Postural control during reaching in typical and atypical development
van Balen, Lieke Cornelia
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van Balen, L. C. (2018). Postural control during reaching in typical and atypical development: Mapping the maze of roads leading to Rome. Rijksuniversiteit Groningen.
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Postural control during reaching
in typical and atypical development
Mapping the maze of roads leading to Rome
Postural control during reaching in
typical and atypical development
Mapping the maze of roads leading to Rome
Proefschrift
ter verkrijging van de graad van doctor aan de Rijksuniversiteit Groningen
op gezag van de
rector magnificus prof. dr. E. Sterken en volgens besluit van het College voor Promoties.
De openbare verdediging zal plaatsvinden op woensdag 20 juni 2018 om 16.15 uur
door
Lieke Cornelia van Balen
geboren op 28 april 1982 te Groningen
Beoordelingscommissie
Prof. dr. B. Steenbergen Prof. dr. J.G. Becher Prof. dr. O.F. Brouwer
© L.C. van Balen, 2018
Postural control during reaching in typical and atypical development. ISBN: 978-94-034-0650-3 (Printed book)
ISBN: 978-94-034-0649-7 (PDF)
Druk: GVO drukkers & vormgevers B.V., Ede
Research School of
Chapter 1: Introduction ... 9 Chapter 2: Development of postural adjustments during reaching in
typically developing infants from 4 to 18 months... 33 Chapter 3: Development of postural adjustments during reaching in
infants at risk for cerebral palsy from 4 to 18 months ... 59 Chapter 4: Early intervention and the development of postural
adjustments during reaching in infants at risk of cerebral palsy: an in-depth analysis of a randomized controlled
trial ... 85 Chapter 5: Postural adjustments in infants at very high risk for
cerebral palsy before and after developing the ability to
sit independently ... 113 Chapter 6: Are postural adjustments during reaching related to
walking development in typically developing infants and
infants at risk of cerebral palsy?... 135 Chapter 7: General Discussion ... 155
Summary 173
Samenvatting 179
Dankwoord 185
Postural control is not the first thing that comes to mind when people think about motor development. In fact, many healthcare professionals are unfamiliar with the term. Yet the control of posture is a skill that underlies all motor activities of daily life, and without postural control we would never develop the ability to reach, sit, stand or walk. The development of motor skills and the development of postural control are tightly intertwined and depend upon each other in a reciprocative fashion. This makes postural control a subject worthy of investigation. Although the knowledge on the subject is accumulating, many things are still unknown. This is particularly true for early development of postural control, both in typical and atypical motor development.
The aim of this thesis is to gain more insight into postural control during early development, both typical and atypical. We examined parameters of postural control during reaching movements of typically developing infants and infants at risk of developmental motor disorders. However, since the term is so unfamiliar to many, perhaps the first question to answer is: ‘What exactly is postural control?’. Therefore, in this chapter, an introduction to the field of postural control is given. It starts with some history of neuroscience and biology, since this history has been very influential in the consecutive theories of motor development that have dominated the ideas on postural development. It then addresses the definition of postural control and describes the relevant current knowledge of postural development in both typically developing infants and infants at risk of developmental motor disorders. Since we also studied the effect of physiotherapeutic intervention on postural control, a short history of the field of early physiotherapeutic intervention is also given. These sections will then have paved the way for the introduction of the research projects that led to this thesis, followed by an outline of the thesis itself.
THEORIES OF MOTOR DEVELOPMENT
The mechanisms of motor development are a long-standing subject of debate. Over the last century, several theories to explain these mechanisms have been put forth. In this paragraph, the Neuromaturation Theory, Dynamic Systems Theory and Neuronal Group Selection Theory (NGST) will be discussed. These theories, like many others in biology and medicine, have been strongly influenced by the nature vs.
nurture debate, which deserves mentioning in this context. In the first half of the 20th
century, the ideas of Darwin were beginning to be accepted while at the same time, in psychology, behaviourism was in full bloom.
The behaviourists, for example John B. Watson and B. F. Skinner, felt that behaviour was the only objectively observable and interpretable variable that was produced by the black box that was the nervous system. The finding that reflexes could be conditioned, which was famously demonstrated by Pavlov’s dog, convinced the behaviourists that behaviour was able to cause changes in neural organisation. At the same time, embryologists and biologists studying the anatomy of the nervous system in relation to its function, were of the opinion that changes in neural organisation caused changes in behaviour. The neuromaturation theory was set forth in these surroundings. It will be explained primarily with the work of Arnold Gesell, who has become the icon of maturationism. Gesell (1880-1961) observed that all infants go through a series of developmental milestones. Although the individual timing was subject to variation, the order of the milestones was consistent between infants and Gesell concluded that motor development must be following a genetically predetermined developmental program that naturally unfolds over time.1,2 This view is now called ‘Maturation Theory’ or ‘Neural Maturation Theory’, in
which motor development is described as the natural maturation of the nervous system according to a genetically predetermined plan. Based on his countless observations of developmental trajectories, Gesell compiled schedules of developmental norms that could be used to assess the ‘developmental age’ of a child.3,4 Although the neuromaturation theory is now adapted with or replaced by
views that incorporate a more important role of environmental experience, such schedules of developmental milestones are still in use today. In the Netherlands, the ‘van Wiechenschema’,5 in which acquisition of milestones is compared to norms
derived from percentiles of the population, is used in public health services as a screening instrument for developmental disorders in almost all Dutch children from birth to the age of 4 years.
Gesell’s ideas were not only inspired by his observed milestone sequences, but also by the work of Darwin and Coghill.1 George Coghill was a neuro-embryologist
who described how changes in neural connections in the Amblystoma salamander species were followed by the emergence of specific motor behaviors.6 For Gesell,
and motor behaviour. The fact that new behaviours in the salamander were preceded by physical changes in the nervous system caused him to conclude that the behavioural changes must be a result of physical growth and not the other way around. Development of motor behaviour, therefore, was essentially the result of development of the physical human and the physical brain. Combining the ideas of Darwin and Coghill, he viewed motor development as growth patterns that, as a result of thousands of years of evolution, had been anchored in the human genes. He compared motor development to embryological growth, stating that development takes place in successive epochs of directional growth, in a cephalo-caudal and proximal-distal direction, following the direction of embryological neuronal growth.1,2 The influence of the environment is reduced to a minimal role.
Gesell wrote that the environment consists of factors that can support growth and development, but can never generate the progressions of ontogenesis.2
A contemporary of Gesell, Myrtle McGraw (1899-1988), was more flexible in her interpretation of the nature-nurture debate. Her initial work clearly reflects maturationist ideas such as the cephalo-caudal direction of development, and the idea that many motor tasks can only be acquired after the nervous system has reached a certain level of maturity.7 However, unlike Gesell, McGraw was not focused
on tables of developmental norms but instead observed development while trying to influence learning processes. In a famous experiment, she selected identical twins Jimmy and Johnny and manipulated Johnny’s development by teaching him new skills, while leaving Jimmy to grow up without interference. She showed that practice could advance the acquisition of certain motor skills, and induce changes in motor performance that were measurable later in life.7 During her career she came to the
conclusion that development is an ongoing, ever-changing process of interaction and feedback, and that one should try not to think in dichotomies such as cortical vs. subcortical, maturation vs. learning and nature vs. nurture.7 In her countless
observations of developing infants, she noticed how normal development was characterized by variation, both within and between infants. She was probably one of the first researchers who acknowledged the bidirectional nature of motor development, in other words that neuronal maturation not only influenced behaviour, but also the other way around. However, her contributions went relatively unrecognized as the interest in motor development diminished during the 1950s and 1960s, and McGraw is often characterized as a maturationist.
With the advent of the computer, theories that viewed the mind as a logical, computing system became popular. The brain was seen as a thinking machine that performed logical operations on sensory input and produced motor actions or other behaviour as a result.8 Learning takes place as a result of feedback loops of the
computational system, and sensory, processing and motor units are regarded as separate systems. While this can be a useful model for some tasks, it was increasingly recognized in the 1980s and 1990s that in reality, it is impossible to regard the brain as a separate system from the body and its inputs and outputs. It is in this setting that the Dynamic Systems Theory of development was born.
Originally, Dynamic Systems Theory is a field in mathematics, physics and chemistry in which differential equations are used to describe the behaviour of complex dynamic systems with multiple measureable quantities. Examples of these systems are numerous: the flow of water through a pipe, the weather, the stock market and so on. At any given time, the system is said to be in a certain state that can be described by a set of numbers representing the components of the system. By continuous interaction between intrinsic and extrinsic factors that influence the system, the system moves from one state to another. These states are coherent, higher-order structures that spontaneously emerge from the dynamic interaction of the system’s components. For example, in the so-called Belousov-Zhabotinskii chemical reaction, the interaction between simple chemicals in a reaction chamber produces moving coloured patterns of circles and spirals that are not intrinsic properties of the chemicals themselves, but emerge from the dynamic interaction of the reaction’s components. As such, dynamic systems are said to be nonlinear. As Farmer and Packard put it (quoted by Thelen and Smith9): “Adaptive behaviour is an
emergent property which spontaneously arises through the interaction of simple components. Whether these components are neurons, amino acids, ants or bit strings, adaptation can only occur if the collective behaviour of the whole is qualitatively different from that of the sum of the individual parts. This is precisely the definition of nonlinear”.
In chemistry, most reactions and systems are in thermodynamic equilibrium, meaning that the energy and momentum of the system are uniformly distributed and there is no flow from one region to another. Such a system is stable unless energy is added to the system. Dynamic systems such as the Belousov-Zhabotinskii reaction, however, are far from thermodynamic equilibrium, yet are stable because
they are open systems that continuously extract energy from the environment, using part of this energy to maintain or reach certain states, and dissipate part of the energy back to the environment (this is why these systems are called dissipative structures).9 Within the constraints of the system caused by its elements and their
interaction with the environment, the system can occupy different states of its potential ‘state space’. States that are relatively stable are called attractor states. For example, if physical fitness could be described by a two-dimensional state space of heart rate and body temperature, the attractor state would be the small part of this state space that constitutes the normal values of these variables. Through exercise or illness, the values of these parameters may be temporarily shifted in one direction or the other, but they would return to their normal ‘attractor state’ once the external stimulus that causes the shift disappears.
In Dynamic Systems Theory, the concept of variability gains a new meaning. While in Maturation Theory, variability is a deviation from the normal pattern and as such is regarded as noise, in dynamic systems variability is regarded as an indicator for stability of the system. A strong attractor state results in less variable behaviour than a weak attractor state. In other words, variability is part of the data, not simply noise. When a child has recently learned to stand upright, the attractor state is weaker and the displacements of the centre of gravity are greater than those of an adult. Thus, changing variability is an indicator for learning and development. Variability is deemed largest when the system is in transition from one attractor state to another. From a developmental view, therefore, variability is very important as it enables the system to explore other states and find new attractor states.
In Dynamic Systems Theory, the physical substance of the elements that comprise the system is deemed relatively unimportant and can be molecules, cells, tissues, organs, neurons, neural networks, or entire organisms. What counts is the dynamic interaction that produces patterns at a higher level of abstraction, such as behavioural patterns from interaction between neurons, and social patterns from interaction between individuals. Not surprisingly, Dynamic Systems Theory opposes maturationist views of development. The nervous system and development are seen as an integrated whole from which behaviour emerges, and the brain and genes are not credited as driving forces of development. For example, walking and learning to walk self-organises because of the behavioural attractor states occupied by the dynamic system that is formed by earlier developmental events, anatomical and
neural constraints, a motivation to move, and environmental factors such as gravity.9
With the concepts of emergence and self-organisation through interaction between components, Dynamic Systems Theory deals with the problem of how complex behaviour can arise from simple elements such as neurons, without referring to a ‘homunculus’ in the brain or genes that controls the process. However, in this way the role of the biological substrate (including genes and heredity) is reduced to a degree that does not do justice to the importance of its contribution. The fact that the behaviour of a system can be described by a set of equations that primarily deal with interactions between elements, doesn’t mean that the elements themselves and their evolution deserve no attention. Therefore, while Dynamic Systems Theory is a very useful frame of reference for explaining certain aspects of development, for others a different framework that pays more attention to the biological substrate and its evolution may be more suitable.
This is where the Neuronal Group Selection Theory (NGST) comes into play: a theory that was also formulated as a reaction to the information processing views of brain function and development, but regards development from an evolutionary perspective while acknowledging the role of the environment. It was formulated in 1978 by Gerald Edelman, who had won a shared Nobel Prize in 1972 for his work on the immune system. He compared the development of the brain to the development of the immune system in an individual, in which an abundance of diverse lymphocytes is created, followed by selection of only the ones that meet the selection criteria and degeneration of the non-qualifying surplus. His theory of neural Darwinism and neuronal group selection is now referred to as the Neuronal Group Selection Theory (NGST).10,11
According to this theory, large amounts of structured neuronal groups containing 50-105 neurons are formed during embryogenesis and development.
Primary connections between and within these groups are determined by genetic programming and epigenetic events, including cell growth, cell migration, cell death, synapse formation and synaptic selection. Together, these interconnected groups form a primary repertoire of responses in such a way that there is a very large diversity of responses, yet many groups can respond, to a smaller or larger extent, to a given signal. This provides the basis for the enormous variability in neuronal activity that is needed for adaptive behaviour. The strengthening and weakening of synaptic connections (by temporal correlations between firing patterns of connected cells and
cell groups) provides a mechanism by which the system can select connections based on input signals. In this way, a secondary neural repertoire is formed that is shaped by experience. Memory and consciousness result from phasic re-entrant signalling, which is defined as ongoing parallel signalling between different neuronal groups (or back into the same single neuronal group) in a bidirectional and recursive fashion. This results in associations between stored patterns and current sensory or internal input. Novelty of signals is dealt with by comparison of re-entrant and new signals in a cycle as well as by the fact that there are primary and secondary repertoires. Completely new information must activate the primary repertoire, with subsequent information activating selected subsets from the secondary repertoire based on the earlier experience.10,11
The Neuronal Group Selection Theory was formulated in general terms to provide a framework for understanding higher brain function and development, but can nicely be translated to motor development. The primary and secondary neural repertoires translate into variation and adaptability of motor behaviour. Similar to Dynamic Systems, variability is a key concept in NGST, as it provides the basis for selecting adaptive behaviour. For the purpose of clarity, I will devote some words to the various terminology used in this context. Based on NGST, there are two aspects to the concept of variability, which are visible in two phases of motor development. The first is variation,12 previously referred to as primary variability.13 Variation refers
to the size of the primary and secondary repertoire. This is visible in the variation in motor behaviour that is seen when the nervous system explores all options provided by the primary repertoire, and in the number of adaptive strategies available in the secondary repertoire. The second aspect of variability is adaptability, previously referred to as (secondary) variability.12,13 It emerges in the phase of secondary
variability and refers to the ability to adapt motor behaviour to the specifics of the situation.
Learning a new motor skill starts with the phase of variation, in which all possibilities of the primary repertoire are explored. Part (but not all) of the primary repertoire are the so-called central pattern generators (CPG), which are groups of cells with a more or less pre-defined activation pattern resulting in certain motor behaviour. For example, rhythmical movements such as chewing and early locomotion in animals have been shown to be generated by CPGs.14 This is where
complex movement patterns are assumed to emerge by self-organisation of the different parts of the system in conjunction with environmental factors, while NGST proposes a genetic foundation in the form of CPGs and anatomical growth patterns that are adapted throughout development as a result of epigenetic processes and experience. Exploring the options of the primary repertoire results in abundant variation in motor behaviour as well as a wealth of self-produced afferent information that can be used to adapt the neural networks to specific needs. This results in the phase of adaptability, in which optimal strategies are selected and adapted to the situation. In this phase, situations are compared to earlier experience, and synaptic strengthening has led to fast and selective activation of signalling pathways that were successful in the past.
The principles of NGST have proven very useful for explaining various developmental phenomena (they will also be discussed in the subsequent section on the development of postural control). For example, very early in life, it can already be demonstrated that variation is an important characteristic of normal motor development. Already in the foetal stage, the nervous system produces spontaneous movement patterns which are termed ‘general movements’ (GMs).15 These patterns
consist of continuous, elegant movements potentially involving all parts of the body, which have a certain randomness to them and are rich in diversity. General movements continue to be expressed until approximately 4 months after term birth, when goal-directed movements appear.15 There are age-related changes in GM
characteristics.16 The integrity of the quality of the GMs, in which variability and
complexity are important characteristics, depends on a normal and intact developing nervous system, and changes in the quality of GMs predict developmental motor disorders such as cerebral palsy (CP).17–19 In terms of NGST, general movements can
be seen as explorations of the primary repertoire that give the infant trial-and-error information, thus laying the groundwork for formation of the secondary repertoire of goal-directed movement. In the next section, the neuronal group selection theory will also be used as a framework for explaining the development of postural control.
DEVELOPMENT OF POSTURAL CONTROL
Posture refers to the relative position of the body and its parts with respect to each other and the environment. Postural control or the regulation of posture is necessary for practically all motor actions. It involves maintaining balance (i.e., keeping the centre of gravity within the support surface) and providing the prerequisite link between perception and action. The development of postural control is therefore highly intertwined with development of other motor skills and has been the subject of many studies on motor development. Nevertheless, there is still a lot to be learned. The ability to maintain balance has often been studied with perturbation studies, in which a person’s balance is disturbed by a sudden movement of the support surface on which the person sits or stands. The postural responses to a sudden balance disturbance can be measured by electromyography (EMG). The perturbation causes a complex pattern of muscle contractions independent of muscle stretch, suggesting that these postural adjustments are centrally generated and not just a combination of reflexes generated from the spinal cord.20 In 1985, Nashner &
McCollum21 found several more or less fixed postural recruitment patterns and
suggested that the postural adjustments evoked by such sudden balance disturbances were derived from a limited set of distinct muscle recruitment strategies that they referred to as ‘movement synergies’. Forssberg & Hirschfeld20 noted that
backward sway was always accompanied by early recruitment of the ventral muscles, while forward sway was accompanied by early recruitment of the dorsal muscles. In other words, the postural adjustments were direction-specific. Similar responses were seen in five- to eight-month-old infants who had not yet mastered sitting independently.22 Given these characteristics, they proposed a two-level central
pattern generator for postural adjustments: at the first level, a simple format such as the spatial pattern of the muscle activation would be generated; at the second level, the centrally generated pattern could be shaped and timed by interaction from the entire somatosensory, vestibular, and visual input.20,22 Supporting the supposition
that the ability to produce direction-specific postural adjustments is a basic level of postural control with an innate origin, direction-specific postural adjustment were also found after the majority of perturbations in one-month-old infants.23,24 In other
words, direction-specificity or a basic spatial organisation of postural adjustments could be part of the primary repertoire, while fine-tuning of the postural response
would be part of de secondary repertoire. This fine-tuning is visible in for example the number of muscles that are recruited and the amplitude of the postural response as measured by EMG. Initially, these parameters are characterized by variation. However, between 3 and 10 months of age, a preference for the so-called ‘complete pattern’ emerges, in which all direction-specific muscles are recruited in concert in response to a perturbation.24 During the same period, the ability to adjust the EMG
amplitude of the postural response to the degree of perturbation develops.25
Inducing balance disturbances by perturbations is, of course, a rather artificial way of studying postural adjustments. In addition, only reactive postural adjustments can be studied with this design. This is why postural control has also been studied during reaching movements, since such movements are more subtle, internally triggered balance disturbances. Not only is this experimental design a better approximation of real life, but it also has the advantage that anticipatory postural adjustments can be studied. These are postural adjustments that result from feed-forward processes in anticipation of a balance disturbance. Anticipatory adjustments are seen in adults before the onset of the actual movements that might induce a balance disturbance, but knowledge on the development of anticipatory postural adjustments in infants is still scarce. In general, studies using a reaching movements design show a less clear-cut picture of postural development than perturbation studies. At the age of 4 months, only 40-50% of reaching movements are accompanied by direction-specific postural adjustments.26 Little is known on the
development of postural fine-tuning – this is one of the subjects of this thesis: chapter 2 deals with development of postural adjustments during reaching in typically developing infants between 4 and 18 months of age.
Finally, the development of postural control has also been studied by measuring postural sway. The most often used approach for this is measuring displacements of the centre of pressure (COP), which is the point of application of the sum of all forces acting between the body and its support surface. Both linear and nonlinear COP measurements have been studied. Linear COP aspects include amplitude and velocity of COP displacement, usually measured in the anterior-posterior and lateral directions. Characteristic of the COP is that it is never entirely still; there is always some displacement around a central point even in quiet stance or sitting. This variation in linear COP measurements was traditionally regarded as noise of the nervous system combined with measurement error. However, it is now recognized
that this variation is a key element of balance control, reflecting a purposeful search of the limits of stability. Such an active search provides sensory information about posture, orientation and the dynamics of the interaction between the body and the environment, enabling the individual to adjust balance control processes to the current situation. In other words, perception supports action and action supports perception.27,28 In terms of NGST, the variation reflects active exploration by the
nervous system of the possibilities and limits of balance. In terms of Dynamic Systems theory, the system shows continuous variation due to interaction of the limbs, muscles, nervous system, gravity and the environment, causing the system to move within and between attractor states of balance. Dynamic Systems theory has inspired the use of nonlinear COP measurements, which have become increasingly popular in recent years. Nonlinear measurements include the Lyapunov Exponent, which is an indicator of the stability (as opposed to degree of variability) of COP trajectories; the Correlation Dimension, which is a method to evaluate the number of degrees of freedom during posture; and Approximate Entropy, which is a method to determine the complexity of the COP time series.29 These nonlinear measurements show
differences between infants who have not yet mastered a certain motor skill, such as sitting, and infants who have mastered the skill.29 They are also different for typically
developing infants compared to infants at risk of motor disorders,30,31 providing
opportunities for evaluating postural development and therapy.
INFANTS AT RISK OF DEVELOPMENTAL MOTOR DISORDERS
The most common cause of serious childhood disability in developed countries is Cerebral Palsy (CP). CP was traditionally defined as a ‘disorder of posture and movement due to a defect or lesion in the immature brain’, but this definition has undergone several revisions over the years and is still the subject of debate.32 It is
now considered to be an umbrella term for a heterogeneous group of developmental disorders, described as ‘permanent disorders of the development of movement and posture, causing activity limitation, that are attributed to non-progressive disturbances that occurred in the developing foetal or infant brain. The motor disorders of CP are often accompanied by disturbances of sensation, perception, cognition, communication, behaviour, by epilepsy and by secondary musculoskeletal
problems’.32,33 CP is attributed to brain lesions that occurred during the foetal stage
or early infancy. Many factors can contribute to the development of CP, including premature birth, infections (both during pregnancy and in early infancy), asphyxia (usually in combination with other factors), intoxications and genetic abnormalities. As implied by the definition, postural control is impaired in children with CP. The extent of the impairment varies with the degree of disability, which ranges from minor dysfunction to major impairments causing severe disability in daily life. This broad range has given rise to several classification schemes for CP, of which the most widely used is the Gross Motor Function Classification System (GMFCS).33,34 The
GMFCS classifies children with CP into five levels of disability, based on functional mobility or activity limitation. Emphasis in this classification is on sitting and walking ability and to which extent assistive devices are needed. For example, a child at GMFCS level I walks without restrictions, can sit independently and only has limitations in more advanced gross motor skills, while a child at level III walks with assistive mobility devices and eventually learns to sit independently but often needs additional support. Finally, a child at level V has severely limited self-mobility even with the help of assistive technology, requires extensive support in sitting and never learns to sit independently.
A stable sitting position enables an individual to use the arms and hands for all sorts of tasks, which is why considerable effort has been invested in studying postural control during sitting in children with cerebral palsy. In perturbation studies, children with cerebral palsy usually show direction-specific postural adjustments, like typically developing children.35,36 Those that do not, presumably never develop the ability to
sit independently. Thus, the basic level of postural control is present in most children with CP, and seems to be a prerequisite for independent sitting. However, there may be some impairment at the basic level, as infants at high risk of CP (with the ability to sit independently) less often show direction-specific postural adjustments after perturbations.37 In contrast, fine-tuning of postural adjustments is almost always
impaired in children with cerebral palsy. Responses to perturbations are more stereotyped and less adapted to task constraints, which is visible in both the number and order of muscle recruitment and (lack of) amplitude modulation.35
Reaching studies also show that the development of postural control is impaired in children with CP. Like in perturbation studies, children with CP usually show direction-specific postural adjustments during reaching, but they only start using
them consistently at a later age than typically developing children. The second level of control is characterised by stereotyped top-down recruitment, where typically developing children show much more variation. In addition, like in perturbation studies, postural adjustments during reaching are not or to a lesser degree adapted to task constraints, for example in amplitude modulation.
Due to the inscrutable plasticity of the developing brain, cerebral palsy can only be reliably diagnosed at the age of 1½-2 years. Therefore, studies in early infancy are usually performed with groups of children at risk of developing CP, for example infants born prematurely, infants with brain lesions, or infants with abnormal general movements or development. Part, but not all, of these infants will eventually develop CP. Those who do not develop CP usually develop a minor neurological dysfunction (i.e. their neurological development is suboptimal but not impaired to such a degree that it can be diagnosed as CP). As a group, infants at risk of CP seem to have a postural development that is different from that of typically developing infants. For example, preterm infants at 4-6 months corrected age show relatively immobile postural behaviour (i.e., fewer and/or smaller COP displacements) than typically developing infants.39 Similar findings were reported by Kyvelidou et al. in infants who
later developed CP.40 Nonlinear COP measurements also show that high-risk infants
have more repetitive (less varied) and less complex postural sitting behaviour than typically developing infants.30,41,42
EARLY INTERVENTION
Many children with or at risk of developmental motor disorders are given physiotherapy from an early age onwards. The rationale for starting physiotherapeutic intervention as early as possible is that plasticity of the brain is largest in early infancy, thus early intervention has the greatest potential for beneficial effects. The goals of intervention, however, are not only to optimize motor development and maximize the potential of the child, although these form an important focus of therapy. Early intervention programmes also increasingly focus on general well-being of the child, parenting and coping techniques of the caregivers, and overall family functioning.
In the Netherlands, early paediatric physiotherapy is mainly based on the principles of Neurodevelopmental Treatment (NDT) and functional physiotherapy. NDT was developed by Karel and Berta Bobath in the 1940s. The Bobaths considered the handicap of children with CP to be due to an interference with the development of normal postural control against gravity.43 According to them, the underlying brain
lesion results in the release of abnormal movement patterns, in association with various types of abnormality of postural tone. NDT uses ‘key points of control’ from which patterns of abnormal activity can be inhibited, while at the same time facilitating normal movements. Treatment consists of ‘handling’ the child: the therapist guides the child and the child guides the therapist in continuous feedback loops with the goal of making the child’s reactions as normal as possible. Through the close relationship between muscle tone on the one hand and patterns of posture and movement on the other, the Bobaths advocated that normal movements obtained during treatment would also normalise muscle tone.43 Thus, treatment
consists of inhibiting abnormal movement patterns while at the same time facilitating normal movement patterns by special handling techniques. The idea behind this is that the damaged brain has produced (only) abnormal movement, and the child needs the experience and the sensation of normal movements in order to learn these patterns: these sensations produce memories that the child can use to produce normal movements. Nevertheless, therapy should not focus on following a ‘normal’ developmental sequence, but rather on the needs of the individual child. Treatment should be flexible and guided by the child’s response to it, and individualised therapy develops on the basis of the close interplay between child and therapist. It should focus on those motor skills that are needed for development of the most needed functional skills of that particular child.
Although the Bobaths had initially thought that the exercises from treatment would automatically carry over into activities of daily life, this turned out not to be the case.43 Therefore, they later sought to actively incorporate preparation for specific
functions into the treatment. They also saw the need to teach the parents to continue therapy at home, as the time the child spends with the therapist is limited and most movement is carried out at home. However, despite these adaptations of NDT, studies have shown that there is little carry-over of results into daily-life activities44,45
and that early interventions based on NDT do not seem to have a beneficial effect on motor development.46,47 Under the influence of Dynamic Systems theory, the goal
of physiotherapy therefore shifted from ‘normality’ to ‘functionality’. Functional physiotherapy emphasizes the importance of practicing functional tasks, especially those that are problematic in daily life. Rather than striving for ‘normal movement patterns’, it is important to set goals of therapy in the functional domain, based on the interaction of the individual with the environment with respect to functional skills. This also implies that therapy should always be given in a context-specific environment. Another major conceptual difference between NDT and functional therapy is that the functional approach is based on an active rather than a passive view of motor learning; people learn by actively attempting to solve the problems inherent to a functional task, rather than repetitively practicing normal patterns of movement.44 The different approach of functional therapy has gained popularity and
has been compared with NDT-based therapy in clinical trials, but with inconsistent results. Some studies have shown better results for functional therapy than for NDT-based therapy,44,48 but not in all studies a difference was found.49 Early paediatric
physiotherapy in the Netherlands is usually based on NDT, functional therapy, or a mixture of both, with or without influences of other schools of physiotherapy.
Another concept that is now becoming increasingly influential in infant physiotherapy, is the concept of family-centred care. In a family-centred approach, the service provider (meaning any healthcare professional involved in the infant’s care, for example a physiotherapist or paediatric neurologist) forms a collaborative partnership with family and child and actively involves them in the care process, including information exchange for informed decisions, collaborative goal setting, and responsiveness to family priorities and choices.50,51 Caring for children with or at
risk of developmental motor disorders involves more than just helping the child to achieve optimal motor development; coping with the situation of a child who may have life-long special needs can be a challenge that requires different coping strategies from parents. The goal of family-centred care is to increase quality of life of all family members. Fostering parental well-being, in addition to that of the child, promotes 1) a positive caregiving environment, 2) better family functioning and a better parent-child relationship, and 3) an active role of the parent in managing their child’s care and supporting their child’s development, all of which may contribute to the well-being and developmental outcome of the child. Several studies have shown beneficial effects on both child and parental outcomes.50,51
In the last decade, a family-centred physiotherapy programme was developed at the University Medical Center Groningen (UMCG). The COPCA programme (COPing with and CAring for children with special needs) is based on two components: (1) family involvement and educational parenting and (2) the neuromotor principles of the neuronal group selection theory.52 The
family-involvement and educational component focuses on family autonomy, family responsibility and family-specific parenting. The therapist takes on a coaching role in which there is a bidirectional, open dialogue to uncover the family’s competences, goals, hopes and coping strategies. Through this coaching strategy, the COPCA coach aims to promote autonomous decision-making of the family, and to encourage their capacity for solving problems of daily care, while respecting individuality in parenting. COPCA aims to promote activities and participation of the family, including the infant with special needs.
The neurodevelopmental component of COPCA is based on the principles of NGST, with emphasis on self-exploration and trial-and-error. As discussed earlier, NGST proposes a phase of extensive exploration, which is characterized by variation, followed by a phase of adaptability, which is characterized by learning to select optimal strategies for adapting motor actions to the task at hand. An infant with an early brain lesion not does not only have a limited repertoire of motor strategies, but also a limited ability to select optimal strategies (due to deficits in sensory information processing). Therefore, far more exploration and trial-and-error experience is needed for selecting an optimal strategy. To this end, COPCA promotes ample active motor experience in a variety of conditions, as well as challenging the infant to test his/her limits. While NDT promotes facilitation of movements using handling techniques, COPCA uses a hands-off approach that challenges the infant to explore his/her own motor repertoire, as hands-on facilitation may interfere with the infant’s active motor learning process.52 Since the limited repertoire of the child may
not include all strategies of typical development, the goal of COPCA is not to obtain the ‘normal’ strategy, but to obtain the best and most adaptive strategy given the infant’s ability. This implies accepting atypical strategies, in contrast to the NDT approach that tries to inhibit ‘abnormal’ strategies. COPCA aims to increase functionality while acknowledging the impairments of the infant.
THE VIP AND L2M 0-2 PROJECTS
The effects of COPCA were first evaluated in the ‘vroegtijdige interventie project’ (VIP; Dutch for ‘early intervention project’). This was a randomized controlled trial comparing COPCA to traditional infant physiotherapy (TIP) consisting of a mix of NDT and functional approaches. From 2003 to 2005, infants admitted to the neonatal intensive care unit of the University Medical Center Groningen were eligible for inclusion if they showed definitely abnormal general movements at 10 weeks corrected age, indicating a high risk of developmental disorders. The infants were block-randomized to receive either COPCA or TIP between 3 and 6 months corrected age. Outcome measures of the study included neurological condition, gross motor development, and cognitive development. Results of the VIP project show that although motor development was similar between the groups, typical COPCA actions such as family involvement, variably challenging the infant to produce active motor behaviour and stimulating at the limit of the infant’s capabilities, had positive correlations with developmental outcome at 18 months corrected age.53 In addition
to the primary endpoints, EMG measurements were taken at 4, 6 and 18 months corrected age to evaluate postural control during reaching movements. Results of these EMG measurements are described in chapter 3 and 4 of this thesis.
In the VIP trial, about 25% of infants eventually developed CP, which made the CP subgroup rather small for proper evaluation of effects in this group. Therefore a second trial, named LEARN 2 MOVE 0-2 or L2M 0-2, was designed in which infants with a very high risk of CP were investigated.54 L2M 0-2 was set up as part of the
Dutch national LEARN 2 MOVE research programme L2M, which evaluates new interventions in rehabilitation for children and adolescents with CP in different age cohorts. Infants between 0 and 9 months corrected age were recruited based on the presence of either 1) cystic periventricular leukomalacia diagnosed by serial ultrasound, 2) a unilateral or bilateral parenchymal lesion of the brain, 3) term/near-term asphyxia resulting in Sarnat55 2 or 3 with brain lesions on MRI and/or with
neurological dysfunction during infancy suggesting the development of CP, or 4) neurological dysfunction suggestive of development of CP. Infants were randomized to receive either COPCA or TIP once a week for a year. Outcome measures focused on performance of mobility-related activities, participation and family function and on body functions and structures. The infants were assessed at inclusion (T0), and at
3, 6 and 12 months after the onset of the intervention (T1, T2, and T3). Infants included prior to the corrected age of 8 months were also assessed at 21 months corrected age (T4). The assessments also included EMG measurements of reaching movements. Part of the results of these postural control assessments form chapters 5 and 6.
OUTLINE OF THE THESIS
This thesis studies the development of postural control mechanisms in both typically developing infants and infants at risk of developing CP. The field of motor development is highly influenced by the history of neuroscience and biology in general, particularly the nature-nurture debate, which is why the current chapter (chapter 1) began with a historical perspective. The aim of this chapter was to give the necessary background for the subsequent chapters, by first introducing different theories of motor development, and subsequently introducing the relevant current knowledge and recent advances leading to the research reported in this thesis.
Chapter 2 describes the development of postural control in terms of EMG parameters during reaching movements of typically developing infants between 4 and 18 months of age. The EMG parameters studied include direction-specificity, postural recruitment patterns, recruitment order of direction-specific postural muscles, and anticipatory postural activation.
Chapter 3 compares the results of the postural control data from the typically developing infants described in chapter 2 to those of infants at risk of developmental motor disorders. These at-risk infants formed the control group (receiving traditional infant physiotherapy; TIP) of the VIP trial that evaluated the effects of the new intervention programme COPCA compared to TIP.
Chapter 4 evaluates whether intervention according to COPCA has a different effect on the infant’s postural parameters compared to those of TIP intervention.
Chapters 5 and 6 explore the relationship between changes in postural control and the acquisition of the developmental milestones of independent sitting and independent walking, respectively. To this end, in chapter 5, the data of the children of L2M 0-2 were compared to those of the typically developing infants from the VIP-project, but this time the groups were not based on age but on stage of sitting
development. Similarly, in chapter 6, the data of L2M-infants who developed the ability to stand and walk independently were compared to those of a newly recruited group of typically developing infants, with groups also based on developmental stage instead of age.
Chapter 7 presents a discussion of the findings reported in the previous chapters.
REFERENCES
1. Gesell AL. The embryology of behavior: the beginnings of the human mind. New York: Harper, 1945.
2. Gesell AL. Infant development: The embryology of early human behavior.
London: Hamilton, 1952.
3. Gesell AL, Amatruda CS (eds). The first five years of life: a guide to the study of the preschool child : from the Yale clinic of child development. New York: Harper & Brothers, 1940.
4. Gesell AL, Amatruda CS. Developmental diagnosis; normal and abnormal child development. Oxford: Hoeber, 1941. 5. Laurent De Angulo MS, Brouwers-de Jong EA,
Bulk A (eds). Ontwikkelingsonderzoek in de jeugdgezondheidszorg: het van Wiechenonderzoek; de Backe-Fassaert motoriektest. Assen: Van Gorcum B.V., 2015. 6. Coghill GE. Anatomy and the problem of
behaviour. Cambridge: University Press, 1929. 7. McGraw MB. The Neuromuscular Maturation of the Human Infant. 1943, Reprint ed. Mac Keith Press, 1989.
8. Rescorla M. The Computational Theory of Mind. In: Zalta EN (ed). The Stanford Encyclopedia of Philosophy. 2015. http://plato.stanford.edu/archives/win2015/e ntries/computational-mind/ (accessed 6 March 2016).
9. Thelen E, Smith LB. A dynamic systems approach to the development of cognition and action. Cambridge, Mass.: MIT Press, 1994.
10. Edelman GE. Group selection and phasic reentrant signaling: a theory of higher brain function. In: The mindful brain. Cambridge, Mass: MIT Press, 1978.
11. Edelman GM. Neural Darwinism: selection and reentrant signaling in higher brain function. Neuron 1993; 10: 115–125. 12. Hadders-Algra M. Variation and variability:
key words in human motor development.
Phys Ther 2010; 90: 1823–1837.
13. Touwen BC. How normal is variable, or how variable is normal? Early Hum Dev 1993; 34: 1–12.
14. Forssberg H. Neural control of human motor development. Curr Opin Neurobiol 1999; 9: 676–682.
15. Prechtl HF. Continuity of Neural Functions from Prenatal to Postnatal Life. Oxford: Blackwell Scientific Publications Ltd., 1984. 16. Prechtl HF, Hopkins B. Developmental
transformations of spontaneous movements in early infancy. Early Hum Dev 1986; 14: 233– 238.
17. Hadders-Algra M. Early brain damage and the development of motor behavior in children: clues for therapeutic intervention? Neural Plast 2001; 8: 31–49.
18. Hadders-Algra M. General movements: A window for early identification of children at high risk for developmental disorders. J Pediatr 2004; 145: S12-18.
19. Prechtl HF. Qualitative changes of spontaneous movements in fetus and preterm infant are a marker of neurological dysfunction. Early Hum Dev 1990; 23: 151– 158.
20. Forssberg H, Hirschfeld H. Postural adjustments in sitting humans following external perturbations: muscle activity and kinematics. Exp Brain Res 1994; 97: 515–527. 21. Nashner LM, McCollum G. The organization
of human postural movements: a formal basis and experimental synthesis. Behav Brain Sci
1985; 8: 135–172.
22. Hirschfeld H, Forssberg H. Epigenetic development of postural responses for sitting during infancy. Exp Brain Res 1994; 97: 528– 540.
23. Hedberg A, Forssberg H, Hadders-Algra M. Postural adjustments due to external perturbations during sitting in 1-month-old infants: evidence for the innate origin of direction specificity. Exp Brain Res 2004; 157: 10–17.
24. Hedberg A, Carlberg EB, Forssberg H, Hadders-Algra M. Development of postural adjustments in sitting position during the first half year of life. Dev Med Child Neurol 2005; 47: 312–320.
25. Hadders-Algra M, Brogren E, Forssberg H. Ontogeny of postural adjustments during sitting in infancy: variation, selection and modulation. J Physiol 1996; 493 (Pt 1): 273– 288.
26. de Graaf-Peters VB, Bakker H, van Eykern LA, Otten B, Hadders-Algra M. Postural adjustments and reaching in 4- and 6-month-old infants: an EMG and kinematical study.
Exp Brain Res 2007; 181: 647–656.
27. Riccio GE. Information in movement variability about the qualitative dynamics of posture and orientation. In: Newell KM, Corcos DM (eds). Variability and Motor Control. Champagne, IL, USA: Human Kinetics Publishers, 1993, pp. 317–357.
28. Riley MA, Wong S, Mitra S, Turvey MT. Common effects of touch and vision on postural parameters. Exp Brain Res 1997; 117: 165–170.
29. Harbourne RT, Stergiou N. Nonlinear analysis of the development of sitting postural control. Dev Psychobiol 2003; 42: 368–377. 30. Deffeyes JE, Harbourne RT, Kyvelidou A,
Stuberg WA, Stergiou N. Nonlinear analysis of sitting postural sway indicates developmental delay in infants. Clin Biomech (Bristol, Avon)
2009; 24: 564–570.
31. Dusing SC, Kyvelidou A, Mercer VS, Stergiou N. Infants born preterm exhibit different patterns of center-of-pressure movement than infants born at full term. Phys Ther 2009; 89: 1354–1362.
32. Morris C. Definition and classification of cerebral palsy: a historical perspective. Dev Med Child Neurol Suppl 2007; 109: 3–7. 33. Rosenbaum P, Paneth N, Leviton A, Goldstein
M, Bax M, Damiano D, Dan B, Jacobsson B. A report: the definition and classification of cerebral palsy April 2006. Dev Med Child Neurol Suppl 2007; 109: 8–14.
34. Palisano R, Rosenbaum P, Walter S, Russell D, Wood E, Galuppi B. Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child Neurol 1997; 39: 214–223. 35. Hadders-Algra M, Brogren E, Katz-Salamon
M, Forssberg H. Periventricular leucomalacia and preterm birth have different detrimental effects on postural adjustments. Brain J Neurol 1999; 122: 727–740.
36. Brogren E, Forssberg H, Hadders-Algra M. Influence of two different sitting positions on postural adjustments in children with spastic diplegia. Dev Med Child Neurol 2001; 43: 534–546.
37. Washington K, Shumway-Cook A, Price R, Ciol M, Kartin D. Muscle responses to seated perturbations for typically developing infants and those at risk for motor delays. Dev Med Child Neurol 2004; 46: 681–688.
38. Hadders-Algra M, van der Fits IB, Stremmelaar EF, Touwen BC. Development of postural adjustments during reaching in infants with CP. Dev Med Child Neurol 1999; 41: 766–776.
39. Fallang B, Saugstad OD, Hadders-Algra M. Postural adjustments in preterm infants at 4 and 6 months post-term during voluntary reaching in supine position. Pediatr Res 2003; 54: 826–833.
40. Kyvelidou A, Harbourne RT, Willett SL, Stergiou N. Sitting postural control in infants with typical development, motor delay, or cerebral palsy. Pediatr Phys Ther 2013; 25: 46– 51.
41. Deffeyes JE, Harbourne RT, Stuberg WA, Stergiou N. Approximate entropy used to assess sitting postural sway of infants with developmental delay. Infant Behav Dev 2011; 34: 81–99.
42. Kyvelidou A, Harbourne RT, Stergiou N. Severity and characteristics of developmental delay can be assessed using variability measures of sitting posture. Pediatr Phys Ther
2010; 22: 259–266.
43. Bobath K, Bobath B. The neurodevelopmental treatment. In: Scrutton D (ed). Management of the motor disorders of children with cerebral palsy. London: Spastics International Medical Publications, pp. 6–18.
44. Ketelaar M, Vermeer A, Hart H, van Petegem-van Beek E, Helders PJ. Effects of a functional therapy program on motor abilities of children with cerebral palsy. Phys Ther 2001; 81: 1534–1545.
45. Butler C, Darrah J. Effects of neurodevelopmental treatment (NDT) for cerebral palsy: an AACPDM evidence report.
Dev Med Child Neurol 2001; 43: 778–790. 46. Blauw-Hospers CH, Hadders-Algra M. A
systematic review of the effects of early intervention on motor development. Dev Med Child Neurol 2005; 47: 421–432. 47. Blauw-Hospers CH, de Graaf-Peters VB, Dirks
T, Bos AF, Hadders-Algra M. Does early intervention in infants at high risk for a developmental motor disorder improve motor and cognitive development? Neurosci Biobehav Rev 2007; 31: 1201–1212.
48. Bar-Haim S, Harries N, Nammourah I, Oraibi S, Malhees W, et al. Effectiveness of motor learning coaching in children with cerebral palsy: a randomized controlled trial. Clin Rehabil 2010; 24: 1009–1020.
49. Law MC, Darrah J, Pollock N, Wilson B, Russell DJ, Walter SD, Rosenbaum P, Galuppi B. Focus on function: a cluster, randomized controlled trial comparing child- versus context-focused intervention for young children with cerebral palsy. Dev Med Child Neurol 2011; 53: 621– 629.
50. King S, Teplicky R, King G, Rosenbaum P. Family-centered service for children with cerebral palsy and their families: a review of the literature. Semin Pediatr Neurol 2004; 11: 78–86.
51. King G, Chiarello L. Family-centered care for children with cerebral palsy: conceptual and practical considerations to advance care and practice. J Child Neurol 2014; 29: 1046–1054.
52. Dirks T, Blauw-Hospers CH, Hulshof LJ, Hadders-Algra M. Differences between the family-centered ‘COPCA’ program and traditional infant physical therapy based on neurodevelopmental treatment principles.
Phys Ther 2011; 91: 1303–1322.
53. Blauw-Hospers CH, Dirks T, Hulshof LJ, Bos AF, Hadders-Algra M. Pediatric physical therapy in infancy: from nightmare to dream? A two-arm randomized trial. Phys Ther 2011; 91: 1323–1338.
54. Hielkema T, Hamer EG, Reinders-Messelink HA, Maathuis CGB, Bos AF, et al. LEARN 2 MOVE 0-2 years: effects of a new intervention program in infants at very high risk for cerebral palsy; a randomized controlled trial.
BMC Pediatr 2010; 10: 76.
55. Sarnat HB, Sarnat MS. Neonatal encephalopathy following fetal distress. A clinical and electroencephalographic study.
Chapter 2:
Development of postural adjustments
during reaching in typically developing
infants from 4 to 18 months
Lieke C. van Balen Linze Jaap Dijkstra Mijna Hadders-Algra
ABSTRACT
Knowledge on the development of postural adjustments during infancy, in particular on the development of postural muscle coordination, is limited.
This study aimed at the evaluation of the development of postural control during reaching in a supported sitting condition. Eleven typically developing infants participated in the study and were assessed at the ages of 4, 6, 10 and 18 months.
We elicited reaching movements by presenting small toys at an arm’s length distance, whilst activity of multiple arm, neck and trunk muscles was recorded using surface EMG. A model-based computer algorithm was used to detect the onset of phasic muscle activity.
The results indicated that postural muscle activity during reaching whilst sitting supported is highly variable. Direction-specific postural activity was inconsistently present from early age onwards and increased between 10 and 18 months without reaching a 100 % consistency. The dominant pattern of activation at all ages was the ‘complete pattern’, in which all direction-specific muscles were recruited. At 4 months, a slight preference for top-down recruitment existed, which was gradually replaced by a preference for bottom-up recruitment.
We conclude that postural control during the ecological task of reaching during supported sitting between 4 and 18 months of age is primarily characterized by variation. Already from 4 months onwards, infants are - within the variation - sometimes able to select muscle recruitment strategies that are optimal to the task at hand.
INTRODUCTION
In the first 18 months of life, an infant’s motor skills develop at an astounding rate: the child learns to balance the head, to reach and grasp, to sit, to crawl and to walk. It is therefore not surprising that postural control improves rapidly during this period. However, our knowledge on the development of postural control during infancy, in particular on the development of postural muscle coordination, is limited. In general, knowledge on neurobiological substrate and mechanisms underlying motor development is scarce. As a result, various theoretical models are used to explain motor development.
A well-known theoretical framework is the Dynamic Systems Theory (DST).1,2 This
theory considers motor development as a dynamic system in which motor behaviour emerges as a result of a complex interaction between the intrinsic properties of the body, the results of previous experiences and environmental factors. The Neuronal Group Selection Theory (NGST) is an alternative theoretical framework.3 DST and
NGST partially overlap. The two theories share the opinion that motor development is a non-linear process with phases of transition, a process that is affected by many factors. Both theories acknowledge the importance of experience and the relevance of context. But the two theories differ in their opinion on the role of genetically determined neurodevelopmental processes. Genetic factors only play a limited role in DST, whereas in NGST genetic endowment, epigenetic cascades and experience play equally prominent roles.3
According to NGST, typical motor development is characterized by two phases of variability. Development starts with primary variability: the nervous system explores its repertoires of possibilities. The borders of the repertoires are determined by genetic instructions. Exploration of the repertoires results in abundant variation in motor behaviour and in a wealth of self-produced afferent information. During the phase of primary variability, afferent information is not used for the adaptation of motor behaviour to the specifics of the situation. This alters during the phase of secondary variability. During secondary variability, afferent information associated with exploration and trial-and-error experiences is used for the selection of the optimal movement strategy for each situation.3
According to NGST, the consequences of an early lesion of the brain are twofold: (a) a reduction in the size of the repertoire (reduced variation) and (b) a limited ability
to select the best strategy from the repertoire (reduced variability). Here, it is important to note that the word ‘variability’ has been used in different ways in scientific literature. For instance, ‘variability’ has been used to denote variation; following this word use, reduced variability has been considered a sign of dysfunction. Variability has also been used to denote the ability to vary; following this word use, an excess of variation in motor output (also termed excessive variability) has been considered non-optimal behaviour.4,5
In this study, we follow Hadders-Algra3 where variation refers to the size of the
motor repertoire and variability to the ability to vary (i.e. the ability to select different strategies from the motor repertoire in order to adapt motor output to the specifics of the situation). This article aims to study the development of postural control in infancy. Both in adults and children, control of posture has mainly been studied during standing and walking. Knowledge on the early development of postural control, such as during the development of sitting, is limited. Harbourne and Stergiou6 studied postural control in infants just before and after they developed the
ability to sit independently and found that as infants learn to sit, the approximate entropy (a measure of variation) of the sway path of their centre of pressure decreased, indicating that the infants had learned to select those strategies that were optimal for sitting independently. However, centre of pressure data do not furnish information on the strategies used by the nervous system to achieve the various sway paths. Data on muscle recruitment may provide such insight.
Muscle recruitment strategies during postural development
Successful control of body posture is accomplished by activating the proper muscles at the proper time with an optimal contraction strength. Earlier studies into postural muscle activation strategies have revealed several parameters with which the development of postural control can be described.
Direction-specificity
According to Forssberg and Hirschfeld,7 direction-specificity is the first or basic level
of postural control. Direction-specificity means that when equilibrium is threatened by a forward sway of the body, the muscles on the dorsal side of the body are primarily activated in order to maintain balance, and when equilibrium is threatened by a backward sway, the muscles on the ventral side are primarily activated. The
ability to recruit directionally appropriate muscles has been shown to exist already in early infancy: from the age of one month onwards, infants consistently use direction-specific postural adjustments in response to external perturbations of balance.7–10 In
terms of NGST, this suggests that infants are endowed with a direction-specific repertoire of postural adjustments, that is, with variation in direction-specific adjustments.
However, research findings are less clear in case of internally triggered movements, such as reaching. Van der Fits and Hadders-Algra,11 and van der Fits et
al.,12,13 who longitudinally assessed postural adjustments during reaching between 3
and 18 months of age, reported that postural adjustments are direction-specific from the moment that successful reaching movements emerge, which happens around 4– 5 months. A more recent study indicated, however, that only approximately half of the reaching movements at 4 and 6 months are accompanied by direction-specific postural adjustments.14 The difference between the older and more recent data is
explained by the use of a more stringent definition of direction-specificity in the latter: in the older studies of van der Fits et al.,11–13 a trial was classified as
direction-specific when direction-direction-specificity was present at one of the body levels (e.g. neck, trunk or legs) recorded irrespective of the organization of postural activity at other levels of the body. In the recent study of de Graaf-Peters et al.,14 trials were only
considered direction-specific when postural activity at all levels of the body was direction-specific (cf., Hedberg et al.8,9). Using the same stringent definition, van der
Heide et al.15 found that from the age of 2 years onwards children consistently use
direction-specific postural adjustments whilst reaching. The data may imply that at early age the direction-specific networks are present, but not recruited consistently during the early phases of the development of reaching. A question that remains is at which age between 4 months and 2 years reaching movements are consistently accompanied by direction-specificity.
Forssberg and Hirschfeld7 described that the second level of postural control consists
of the ability to adapt direction-specific adjustments to the specifics of the situation. In terms of NGST, the parameters of the second level of control are parameters of variability. Some of the parameters that can be distinguished are:
