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; Thelen and Smith 1994; Adolph and Robinson 2008). 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, Hadders-Algra 2010) is an alternative theoretical framework. 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 (Hadders-Algra 2010). 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 (Hadders-Algra 2010). 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; Hadders-Algra 2010). 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 (Harbourne and Stergiou 2009; Dusing and Harbourne 2010). In this study, we follow Hadders-Algra (2010) 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 Stergiou (2003) 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.
According to Forssberg and Hirschfeld (1994), 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 (Forssberg and Hirschfeld 1994; Hedberg et al. 2004, 2005; Washington et al. 2004). 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 (1998) and Van der Fits et al. (1999a, b), 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 (De Graaf-Peters et al. 2007). 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., a trial was classified as direction-specific when 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., trials were only considered direction-specific when postural activity at all levels of the body was direction-specific (cf., Hedberg et al. 2004, 2005). Using the same stringent definition, Van der Heide et al. (2003) 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 Hirschfeld (1994) 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:
One way to adapt postural adjustments is the selection of particular direction-specific muscles or a particular combination of direction-specific muscles. The study of De Graaf-Peters et al. (2007) indicated that at 4 months the number of direction-specific muscles that are recruited is highly variable. Already at 6 months, some selection occurs: the ‘complete pattern’, that is, the pattern in which all recorded direction-specific muscles are recruited, becomes a more prominent pattern. It also has been shown that the complete pattern is the dominant pattern whilst reaching in a sitting position during the second postnatal year (Van der Heide et al. 2003; Hadders-Algra 2008). This preference for the complete pattern in early infancy may be related to the difficulty of the balance problem that is encountered, as this preference disappears after the second year, when infants have mastered walking (Hadders-Algra 2008).
Our knowledge on the development of the recruitment order of direction-specific muscles during infancy is limited. Variation appears to be the major characteristic of recruitment order at early age. Varied recruitment is evident at 4 months of age. At 6 months, infants who sit supported show a mild preference for top-down recruitment (De Graaf-Peters et al. 2007). However, independently sitting 8- to 10-month-old infants demonstrate a slight preference for bottom-up recruitment (Hadders-Algra et al. 1996a, b; Van der Fits et al. 1999b). Longitudinal data on the development of the recruitment order of direction-specific muscles in supported sitting are lacking. Recruitment order of postural muscles in independently sitting children beyond the age of 10 months is mainly characterized by variation (Van der Heide et al. 2003).
In EMG-studies of postural control during reaching, anticipatory postural activity has been defined as the occurrence of activity in postural muscles prior to the activation of the first arm muscle that initiates the reaching movement (the ‘prime mover’). Anticipatory muscle activation is a form of postural fine-tuning that heavily relies on feed-forward processing (Massion 1992). The studies of Van der Fits and Hadders-Algra (1998), Van der Fits et al. (1999a, b) indicated that, from 15 months onwards, infants show a significant increase in the use of anticipatory postural activity during reaching whilst sitting.
One of the challenges of studying postural control in an ecological setting is that the task-related activation in the EMG signal is more or less ‘hidden’ in the noise of other movements. Previous studies using the ecological design of reaching movements to study postural control (Van der Fits et al. 1999a, b; De Graaf-Peters et al. 2007) used a separate video analysis to indicate the approximate time of the start of the reaching movement in the EMG signal, combined with a fixed detection level threshold (compared with a long-term mean baseline activity) to identify task-related activation. The latter implied that spontaneous activity prior to the reaching movement had a relatively large impact on whether or not reaching-related postural EMG-activity could be detected in the window of analysis. In order to improve the accuracy of data analysis, we developed a software program (PedEMG). PedEMG has two advantages. Firstly, it integrates video and EMG analysis. The simultaneous view of infant behaviour and EMG signals allows for a better selection of trials that are not affected by simultaneously occurring additional activities. Secondly, the program does not use a fixed-threshold algorithm for onset detection, but a dynamic threshold statistical algorithm as the latter performs better in noisy signals than the former (Staude and Wolf 1999).
The aim of this study is to increase our understanding of postural development in the ecological situation of reaching during supported sitting between 4 and 18 months. To this end, we carried out a longitudinal study with eleven typically developing infants who were assessed at 4, 6, 10 and 18 months in which the novel program PedEMG was applied. We opted to study the infants at specific ages instead of at specific functional levels. Either option has advantages and disadvantages, which are related to the fact that development is the net result of the continuous interaction between genetic endowment and external influences, including experience. We chose the age approach as previous studies indicated that the relationships between functional achievements such as ‘being able to sit without help’ and parameters of postural control are only weakly associated (Hadders-Algra et al. 1996a; Van der Fits et al. 1999b). In addition, we aim to continue our research with infants at high risk of developmental disorders. In general, clinical follow-up of high-risk infants involved assessment at specific ages and not at specific abilities. We did, however, include the development of motor milestones in our assessments in order to explore possible associations between functional motor development and the development of postural control.
We addressed the following questions: (1) At what age do infants consistently show direction-specific postural adjustments when reaching? (2) Can we replicate the finding of an increased selection of the complete pattern with increasing age similar to that occurring during external perturbations in a sitting position (Hedberg et al. 2005)? (3) Does recruitment order of the direction-specific muscles during reaching whilst sitting supported change with increasing age, that is, do infants develop a preference for top-down (cf. De Graaf-Peters et al. 2007) or bottom-up recruitment (Van der Fits et al. 1999b; Van der Heide et al. 2003), or is recruitment primarily characterized by variation? (4) Do infants between 4 and 18 months of age exhibit anticipatory postural activity when reaching? (5) Are the postural control parameters mentioned above (i.e. direction specificity, presence of the complete pattern, recruitment order and anticipatory activation) associated with the achievement of milestones in sitting and grasping behaviour?