Evidence of tactile arm stepping in newborns and its responsiveness to optic flows specifying self-translation.

Although the arms participate in many forms of human locomotion, we know very little about when arm movements emerge during locomotor development. Here we investigated whether newborns would make tactile arm stepping movements when we supported them almost horizontally so their hands touched a surface and blocked their leg movements. Building off prior work showing that newborns make more crawling and air stepping leg movements when exposed to optic flows specifying forward and backward self-translation, we also examined whether newborns would make more tactile arm steps when exposed to forward and backward optic flows compared to a random optic flow that did not specify translation. We found that newborns can perform arm stepping and produce a significantly higher number of tactile arm steps in the optic flow condition specifying backward translation than in the random optic flow condition. Both translating optic flow conditions had significantly higher numbers of alternating arm steps than the random optic flow condition. These findings show that tactile arm stepping exists at birth and that optic flows can facilitate their production, similar to leg stepping. We argue that these results further support the idea that a quadrupedal organization underlies early upright stepping.

Generating variability from motor primitives during infant locomotor development.

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.

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.

Stimulating the motor development of very premature infants: effects of early crawling training on a mini-skateboard.

Aim: To examine the effects of an early home-based 8-week crawling intervention performed by trained therapists on the motor and general development of very premature infants during the first year of life. Methods: At term-equivalent age, immediately following discharge from the Neonatal Intensive Care Unit (NICU), we randomly allocated 44 premature infants born before 32 weeks' gestation without major brain damage to one of three conditions in our intervention study: crawling on a mini-skateboard, the Crawliskate (Crawli), prone positioning control (Mattress), or standard care (Control). The Crawli and Mattress groups received 5 min daily at-home training administered by trained therapists for 8 consecutive weeks upon discharge from the NICU. The outcomes of greatest interest included gross motor development (Bayley-III) at 2, 6, 9, and 12 months (primary outcome) corrected age (CA), mature crawling at 9 months CA and general development at 9 and 12 months CA [Ages and Stages Questionnaires-3 (ASQ-3)]. The study was registered at www.clinicaltrials.gov; registration number: NCT05278286. Results: A 3 (Condition) × 4 (Age) repeated measures ANOVA revealed that Crawli group infants had significantly higher Bayley-III gross motor development scores than Mattress and Control group infants. Crawli group infants also scored significantly higher on groups of Bayley-III items related to specific motor skills than infants in the other groups, including crawling at 9 months CA. We found significant differences in favor of the Crawli group in separate one-way ANOVAs at each of the ages we examined. A 3 (Condition) × 2 (Age) repeated measures ANOVA revealed that the Crawli group scored significantly higher than the Control group for the ASQ-3 total score and communication score and significantly higher for the fine motor score than the Control and Mattress groups. We found additional significant differences in favor of the Crawli group for other dimensions of the ASQ-3 in separate one-way ANOVAs at 9 and 12 months CA. Interpretation: Early crawling training on a Crawliskate provides an effective way to promote motor and general development in very premature infants. The findings also provide clear evidence for a link between newborn crawling and more mature crawling later in development.

Newborns modulate their crawling in response to their native language but not another language.

Human newborns can propel themselves to their mother's breast when positioned skin to skin on her abdomen just after birth. For decades, researchers have considered this primitive crawling behavior a spinal reflex, immune to supra spinal control. However, recent research suggests that neonatal crawling is already responsive to visual and olfactory stimuli processed at a supra spinal level. Here we report that a few hours post birth, French newborns can also modulate their crawling in response to their native language - a source of information that is processed supra-spinally. The crawling patterns of 23 French-born newborns were recorded on video and via an infrared motion capture system during two randomly ordered 2-min trials. The newborns were secured on a mini skateboard to facilitate arm and leg movements during their crawling propulsion. They heard a repetitive sequence of the same sentences either in French, their native language, or in English, a rhythmically different and hence discriminable unfamiliar language, on each trial. In French, compared to English, crawling was enhanced, with significantly more arm and leg steps and significantly more and larger trunk rotations in the cephalo-caudal axis. Moreover, newborns rotated their heads and trunk toward the appropriate loud speaker when hearing French but not English. These preliminary findings suggest that newborn crawling is not a simple stereotyped reflex under spinal control, but a complex pattern that can be modulated in response to higher-order, supra-spinally processed stimuli. The findings open fascinating questions about the range of stimuli to which newborn crawling is responsive.

Optimization of modularity during development to simplify walking control across multiple steps.

Introduction: Walking in adults relies on a small number of modules, reducing the number of degrees of freedom that needs to be regulated by the central nervous system (CNS). While walking in toddlers seems to also involve a small number of modules when considering averaged or single-step data, toddlers produce a high amount of variability across strides, and the extent to which this variability interacts with modularity remains unclear. Methods: Electromyographic activity from 10 bilateral lower limb muscles was recorded in both adults (n = 12) and toddlers (n = 12) over 8 gait cycles. Toddlers were recorded while walking independently and while being supported by an adult. This condition was implemented to assess if motor variability persisted with reduced balance constraints, suggesting a potential central origin rather than reliance on peripheral regulations. We used non-negative matrix factorization to model the underlying modular command with the Space-by-Time Decomposition method, with or without averaging data, and compared the modular organization of toddlers and adults during multiple walking strides. Results: Toddlers were more variable in both conditions (i.e. independent walking and supported by an adult) and required significantly more modules to account for their greater stride-by-stride variability. Activations of these modules varied more across strides and were less parsimonious compared to adults, even with diminished balance constraints. Discussion: The findings suggest that modular control of locomotion evolves between toddlerhood and adulthood as the organism develops and practices. Adults seem to be able to generate several strides of walking with less modules than toddlers. The persistence of variability in toddlers when balance constraints were lowered suggests a link with the ability to explore rather than with corrective mechanisms. In conclusion, the capacity of new walkers to flexibly activate their motor command suggests a broader range of possible actions, though distinguishing between modular and non-modular inputs remains challenging.

Effects of Early Motor Interventions on Gross Motor and Locomotor Development for Infants at-Risk of Motor Delay: A Systematic Review.

Aim: To systematically examine the effect of early motor interventions on motor and locomotor development in infants <1 year of age with motor developmental disability or at risk of motor delay. Methods: Pertinent literature from January 2000 to September 2021 was identified by searching the PubMed, Embase, Cochrane, Pedro and Web of Science databases. Selection criteria included interventions starting before 12 months corrected age. Methodological quality was assessed with AACPDM criteria, Mallen score and Cochrane risk of bias methodology. Evaluation procedure was performed using PRISMA protocol (PICO approach) and AMSTAR-2. This review was preregistered in PROSPERO (CRD42021286445). Results: Ten articles met the inclusion criteria; seven had moderate to strong methodological quality. The interventions included treadmill training (n = 3), crawling training (n = 1), "tummy time" (n = 1), physical therapy with neonatal developmental program (n = 1) or Bobath approach (n = 1), treadmill training combined with active leg movements (n = 2) or Bobath physiotherapy (n = 1). The three key characteristics of effective interventions that emerged from the review were: (1) the infants' disability or risk of delay was well-defined; (2) the protocol was standardized and easy to replicate; (3) infants were required to make active movements. Conclusion: There is an urgent need for additional high-quality studies on the effects of early motor interventions on the gross motor and locomotor development of infants with a range of disabilities or risks for delay. Suggestions for future research are outlined.

Can Optic Flow Further Stimulate Treadmill-Elicited Stepping in Newborns?

Typically developing 3-day-old newborns take significantly more forward steps on a moving treadmill belt than on a static belt. The current experiment examined whether projecting optic flows that specified forward motion onto the moving treadmill surface (black dots moving on the white treadmill surface) would further enhance forward stepping. Twenty newborns were supported on a moving treadmill without optic flow (No OF), with optic flow matching the treadmill's direction and speed (Congruent), with optic flow in the same direction but at a faster speed (Faster), and in a control condition with an incoherent optic flow moving at the same speed as in the Congruent condition but in random directions (Random). The results revealed no significant differences in the number or coordination of forward treadmill steps taken in each condition. However, the Faster condition generated significantly fewer leg pumping movements than the Random control condition. When highly aroused, newborns made significantly fewer single steps and significantly more parallel steps and pumping movements. We speculate the null findings may be a function of the high friction material that covered the treadmill surface.

Newborn crawling and rooting in response to maternal breast odor.

A growing literature shows that perception and action are already tightly coupled in the newborn. The current study aimed to examine the nature of the coupling between olfactory stimuli from the mother and the newborn's crawling and rooting (exploratory movements of the head). To examine the coupling, the crawling and rooting behavior of 28 2-day-old newborns were studied while they were supported prone on a mobility device shaped like a mini skateboard, the Crawliskate®, their head positioned directly on top of a pad infused with either their mother's breast odor (Maternal) or the odor of water (Control). Video and 3D kinematic analyses of the number and types of limb movements and quantification of displacement across the surface revealed that newborns are significantly more efficient crawlers when they smell the maternal odor, moving greater distances although performing fewer locomotor movements. In addition, the newborns made significantly more head rooting movements in the presence of the maternal odor. These findings suggest that the circuitry underlying quadrupedal locomotion and exploratory movements of the head is already adaptable to olfactory information via higher brain processing. Moreover, the coupling between olfaction and the two action systems, locomotion and rooting, is already differentiated. As crawling enables the newborn to move toward the mother's breast immediately after birth and facilitates mother-infant interaction, the results of this study highlight the potential value of using maternal odors to stimulate mobility in infants at risk of motor delay and/or deprived of this odor when born prematurely.

What Does Prone Skateboarding in the Newborn Tell Us About the Ontogeny of Human Locomotion?

The crawling behavior of sixty 2-day-old newborns was studied while they were supported prone on a mini skateboard and on a pediatric mattress without additional support. Analyses of the number and types of limb movements and their characteristics, the coactivation of limb pairs, and the displacement across the surface, revealed that newborns can crawl with locomotor patterns similar to those documented during quadrupedal locomotion in animals and human adults. This was particularly apparent on the skateboard. This discovery suggests that locomotor circuitry underlying quadrupedal locomotion develops during fetal life. Drawing upon other evidence for a quadrupedal organization underlying bipedal gait, we argue that early quadrupedal training may enhance interventions designed to hasten the onset of independent walking.

Effect of optic flows on newborn crawling.

This study examined the crawling characteristics of newborns placed prone on a water-filled, transparent pediatric mattress and whether exposure to terrestrial optic flows that specify forward and backward displacement would influence leg and arm crawling movements. Twenty-six 3-day-old newborns were exposed to a static checkerboard pattern that was back-projected onto the surface underneath the mattress or a checkerboard pattern that moved toward or away from them at 0.12 m/s. Significantly more flexion and extension crawling movements of the legs were observed in the optic flow conditions, although infants did not displace their bodies significantly further on the mattress in these conditions. Unique aspects of newborn crawling were also identified.

Effects of support surface and optic flow on step-like movements in pre-crawling and crawling infants.

Step-like movements were examined in pre-crawling (n=9) and crawling (n=9) 6-13 month-old infants in the air and on a surface in response to a static pattern or optic flows that moved toward or away from the infant. Infants completed six 60-s trials. A significant interaction between locomotor status and support condition revealed that pre-crawling infants made more step-like movements in the air than on a rigid surface. In contrast, crawling infants made an equivalent number of step-like movements in the air and on the surface. Optic flow did not influence the number of step-like movements made by infants. The pre-crawling infant finding is consistent with a finding in a previous study in which two month-old infants were shown to step more in the air than on the ground. This finding is discussed relative to the idea that the infant stepping pattern disappears because the legs become too heavy to lift.

Infant manual performance during reaching and grasping for objects moving in depth.

Few studies have investigated manual performance in infants when reaching and grasping for objects moving in directions other than across the fronto-parallel plane. The present preliminary study explored object-oriented behavioral strategies and side preference in 8- and 10-month-old infants during reaching and grasping for objects approaching in depth from three positions (midline, and 27° diagonally from the left and right). Effects of task constraint by using objects of three different types and two sizes were further examined for behavioral strategies and hand opening prior to grasping. Additionally, assessments of hand preference by a dedicated handedness test were performed. Regardless of object starting position, the 8-month-old infants predominantly displayed right-handed reaches for objects approaching in depth. In contrast, the older infants showed more varied strategies and performed more ipsilateral reaches in correspondence with the side of the approaching object. Conversely, 10-month-old infants were more successful than the younger infants in grasping the objects, independent of object starting position. The findings regarding infant hand use strategies when reaching and grasping for objects moving in depth are similar to those from earlier studies using objects moving along a horizontal path. Still, initiation times of reaching onset were generally long in the present study, indicating that the object motion paths seemingly affected how the infants perceived the intrinsic properties and spatial locations of the objects, possibly with an effect on motor planning. Findings are further discussed in relation to future investigations of infant reaching and grasping for objects approaching in depth.

Treadmill stimulation improves newborn stepping.

To shed further light on infant stepping, we investigated whether newborns could step on a treadmill and adapt their steps to graded velocities. Twenty-one newborns (mean = 3 days) were supported for 60 s trials on a treadmill that was static or moved at 13.4, 17.2, or 23.4 cm/s. Video analysis revealed that newborns made more real steps than in-place "pumps" on the moving treadmill than on the static treadmill and made more real steps at 17.2 than 23.4 cm/s. While the treadmill had no effect on arousal, stepping increased and showed higher quality and coordination across conditions when infants were crying. These findings suggest that treadmill interventions currently used to promote the development of independent locomotion in infants at risk of delay could begin at birth. Further investigation is needed to establish the optimal conditions for newborn treadmill stepping and to specify how arousal affects step rate, quality, and coordination.

Why does infant stepping disappear and can it be stimulated by optic flow?

Two independent experiments (n = 22 and n = 22) showed that 2-month-old infants displayed significantly more stepping movements when supported upright in the air than when supported with their feet contacting a surface. Air- and surface-stepping kinematics were quite similar (Experiment 2). In addition, when data were collapsed across both experiments, more air steps and more donkey kicks were seen when infants were exposed to optic flows that specified backward compared to forward translation. The findings challenge the currently accepted heavy legs explanation for the disappearance of stepping at 2 months of age and raise new questions about the visual control of stepping.

Rhythm perception, production, and synchronization during the perinatal period.

Sensori-motor synchronization (SMS) is the coordination of rhythmic movement with an external rhythm. It plays a central role in motor, cognitive, and social behavior. SMS is commonly studied in adults and in children from four years of age onward. Prior to this age, the ability has rarely been investigated due to a lack of available methods. The present paper reviews what is known about SMS in young children, infants, newborns, and fetuses. The review highlights fetal and infant perception of rhythm and cross modal perception of rhythm, fetal, and infant production of rhythm and cross modal production of rhythm, and the contexts in which production of rhythm can be observed in infants. A primary question is whether infants, even newborns, can modify their spontaneous rhythmical motor behavior in response to external rhythmical stimulation. Spontaneous sucking, crying, and leg movements have been studied in the presence or absence of rhythmical auditory stimulation. Findings suggest that the interaction between movement and sound is present at birth and that SMS can be observed in special conditions and within a narrow range of tempi, particularly near the infant's own spontaneous motor tempo. The discussion centers on the fundamental role of SMS in interaction and communication at the beginning of life.

Air stepping in response to optic flows that move Toward and Away from the neonate.

To shed further light on the perceptual regulation of newborn stepping, we compared neonatal air stepping in response to optic flows simulating forward or backward displacement with stepping forward on a surface. Twenty-two 3-day-olds performed four 60 s trials in which they stepped forward on a table (Tactile) or in the air in response to a pattern that moved toward (Toward) or away (Away) from them or was static (Static). Significantly more steps were taken in the Tactile and Toward conditions than the Static condition. The Away condition was intermediate to the other conditions. The knee joint activity across the entire trial was significantly greater in the Toward than the Away condition. Within-limb kinematics and between-limb coordination were very similar for steps taken in the air and on the table, particularly in the Toward and Tactile conditions. These findings highlight that visual and tactile stimulation can equally elicit neonatal stepping.

The role of locomotion in psychological development.

The psychological revolution that follows the onset of independent locomotion in the latter half of the infant's first year provides one of the best illustrations of the intimate connection between action and psychological processes. In this paper, we document some of the dramatic changes in perception-action coupling, spatial cognition, memory, and social and emotional development that follow the acquisition of independent locomotion. We highlight the range of converging research operations that have been used to examine the relation between locomotor experience and psychological development, and we describe recent attempts to uncover the processes that underlie this relation. Finally, we address three important questions about the relation that have received scant attention in the research literature. These questions include: (1) What changes in the brain occur when infants acquire experience with locomotion? (2) What role does locomotion play in the maintenance of psychological function? (3) What implications do motor disabilities have for psychological development? Seeking the answers to these questions can provide rich insights into the relation between action and psychological processes and the general processes that underlie human development.

The epigenesis of wariness of heights.

Human infants with little or no crawling experience surprisingly show no wariness of heights, but such wariness becomes exceptionally strong over the life span. Neither depth perception nor falling experiences explain this extraordinary developmental shift; however, something about locomotor experience does. The crucial component of locomotor experience in this emotional change is developments in visual proprioception-the optically based perception of self-movement. Precrawling infants randomly assigned to drive a powered mobility device showed significantly greater visual proprioception, and significantly greater wariness of heights, than did controls. More important, visual proprioception mediated the relation between wariness of heights and locomotor experience. In a separate study, crawling infants' visual proprioception predicted whether they would descend onto the deep side of a visual cliff, a finding that confirms the importance of visual proprioception in the development of wariness of heights.

Neonatal stepping in relation to terrestrial optic flow.

This experiment examined whether newborn stepping, a primitive form of bipedal locomotion, could be modulated by optical flow. Forty-eight 3-day-old infants were exposed to optical flows that were projected onto a horizontal surface above which the infants were suspended. Significantly more air steps were elicited by exposure to a terrestrial optical flow specifying forward translation than by a rotating optical flow or a static optical pattern. Thus, a rudimentary coupling between optical flow and stepping is present at birth, suggesting a precocious capacity in the newborn to perceive and utilize visual information specifying self-motion. The findings may help the early diagnosis of infants with visual or visual-motor deficits and the development of visually based interventions for disabled infants.