Motor variability is a fundamental feature of developing systems allowing motor exploration and learning. In human infants, leg movements involve a small number of basic coordination patterns called locomotor primitives, but whether and when motor variability could emerge from these primitives remains unknown. Here we longitudinally followed 18 infants on 2-3 time points between birth (~4 days old) and walking onset (~14 months old) and recorded the activity of their leg muscles during locomotor or rhythmic movements. Using unsupervised machine learning, we show that the structure of trial-to-trial variability changes during early development. In the neonatal period, infants own a minimal number of motor primitives but generate a maximal motor variability across trials thanks to variable activations of these primitives. A few months later, toddlers generate significantly less variability despite the existence of more primitives due to more regularity within their activation. These results suggest that human neonates initiate motor exploration as soon as birth by variably activating a few basic locomotor primitives that later fraction and become more consistently activated by the motor system.
Keywords: human; infancy; locomotor development; modularity; motor primitives; muscle synergies; neuroscience; trial-to-trial variability.
Human babies start to walk on their own when they are about one year old, but before that, they can move their legs to produce movements called ‘stepping’, where they take steps when held over a surface; and kicking, where they kick in the air when lying on their backs. These two behaviors are known as ‘locomotor precursors’ and can be observed from birth. Previous studies suggest that infants produce these movements by activating a small number of motor primitives, different modules in the nervous system – each activating a combination of muscles to produce a movement. However, babies and toddlers exhibit a lot of variability when they move, which is a hallmark of typical development that furthers exploring and learning. So far, it has been unclear whether such differences arise as soon as babies are born and if so, how a small number of motor primitives could result in this variability. Hinnekens et al. hypothesized that the great variety of movements in infants can be generated from a small set of motor primitives, when several cycles of flexing and extending the legs are considered. To test their hypothesis, the researchers first needed to establish how and when infants generate this variability of movement. To do so, they used electromyography to record the leg muscle activity of 18 babies during either movement resulting in a body displacement (locomotor movement) or rhythmic movement. These measurements were taken at either two or three timepoints between birth and the onset of walking. Next, the scientists used a state-of-the-art machine learning approach to model the neural basis underlying these recordings, which showed that newborns generate a lot of movement variability, but they do so by activating a small number of motor primitives, which they can combine in different ways. Hinnekens et al. also show that as babies get older, the number of motor primitives increases while the variety of movements decreases due to a more steady activation of each motor primitive. Cerebral plasticity is maximal during the first year of life, and infants can regularly learn new motor skills, each leading to the ability to perform more movements. Motor variability is believed to play an important role in this learning process and is known to be decreased in atypical development. As such, examining motor variability may be a promising tool to identify neurodevelopmental delays at younger ages.
© 2023, Hinnekens et al.