Emergence of neuromuscular patterns during walking in toddlers with typical development and with Down syndrome
Introduction
For humans, the process of acquiring functional motor skills is complicated, involving a system of many muscles, joints, and segments that need to be controlled. Yet many skills seem to emerge quite readily, quickly leading to efficient and adaptive use. For scientists, explaining this process is also complicated. But unlike acquiring skills, many years of study have not led to a seamless explanation of how control of functional behavior emerges. For example, researchers have shown that to become highly skilled in some functional tasks, such as playing the piano or tennis requires up to 10 years of dedicated practice (Ericsson et al., 1993, Starkes et al., 1996). And the fact that practice is important to acquiring motor skills such as reaching, writing, or kicking a soccer ball is seldom disputed. Yet, for a subset of skills, ones that some might call innate, autonomic, or life sustaining, such as sucking, breathing, and swallowing, substantial opinion is that the underlying neuromotor coordination is built into the system a priori so that it can “come on line” as soon as needed (Hadders-Algra, 2002, Hadders-Algra et al., 1996). That is to suggest, the timing and coordination of the rhythmic patterns of muscle activations are so important to survival that they have evolved as part of our genetic code, with little, if any, practice needed for function to appear.
Walking is one skill that seems to straddle both the innate and acquired skill perspectives, when it comes to explaining the underlying processes involved. Scientists have detailed many characteristics of this behavior via some quite elegant and creative approaches. Data that contribute to the arguments for innate neural control of walking include the fact that alternation between the legs can be observed in utero (de Vries et al., 1982, Kleven et al., 2004) and alternating leg movements show a predictable developmental trajectory that ebbs and flows over the first year post birth until independent walking emerges around 11 months of age (Thelen & Ulrich, 1991). While alternation seems to emerge quite early as one form of interlimb coordination it is by no means the only or always the dominant interlimb characteristic.
More gait parameters tend to reflect significant change due to practice than to be in place a priori. At walking onset interlimb phase relations average 180° out of phase but 3 months of practice are required to reach the stability of mature walkers (Clark, Whitall, & Phillips, 1988). Similarly, intralimb kinematic patterns and variability changed rapidly over the first months of independent practice (Ivanenko et al., 2005, Looper et al., 2006). Many overt gait parameters show rapid improvements over the first 3 to 4 months after toddlers’ initial precarious steps. Stride lengths increase, step widths decrease, progression velocities increase, and so on (Bril and Brenière, 1992, Chang et al., 2006).
Still, for all the ways in which practice enables toddlers to look more and more like their adult counterparts in terms of kinematic patterns and variability, the system continues to fail frequently. Adolph and colleagues (Joh & Adolph, 2006) report that 14-month-olds toddlers, on average, fall between 0 and 14 times during a brief walk around a city block or in free play. Why, if walking pattern generation is innate and toddlers practice many steps per day leading to dramatic improvements over the first few months, does the system fail, or misstep, so frequently? Perhaps underlying this observable limb coordination behavior is a control system still struggling to settle into a consistent organization of its many options for generating movement through space.
Some motor theorists argue that coordination is not, in fact, what is being learned. Rather, joint patterns, cycle durations, and so on emerge as secondary consequences to learning underlying control strategies that drive the system (Kelso, Holt, Rubin, & Kugler, 1981). Control and coordination emerge as the consequence of interacting subsystems that include the physical properties of the system (body and segment masses, lengths, configurations, tissue characteristics, etc.), passive gravitational and interactive forces, and impulses generated by active muscle bursts. It is to these muscle bursts that we turn here to examine underlying control of early gait more directly. Stable and adaptive control involves muscle synergies that generate the necessary and sufficient amount of and appropriately timed flexor and extensor forces. The degrees of freedom available at the muscle level are enormous; humans have 30 muscles in the thigh and shank segments alone. This complexity allows the discovery of complicated patterns and fine precision but it creates a challenge, as well, to sort out efficient and stable muscle firing patterns, if they are not innate.
In a previous study we compared the muscle activation patterns of infants with typical development (TD) who had 1 month of walking experience with their muscle activity at 4 months, during simple overground walking at their self-selected speed (Chang et al., 2006). We limited our analysis to the four most commonly studied gait muscles and showed that after 1 month of walking experience only one muscle, the gastrocnemius, showed signs of rhythmic muscle bursts. Three months later these same infants showed reduced co-contraction and changes in the dominant combinations of muscles active concurrently. Yet muscle burst patterns remained quite variable; examples of muscle burst patterns that showed adult-like timing appeared among the many variations displayed but did not dominate. Here we expand on this work by starting when toddlers had less experience and finishing with several months more of practice. In addition, we wanted to examine the process of emerging control by comparing the developmental trajectories of toddlers with TD with ones who have Down syndrome (DS). We believe that comparing the development of toddlers with TD and ones with developmental disabilities informs us more acutely of factors that are either innate or emergent via practice. We are easily attracted to assuming that behavior that occurs “normally” is prescribed but when we observe closely and compare the detailed changes to systems with unique constraints we see the potential impact of practice and context in better focus. DS with characteristics of relatively short limbs, lax ligaments, lower muscle strength, and tone (American Academy of Pediatrics & Committee on Genetics, 2001), is a good population for this comparison because there are clear differences (e.g., mechanically, physiologically) and similarities (walk only 1 year later than TD and use this skill over time).
Significant neuromechanical differences can certainly alter gait control and coordination. But, the process of learning a new skill, of discovering how to control the system, involves a similar process of discovery through practice. We do not know the developmental trajectory of underlying muscle activation patterns and their stability over this first year post walking onset. Therefore, our overarching goals for this study were to (a) expand the age range, starting with the very first steps and continuing until 6 months post walking onset and (b) compare the emergence of muscle activity patterns of toddlers with TD to those of toddlers with DS. We predicted that muscle activation patterns for all four muscles examined would be rhythmic and relatively stable in toddlers with TD by 6 months while that of their peers with DS would resolve more slowly and require more practice. We also expected to see group differences in the pattern of change over time and the activation patterns at 6 months, due to inherent biomechanical and neurophysiological subsystem differences.
Section snippets
Participants
Eight toddlers with TD (three females and five males) and eight toddlers with DS (four females and four males) participated in this longitudinal study. We recruited toddlers with TD from the local community and toddlers with DS through flyers distributed to DS support groups as well as notices in their newsletters. We communicated with parents via phone from the time they contacted us, prior to walking onset, until their toddler was able to perform three to six independent steps. At that point
Gait characteristics
Table 2 describes the gait characteristics of each group at four points in time and presents the results of our statistical analyses. Our data show that means for all walking variables in both groups changed significantly over time. More specifically, stride length and velocity increased significantly across time for both groups. Step width, stance and double support phases decreased significantly for both groups over time. The only significant group difference was for step width; toddlers with
Discussion
Our goals for this study were to investigate the emergence of organization of leg muscle activation patterns from walking onset through 6 months of practice and compare group differences in toddlers with TD and those with DS. Because muscle activity happens within a context and underlies the control of body motion it seems useful to review first the kinematics and end-point effector data. In fact, the gait characteristics (end-point effector data) of our samples paralleled those reported
Acknowledgements
We thank Allison McIntyre for assisting in data collection and data reduction. We also thank all of the participants and their families for their commitment to this study. This study was supported by NIH grant R01 HD42728-01 awarded to B. Ulrich.
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