Pitfall or pratfall? Behavioral differences in infant learning from falling.

Researchers routinely infer learning and other unobservable psychological functions based on observable behavior. But what behavioral changes constitute evidence of learning? The standard approach is to infer learning based on a single behavior across individuals, including assumptions about the direction and magnitude of change (e.g., everyone should avoid falling repeatedly on a treacherous obstacle). Here we illustrate the benefits of an alternative "multiexpression, relativist, agnostic, individualized" approach. We assessed infant learning from falling based on multiple behaviors relative to each individual's baseline, agnostic about the direction and magnitude of behavioral change. We tested infants longitudinally (10.5-15 months of age) over the transition from crawling to walking. At each session, infants were repeatedly encouraged to crawl or walk over a fall-inducing foam pit interspersed with no-fall baseline trials on a rigid platform. Our approach revealed two learning profiles. Like adults in previous work, "pit-avoid" infants consistently avoided falling. In contrast, "pit-go" infants fell repeatedly across trials and sessions. However, individualized comparisons to baseline across multiple locomotor, exploratory, and social-emotional behaviors showed that pit-go infants also learned at every session. But they treated falling as an unimpactful "pratfall" rather than an aversive "pitfall." Pit-avoid infants displayed enhanced learning across sessions and partial transfer of learning from crawling to walking, whereas pit-go infants displayed neither. Thus, reliance on a predetermined, "one-size-fits-all" behavioral expression of a psychological function can obscure different behavioral profiles and lead to erroneous inferences. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Gahvora cradling in Tajikistan: Cultural practices and associations with motor development.

In Tajikistan, infants are bound supine in a "gahvora" cradle that severely restricts movement. Does cradling affect motor development and body growth? In three studies (2013-2018), we investigated associations between time in the gahvora (within days and across age) and motor skills and flattened head dimensions in 8-24-month-old Tajik infants (N = 269, 133 girls, 136 boys)) and 4.3-5.1-year-old children (N = 91, 53 girls, 38 boys). Infants had later motor onset ages relative to World Health Organization standards and pronounced brachycephaly; cradling predicted walk onset age and the proficiency of sitting, crawling, and walking. By 4-5 years, children's motor skills were comparable with US norms. Cultural differences in early experiences offer a unique lens onto developmental processes and equifinality in development.

Use it or lose it? Effects of age, experience, and disuse on crawling.

What happens to early acquired but later abandoned motor skills? To investigate effects of disuse on early-developing motor skills, we examined crawling in two groups of habitual crawlers (34 6-12-month-old infants and five adults with Uner Tan Syndrome) and two groups of rusty crawlers (27 11-12-year-old children and 13 college-aged adults). Habitual crawlers showed striking similarities in gait patterns, limbs supporting the body, and crawling speed, despite dramatic differences in crawling practice, posture, and body size. Habitual crawlers trotted predominantly, whereas rusty crawlers showed a variety of gait patterns. Within sequences, habitual crawlers and children showed more switches in gait patterns than young adults. Children crawled faster and kept fewer limbs on the grounds than the other groups. Old crawling patterns were retained despite disuse, but new ones were also added. Surprisingly, results indicate that nothing was lost with disuse, but some features of crawling were gained or altered.

Responsiveness of rat fetuses to sibling motor activity: Communication in utero?

Previous research has revealed that fetuses detect and respond to extrauterine stimuli such as maternal movement and speech, but little attention has been cast on how fetuses may directly influence and respond to each other in the womb. This study investigated whether motor activity of E20 rat fetuses influenced the behavior of siblings in utero. Three experiments showed that; (a) contiguous siblings expressed a higher frequency of synchronized movement than noncontiguous siblings; (b) fetuses that lay between two siblings immobilized with curare showed less movement relative to fetuses between saline or uninjected controls; and (c) fetuses between two siblings behaviorally activated by the opioid agonist U50,488 also showed less activity and specific behavioral changes compared to controls. Our findings suggest that rat fetuses are directly impacted by sibling motor activity, and thus that a rudimentary form of communication between siblings may influence the development of fetuses in utero.

Bouts of steps: The organization of infant exploration.

Adults primarily walk to reach a new location, but why do infants walk? Do infants, like adults, walk to travel to a distant goal? We observed 30 13-month-old and 30 19-month-old infants during natural walking in a laboratory playroom. We characterized the bout structure of walking-when infants start and stop walking-to examine why infants start and stop walking. Locomotor activity was composed largely of brief spurts of walking. Half of 13-month-olds' bouts and 41% of 19-month-olds' bouts consisted of three or fewer steps-too few to carry infants to a distant goal. Most bouts ended in the middle of the floor, not at a recognizable goal. Survival analyses of the distribution of steps per bout indicated that the probability of continuing to walk was independent of the length of the ongoing bout; infants were just as likely to stop walking after five steps as after 50 steps and they showed no bias toward bouts long enough to carry them across the room to a goal. However, 13-month-olds showed an increased probability of stopping after 1-3 steps, and they did not initiate walking more frequently to compensate for their surfeit of short bouts. We propose that infants' natural walking is not intentionally directed at distant goals; rather, it is a stochastic process that serves exploratory functions. Relations between the bout structure of walking and other measures of walking suggest that locomotor exploration is constrained by walking skill in younger infants, but not in older infants.

Spinal mediation of motor learning and memory in the rat fetus.

Fetal rats can alter patterns of interlimb coordination after experience with a yoke that links two legs together. Yoke training results in a pronounced increase in conjugate limb movements (CLM). To determine whether yoke motor learning is mediated by spinal cord circuitry, fetal subjects at embryonic Day 20 (E20) received yoke training after mid-thoracic spinal cord transection or sham surgery. Both spinal and sham-treated fetuses exhibited an increase in CLM during training. In a second experiment, fetuses received initial yoke training, then were transected or sham treated before a 2nd training. Spinal and sham fetuses that were yoked during both training sessions exhibited a more rapid rise in CLM than those yoked only in the later session. These findings indicate that motor learning in fetal rats can be supported by spinal cord circuitry alone, and that savings implies a form of motor memory localized in the spinal cord.

A new twist on old ideas: how sitting reorients crawlers.

Traditionally, crawling and sitting are considered distinct motor behaviors with different postures and functions. Ten- to 12-month-old infants were observed in the laboratory or in their homes while being coaxed to crawl continuously over long, straight walkways (Study 1; N = 20) and during spontaneous crawling during free play (Study 2; N = 20). In every context, infants stopped crawling to sit 3-6 times per minute. Transitions from crawling to sitting frequently turned infants' bodies away from the direction of heading; subsequent transitions back to crawling were offset by as much as 180° from the original direction of heading. Apparently, body reorientations result from the biomechanics of transitioning between crawling and sitting. Findings indicate that sustained, linear crawling is likely an epiphenomenon of how gait is studied in standard paradigms. Postural transitions between crawling and sitting are ubiquitous and can represent a functional unit of action. These transitions and the accompanying body reorientations likely have cascading effects for infants' exploration, visual perception, and spatial cognition.

Human quadrupeds, primate quadrupedalism, and Uner Tan Syndrome.

Since 2005, an extensive literature documents individuals from several families afflicted with "Uner Tan Syndrome (UTS)," a condition that in its most extreme form is characterized by cerebellar hypoplasia, loss of balance and coordination, impaired cognitive abilities, and habitual quadrupedal gait on hands and feet. Some researchers have interpreted habitual use of quadrupedalism by these individuals from an evolutionary perspective, suggesting that it represents an atavistic expression of our quadrupedal primate ancestry or "devolution." In support of this idea, individuals with "UTS" are said to use diagonal sequence quadrupedalism, a type of quadrupedal gait that distinguishes primates from most other mammals. Although the use of primate-like quadrupedal gait in humans would not be sufficient to support the conclusion of evolutionary "reversal," no quantitative gait analyses were presented to support this claim. Using standard gait analysis of 518 quadrupedal strides from video sequences of individuals with "UTS", we found that these humans almost exclusively used lateral sequence-not diagonal sequence-quadrupedal gaits. The quadrupedal gait of these individuals has therefore been erroneously described as primate-like, further weakening the "devolution" hypothesis. In fact, the quadrupedalism exhibited by individuals with UTS resembles that of healthy adult humans asked to walk quadrupedally in an experimental setting. We conclude that quadrupedalism in healthy adults or those with a physical disability can be explained using biomechanical principles rather than evolutionary assumptions.

Odor-induced crawling locomotion in the newborn rat: Effects of amniotic fluid and milk.

Early locomotion in the neonatal rat previously has been reported 3 days after birth during exposure to an odor of biological relevance (nest material). The current study explores if other ecologically relevant stimuli-amniotic fluid (AF) and milk-could evoke a similar locomotor response in the newborn rat and whether the endogenous opioid system mediates the response. Newborn rats tested 24 hr after birth were presented with the odors of AF or milk while placed in a runway. Pups expressed crawling and moved along the runway in response to direct exposure to the odors of AF and milk (Exp. 1). However, there was no evidence that this crawling response was altered after pretreatment with the opioid antagonist naloxone (Exp. 2). This study provides evidence of the capacity of AF and milk to evoke coordinated motor behavior, suggesting that they may play a role in the development of fundamental motor patterns.

Sensory feedback alters spontaneous limb movements in newborn rats: effects of unilateral forelimb weighting.

Perinatal mammals show spontaneous movements that often appear random and uncoordinated. Here, we examined if spontaneous limb movements are responsive to a proprioceptive manipulation by applying a weight unilaterally to a forelimb of postnatal day 0 (P0; day of birth) and P1 rats. Weights were calibrated to approximate 0%, 25%, 50%, or 100% of the average mass of a forelimb, and were attached at the wrist. P0 and P1 pups showed different levels of activity during the period of limb weighting, in response to weight removal, and during the period after weighting. Pups exposed to 50% and 100% weights showed proportionately more activity in the nonweighted forelimb during the period of weighting, suggesting a threshold for evoking proprioceptive changes. Findings suggest that newborn rats use movement-related feedback to modulate spontaneous motor activity, and corroborate studies of human infants that have suggested a role for proprioception during early motor development.

Sampling Development.

Research in developmental psychology requires sampling at different time points. Accurate depictions of developmental change provide a foundation for further empirical studies and theories about developmental mechanisms. However, overreliance on widely spaced sampling intervals in cross-sectional and longitudinal designs threatens the validity of the enterprise. This article discusses how to sample development in order to accurately discern the shape of developmental change. The ideal solution is daunting: to summarize behavior over 24-hour intervals and collect daily samples over the critical periods of change. We discuss the magnitude of errors due to undersampling, and the risks associated with oversampling. When daily sampling is not feasible, we offer suggestions for sampling methods that can provide preliminary reference points and provisional sketches of the general shape of a developmental trajectory. Denser sampling then can be applied strategically during periods of enhanced variability, inflections in the rate of developmental change, or in relation to key events or processes that may affect the course of change. Despite the challenges of dense repeated sampling, researchers must take seriously the problem of sampling on a developmental time scale if we are to know the true shape of developmental change.

Opioid mediation of amniotic fluid effects on chemosensory responsiveness in the neonatal rat.

The present study investigated if oral exposure to milk or amniotic fluid (AF) alters responsiveness to sensory stimulation in the neonatal rat, and whether these effects are mediated by the opioid system. Facial wiping evoked by intraoral lemon infusion was used as a measure of sensory responsiveness. Pups were tested in a supine posture, because they showed more paw-face strokes during facial wiping than pups tested prone (Experiment 1). Moreover, pups orally exposed to milk (Experiment 2) or AF (Experiment 3) showed a diminished wiping response to lemon compared to controls exposed to water. Blockade of opioid receptors with the nonselective antagonist naltrexone (Experiment 4) or the kappa antagonist nor-binaltorphimine (Experiment 5) reinstated higher levels of facial wiping after AF exposure. These findings confirm developmental continuity between fetal and neonatal behavioral responses to AF and the ability of AF to induce activity at kappa receptors of the endogenous opioid system.

Seeing the world through a third eye: Developmental systems theory looks beyond the nativist-empiricist debate.

In response to the commentaries on our paper (Spencer et al., 2009) we summarize what a developmental systems perspective offers for a twenty-first century science of development by highlighting five insights from developmental systems theory. Where applicable, the discussion is grounded in a particular example-the emergence of ocular dominance columns in early development. Ocular dominance columns are a paragon of epigenesis and are inconsistent with the nativist view. We conclude with optimism that developmental science can move beyond the nativist-empiricist debate armed with both modern technological tools and strong theory to guide their use.

Short arms and talking eggs: Why we should no longer abide the nativist-empiricist debate.

The nativist-empiricist debate and the nativist commitment to the idea of core knowledge and endowments that exist without relevant postnatal experience continue to distract attention from the reality of developmental systems. The developmental systems approach embraces the concept of epigenesis, that is, the view that development emerges via cascades of interactions across multiple levels of causation, from genes to environments. This view is rooted in a broader interpretation of experience and an appreciation for the nonobvious nature of development. We illustrate this systems approach with examples from studies of imprinting, spatial cognition, and language development, revealing the inadequacies of the nativist-empiricist debate and the inconvenient truths of development. Developmental scientists should no longer abide the nativist-empiricist debate and nativists' ungrounded focus on origins. Rather, the future lies in grounding our science in contemporary theory and developmental process.

In defense of change processes.

Nativist and constructivist approaches to the study of development share a common emphasis on characterizing beginning and end states in development. This focus has highlighted the question of preservation and transformation-whether core aspects of the adult end state are present in the earliest manifestations during infancy. In contrast, a developmental systems approach emphasizes the process of developmental change. This perspective eschews the notions of objective starting and ending points in a developmental progression and rejects the idea that any particular factor should enjoy a privileged status in explaining developmental change. Using examples from motor development and animal behavior, we show how a developmental systems framework can avoid the pitfalls of the long and contentious debate about continuity versus qualitative change.

What is the shape of developmental change?

Developmental trajectories provide the empirical foundation for theories about change processes during development. However, the ability to distinguish among alternative trajectories depends on how frequently observations are sampled. This study used real behavioral data, with real patterns of variability, to examine the effects of sampling at different intervals on characterization of the underlying trajectory. Data were derived from a set of 32 infant motor skills indexed daily during the first 18 months. Larger sampling intervals (2-31 days) were simulated by systematically removing observations from the daily data and interpolating over the gaps. Infrequent sampling caused decreasing sensitivity to fluctuations in the daily data: Variable trajectories erroneously appeared as step functions, and estimates of onset ages were increasingly off target. Sensitivity to variation decreased as an inverse power function of sampling interval, resulting in severe degradation of the trajectory with intervals longer than 7 days. These findings suggest that sampling rates typically used by developmental researchers may be inadequate to accurately depict patterns of variability and the shape of developmental change. Inadequate sampling regimes therefore may seriously compromise theories of development.

Prenatal Development of Interlimb Motor Learning in the Rat Fetus.

The role of sensory feedback in the early ontogeny of motor coordination remains a topic of speculation and debate. On E20 of gestation (the 20th day after conception, 2 days before birth), rat fetuses can alter interlimb coordination after a period of training with an interlimb yoke, which constrains limb movement and promotes synchronized, conjugate movement of the yoked limbs. The aim of this study was to determine how the ability to express this form of motor learning may change during prenatal development. Fetal rats were prepared for in vivo study at 4 ages (E18-21) and tested in a 65-min training-and-testing session examining hind limb motor learning. A significant increase in conjugate hind limb activity was expressed by E19, but not E18 fetuses, with further increases in conjugate hind limb activity on E20 and E21. These findings suggest substantial development of the ability of fetal rats to modify patterns of interlimb coordination in response to kinesthetic feedback during motor training before birth.

Conjugate limb coordination after experience with an interlimb yoke: evidence for motor learning in the rat fetus.

This study investigated the capacity of the E20 rat fetus to adaptively alter patterns of interlimb coordination in a prenatal model of motor learning. Fetal limb movement was manipulated with an interlimb yoke, consisting of a fine thread attached at the ankles, which created a physical linkage between two limbs. Exposure to the yoke resulted in a gradual increase in conjugate movements of the yoked limbs during a 30-min training period, which persisted after removal of the yoke. Training effects were evident when the yoke was applied to two hindlimbs, two forelimbs, or a homolateral forelimb-hindlimb pair. A savings in the rate of acquisition also was observed when fetuses experienced yoke training in a second session. These data argue that the rat fetus can respond to kinesthetic feedback resulting from variation in motor performance, which suggests that experience contributes to the development of coordinated motor behavior before birth.

The serotonergic agonists quipazine, CGS-12066A, and alpha-methylserotonin alter motor activity and induce hindlimb stepping in the intact and spinal rat fetus.

The effects of serotonergic agonists were examined in intact and spinal fetuses, using an in vivo fetal rat preparation. On Gestational Day 20, fetuses were prepared with a midthoracic or sham spinal transection. Dose-response curves were obtained for quipazine (nonselective 5-hydroxytryptamine [5-HT] agonist; 1.0-10.0 mg/kg), CGS-12066A (5-HT-sub(1B) agonist; 1.0-30.0 mg/kg), and alpha-methylserotonin (alpha-Me-5-HT; 5-HT-sub-2 agonist; 0.2-15.0 mg/kg). During a 10-min test, each of the agonists (delivered via intraperitoneal injection) influenced fetal behavior: They increased the occurrence of head movements, mouthing, and hindlimb stepping. Quipazine and alpha-Me-5-HT also promoted hindlimb activity in spinal fetuses. Thus, stimulation of the fetal 5-HT system modulates motor activity at multiple levels of the developing central nervous system.

Development of interlimb movement synchrony in the rat fetus.

In the fetal rat, interlimb synchrony is a prominent form of temporally organized spontaneous motor activity in which movement of different limbs occurs at nearly the same instant. In the present study, synchrony profiles were created for different pairwise combinations of limbs over the last 5 days of gestation. Observed rates of synchrony differentiated from randomized time series from Gestational Day 19 to Day 21 (E19-E21), with forelimb synchrony emerging earlier than that of other limb pairs. Synchrony profiles were elevated at the shortest intervals between successive limb movements, indicating that movements became more tightly coupled toward the end of gestation. Interlimb synchrony appears to be a robust method of quantifying fetal movement and may prove useful as a tool for assessing prenatal nervous system functioning.