP,
    4. Smotherman WP
    1. Fifer WP,
    2. Moon CM
    . The effects of fetal experience with sound. In: Lecanuet JP, Krasnegor NA, Fifer WP, Smotherman WP eds. Fetal Development: A Psychobiological Perspective. Hillsdale, NJ: Lawrence Erlbaum; 1995:351–366.
  55. ↵
    1. Miikkulainen R,
    2. Bednar J,
    3. Choe Y,
    4. Sirosh J
    . Computational Maps in the Visual Cortex. New York, NY: Springer; 2005.
  56. ↵
    1. Dobkin BH
    . Functional rewiring of brain and spinal cord after injury: the “Three Rs” of neural repair and neurologic rehabilitation. Curr Opin Neurol. 2000;13:655–659.
    OpenUrlCrossRefPubMedWeb of Science
  57. ↵
    1. Taub E,
    2. Griffin A,
    3. Nick J,
    4. et al
    . Pediatric CI therapy for stroke-induced hemiparesis in young children. Dev Neurorehabil. 2007;10:3–18.
    OpenUrlCrossRefPubMed
  58. ↵
    1. Hallett M
    . Neuroplasticity and rehabilitation. J Rehabil Res Dev. 2005;42:xvii–xxii.
    OpenUrlPubMedWeb of Science
  59. ↵
    1. Swain RA,
    2. Harris AB,
    3. Wiener EC,
    4. et al
    . Prolonged exercise induces angiogenesis and increases cerebral blood volume in primary motor cortex of the rat. Neuroscience. 2003;117:1037–1046.
    OpenUrlCrossRefPubMedWeb of Science
  60. ↵
    1. Black JE,
    2. Isaacs KR,
    3. Anderson BJ,
    4. et al
    . Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. Proc Natl Acad Sci U S A. 1990; 87:5568–5572.
    OpenUrlAbstract/FREE Full Text
  61. ↵
    1. Vaynman S,
    2. Gomez-Pinilla F
    . License to run: exercise impacts functional plasticity in the intact and injured central nervous system by using neurotrophins. Neurorehabil Neural Repair. 2005;19:283–295.
    OpenUrlAbstract/FREE Full Text
  62. ↵
    1. Ying Z,
    2. Roy RR,
    3. Edgerton VR,
    4. Gomez-Pinilla F
    . Exercise restores levels of neurotrophins and synaptic plasticity following spinal cord injury. Exp Neurol. 2005;193:411–419.
    OpenUrlCrossRefPubMedWeb of Science
  63. ↵
    1. Dobkin BH
    . An overview of treadmill locomotor training with partial body weight support: a neurologically sound approach whose time has come for randomized clinical trials. Neurorehabil Neural Rep. 1999;13:157–165.
    OpenUrlCrossRef
  64. ↵
    1. Wolf SL,
    2. Winstein CJ,
    3. Miller JP,
    4. et al
    . Effect of constraint-induced movement therapy on upper extremity function 3 to 9 months after stroke: the EXCITE randomized clinical trial. JAMA. 2006;296:2095–2104.
    OpenUrlCrossRefPubMedWeb of Science
  65. ↵
    Christopher Reeve Foundation. Available at: http://www.christopherreeve.org/site/c.ddJFKRNoFiG/b.4048063/k.BDDB/Home.htm. Accessed January 26, 2010.
  66. ↵
    1. Henderson RC,
    2. Kairalla JC,
    3. Barrington JW,
    4. et al
    . Longitudinal changes in bone density in children and adolescents with moderate to severe cerebral palsy. J Pediatr. 2005;146:769–775.
    OpenUrlCrossRefPubMedWeb of Science
  67. ↵
    1. Wilmshurst S,
    2. Ward K,
    3. Adams JE,
    4. et al
    . Mobility status and bone density in cerebral palsy. Arch Dis Child. 1996;75:164–165.
    OpenUrlAbstract/FREE Full Text
  68. ↵
    1. Mazur JM,
    2. Shertleff DB,
    3. Menaelaus M,
    4. Colliver J
    . Orthopedic management of high-level spina bifida: early walking compared with early use of a wheelchair. J Bone Joint Surg Am. 1989;71:56–61.
    OpenUrlPubMed
  69. ↵
    1. Sival DA,
    2. van Weerden TW,
    3. Vles JS,
    4. et al
    . Neonatal loss of motor function in human spina bifida aperta. Pediatrics. 2004;114:427–434.
    OpenUrlAbstract/FREE Full Text
  70. ↵
    1. Chapman D
    . Context effects on the spontaneous leg movements of infants with spina bifida. Pediatr Phys Ther. 2002;14:62–73.
    OpenUrlCrossRefPubMed
  71. ↵
    1. Rademacher N,
    2. Black DP,
    3. Ulrich BD
    . Early spontaneous leg movements in infants born with and without myelomeningocele. Pediatr Phys Ther. 2008;20:137–145.
    OpenUrlCrossRefPubMed
  72. ↵
    1. Maltin CA,
    2. Delday MI,
    3. Sinclair KD,
    4. et al
    . Impact of manipulations of myogensis in utero on the performance of adult skeletal muscle. Reproduction. 2001;122:359–374.
    OpenUrlAbstract
  73. ↵
    1. Tomanek RJ,
    2. Colling-Saltin AS
    . Cytological differentiation of human fetal skeletal muscle. Am J Anat. 1977;149:227–245.
    OpenUrlCrossRefPubMedWeb of Science
  74. ↵
    1. Baldwin KM
    . Muscle development: neonatal to adult. Exerc Sport Sci Rev. 1984;12:1–19.
    OpenUrlCrossRefPubMed
  75. ↵
    1. Lucas A,
    2. Fewtrell MS,
    3. Cole TJ
    . Fetal origins of adult disease: the hypothesis revisited. Br Med J. 1999;319:245–249.
    OpenUrlFREE Full Text
  76. ↵
    1. Demerath EW,
    2. Choh AC,
    3. Czerwinski SA,
    4. et al
    . Genetic and environmental influences on infant weight and weight change: the Fels Longitudinal Study. Am J Hum Biol. 2007;19:692–702.
    OpenUrlCrossRefPubMedWeb of Science
  77. ↵
    1. Chomtho S,
    2. Wells JC,
    3. Williams JE,
    4. et al
    . Infant growth and later body composition: evidence from the 4-component model. Am J Clin Nutr. 2008;87:1776–1784.
    OpenUrlAbstract/FREE Full Text
  78. ↵
    1. Adzick NS
    . Fetal myelomeningocele: natural history, pathophysiology, and in utero intervention. Semin Fetal Neonatal Med. 2010;15:9–14.
    OpenUrlCrossRefPubMedWeb of Science
  79. ↵
    1. Winders P
    . Gross Motor Skills in Children With Down Syndrome: A Guide for Parents and Professionals. Bethesda, MD: Woodbine House; 1997.
  80. ↵
    1. Taub E,
    2. Uswatte G,
    3. Pidikiti R
    . Constraint-induced movement therapy: a new family of techniques with broad application to physical rehabilitation: a clinical review. J Rehabil Res Dev. 1999;36:237–251.
    OpenUrlPubMedWeb of Science
  81. ↵
    1. Brosseau L,
    2. Wells GA,
    3. Finestone HM,
    4. et al
    . Clinical practice guidelines for constraint-induced movement therapy. Top Stroke Rehabil. 2006;13:48–50.
    OpenUrl
  82. ↵
    1. Adolph KE,
    2. Vereijken B,
    3. Shrout PE
    . What changes in infant walking and why. Child Dev. 2003;74:475–497.
    OpenUrlCrossRefPubMedWeb of Science
  83. ↵
    1. Damon W,
    2. Lerner R,
    3. Kuhn D,
    4. Siegler RS
    1. Adolph KE,
    2. Berger SA
    . Motor development. In: Damon W, Lerner R, Kuhn D, Siegler RS eds. Handbook of Child Psychology. Vol 2: Cognition, Perception, and Language. 6th ed. New York, NY: Wiley; 2006:161–213.
  84. ↵
    1. Vereijken B,
    2. Thelen E
    . Training infant treadmill stepping: the role of individual pattern stability. Dev Psychobiol. 1997:30:89–102.
    OpenUrlCrossRefPubMedWeb of Science
  85. ↵
    1. Jensen JL,
    2. Schneider K,
    3. Ulrich BD,
    4. et al
    . Adaptive dynamics of the leg movement patterns of human infants: II. treadmill stepping in infants and adults. J Mot Behav. 1994;26:313–324.
    OpenUrlCrossRefPubMedWeb of Science
  86. ↵
    1. Ulrich DA,
    2. Ulrich BD,
    3. Angulo-Kinzler RM,
    4. Yun J
    . Treadmill training of infants with Down syndrome: evidence-based developmental outcomes. Pediatrics. 2001:108:E84.
    OpenUrlCrossRefPubMedWeb of Science
  87. ↵
    1. Ulrich DA,
    2. Lloyd MC,
    3. Tiernan CW,
    4. et al
    . Effects of intensity of treadmill training on developmental outcomes and stepping in infants with Down syndrome: a randomized trial. Phys Ther. 2008;88:114–122.
    OpenUrlAbstract/FREE Full Text
  88. ↵
    1. Angulo-Barroso R,
    2. Burghardt AR,
    3. Lloyd M,
    4. Ulrich DA
    . Physical activity in infants with Down syndrome receiving a treadmill intervention. Infant Behav Dev. 2008;31:255–269.
    OpenUrlCrossRefPubMedWeb of Science
  89. ↵
    1. Campbell SK,
    2. Vander Linden DW,
    3. Palisano RJ
    1. Hinderer KA,
    2. Hinderer SR,
    3. Shurtleff DB
    . Myelodysplasia. In: Campbell SK, Vander Linden DW, Palisano RJ eds. Physical Therapy for Children. St Louis, MO: Saunders-Elsevier; 2006:735–789.
  90. ↵
    1. Mattern-Baxter K,
    2. Bellamy S,
    3. Mansoor JK
    . Effects of intensive locomotor treadmill training on young children with cerebral palsy. Pediatr Phys Ther. 2009;21:308–318.
    OpenUrlCrossRefPubMed
  91. ↵
    1. Charles J,
    2. Gordon AM
    . A critical review of constraint-induced movement therapy and forced use in children with hemiplegia. Neural Plast. 2005;12:245–261.
    OpenUrlPubMed
  92. ↵
    1. Hoare B,
    2. Imms C,
    3. Carey L,
    4. Wasiak J
    . Constraint-induced movement therapy in the treatment of the upper limb in children with hemiplegic cerebral palsy: a Cochrane systematic review. Clin Rehabil. 2007;21:675–685.
    OpenUrlAbstract/FREE Full Text
  93. ↵
    1. Huang HH,
    2. Fetters L,
    3. Hale J,
    4. McBride A
    . Bound for success: a systematic review of constraint-induced movement therapy in children with cerebral palsy supports improved arm and hand use. Phys Ther. 2009;89:1126–1141.
    OpenUrlAbstract/FREE Full Text
  94. ↵
    1. Coker P,
    2. Lebkicher C,
    3. Harris L,
    4. Snape J
    . The effects of constraint-induced movement therapy for a child less than one year of age. NeuroRehabilitation. 2009;24:199–208.
    OpenUrlPubMedWeb of Science
  95. ↵
    1. Needham A
    . Improvements in object exploration skills may facilitate the development of object segregation in early infancy. J Cogn Dev. 2000;1:131–156.
    OpenUrlCrossRefWeb of Science
  96. ↵
    1. Needham A,
    2. Barrett T,
    3. Peterman K
    . A pick-me-up for infants' exploratory skills: early stimulated experiences reaching for objects using “sticky mittens” enhances young infants' object exploration skills. Infant Behav Dev. 2002;25:279–295.
    OpenUrlCrossRefWeb of Science
  97. ↵
    1. Reese HW,
    2. Lipsitt LP
    1. Rovee-Collier CK,
    2. Gekoski MJ
    . The economics of infancy: a review of conjugate reinforcement. In: Reese HW, Lipsitt LP eds. Advances in Child Development and Behavior, Vol 13. New York, NY: Academic Press; 1979:195–255.
    OpenUrlPubMed
  98. ↵
    1. Angulo-Kinzler RM
    . Motor learning and attention in infants with and without Down syndrome. Poster presented at the 30th Annual Meeting of the Society for Neuroscience; November 4–9, 2000; New Orleans, LA.
  99. ↵
    1. Fetters L
    . Development of Infant Motor Performance Laboratory (DIMPL). Available at: http://pt.usc.edu/SubLayout.aspx?id=2008. Accessed January 10, 2010.
  100. ↵
    1. Liepert J,
    2. Tegenthoff M,
    3. Malin JP
    . Changes of cortical motor area size during immobilization. Electroencephalogr Clin Neurophysiol. 1995;97:382–386.
    OpenUrlCrossRefPubMed
View Abstract
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Vol 96 Issue 12 Table of Contents
Physical Therapy: 96 (12)

Issue highlights

  • Musculoskeletal Impairments Are Often Unrecognized and Underappreciated Complications From Diabetes
  • Physical Therapist–Led Ambulatory Rehabilitation for Patients Receiving CentriMag Short-Term Ventricular Assist Device Support: Retrospective Case Series
  • Education Research in Physical Therapy: Visions of the Possible
  • Predictors of Reduced Frequency of Physical Activity 3 Months After Injury: Findings From the Prospective Outcomes of Injury Study
  • Use of Perturbation-Based Gait Training in a Virtual Environment to Address Mediolateral Instability in an Individual With Unilateral Transfemoral Amputation
  • Effect of Virtual Reality Training on Balance and Gait Ability in Patients With Stroke: Systematic Review and Meta-Analysis
  • Effects of Locomotor Exercise Intensity on Gait Performance in Individuals With Incomplete Spinal Cord Injury
  • Case Series of a Knowledge Translation Intervention to Increase Upper Limb Exercise in Stroke Rehabilitation
  • Effectiveness of Rehabilitation Interventions to Improve Gait Speed in Children With Cerebral Palsy: Systematic Review and Meta-analysis
  • Reliability and Validity of Force Platform Measures of Balance Impairment in Individuals With Parkinson Disease
  • Measurement Properties of Instruments for Measuring of Lymphedema: Systematic Review
  • myMoves Program: Feasibility and Acceptability Study of a Remotely Delivered Self-Management Program for Increasing Physical Activity Among Adults With Acquired Brain Injury Living in the Community
  • Application of Intervention Mapping to the Development of a Complex Physical Therapist Intervention
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Opportunities for Early Intervention Based on Theory, Basic Neuroscience, and Clinical Science
Beverly D. Ulrich
Physical Therapy Dec 2010, 90 (12) 1868-1880; DOI: 10.2522/ptj.20100040

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Opportunities for Early Intervention Based on Theory, Basic Neuroscience, and Clinical Science
Beverly D. Ulrich
Physical Therapy Dec 2010, 90 (12) 1868-1880; DOI: 10.2522/ptj.20100040
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More in this TOC Section

  • Variation and Variability: Key Words in Human Motor Development
  • Variability in Postural Control During Infancy: Implications for Development, Assessment, and Intervention
  • The Complexity of Childhood Development: Variability in Perspective
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