Nina S. Bradley

Infant grasp learning: a computational model.

This paper presents ILGM (the Infant Learning to Grasp Model), the first computational model of infant grasp learning that is constrained by the infant motor development literature. By grasp learning we mean learning how to make motor plans in response to sensory stimuli such that open-loop execution of the plan leads to a successful grasp. The open-loop assumption is justified by the behavioral evidence that early grasping is based on open-loop control rather than on-line visual feedback. Key elements of the infancy period, namely elementary motor schemas, the exploratory nature of infant motor interaction, and inherent motor variability are captured in the model. In particular we show, through computational modeling, how an existing behavior (reaching) yields a more complex behavior (grasping) through interactive goal-directed trial and error learning. Our study focuses on how the infant learns to generate grasps that match the affordances presented by objects in the environment. ILGM was designed to learn execution parameters for controlling the hand movement as well as for modulating the reach to provide a successful grasp matching the target object affordance. Moreover, ILGM produces testable predictions regarding infant motor learning processes and poses new questions to experimentalists.

Kinematic analysis of wing and leg movements for type I motility in E9 chick embryos

Based on studies using direct observation methods, type I motility, the first motility pattern to emerge in chick embryos, is characterized as random, uncoordinated movement. Yet, electromyographic (EMG) studies indicate that leg muscles are recruited in orderly patterns of alternating flexor and extensor activity during type I motility. It has been suggested that this apparent paradox may be attributable to perturbations arising during movement in ovo under buoyant conditions. It is also possible that direct observation methods are insufficient to detect the extent of coordination between body parts during type I motility. To address the apparent discrepancy between random features reported in observational studies and reliable features reported in EMG studies, embryos were video recorded continuously for 60 min at embryonic day 9 and criteria were established to obtain homogeneous samples of motility for kinematic analysis of synchronous wing and leg movements. Limited to a single camera attached to a stereomicroscope, methods were developed to correct for out-of-plane movements of the ipsilateral wing and leg. Also, amniotic fluid was extracted from the egg in some recordings to test the possibility that movement under buoyant conditions may mask coordinated movement. Extended sequences of activity were digitized and analyzed. Results indicated that within a limb (wing or leg), direction and timing of excursions at adjacent joints covaried and limb excursions were characterized by reliable patterns of alternating flexion and extension consistent with EMG studies. Concurrent elbow and ankle excursions for ipsilateral wing and leg movements also shared common spatiotemporal features: the onset of excursions at the beginning of an activity sequence were closely timed, ankle excursions preceded elbow excursions; the number of movement cycles and duration of movement cycles were similar; ankle and elbow excursions closely covaried in 33% of cycles in control embryos; and activity sequences ended with abrupt, synchronous excursions of the elbow and ankle. Reduction in buoyancy increased the spatiotemporal covariation of shoulder and elbow excursions, but had no effect on leg movements — possibly because the leg remained more submerged than the wing. Collectively, results suggest that type I motility at embryonic day 9 is characterized by reliable features indicative of intralimb and interlimb coordination and the effect can be enhanced by a reduction in buoyancy. Thus, the apparent paradox between findings in observational and EMG studies may be attributable to both the effects of perturbations arising under buoyant conditions in ovo and the limitations of observational methods in earlier studies.

Reduction in buoyancy alters parameters of motility in E9 chick embryos.

Over the course of embryonic development, chick embryos express 3 different types of motility (I, II, III). Although neural pattern generators appear to control embryonic motility, the mechanisms responsible for the sequential emergence and/or transformations in these behaviors are not known. Given the early presence of functional sensory connections and substantial changes in movement dynamics associated with body growth in the fixed volume of an egg, it was hypothesized that changes in environmental constraints might contribute to shaping the transformations in motility. In this study, we tested the hypothesis that changes in buoyancy can alter parameters of motility in ovo at embryonic Day 9 (E9). Results demonstrate that attributes of Type I motility can be altered by a reduction in buoyancy. The possible contributions of the environment and experience to transformations in embryonic motor behavior are discussed.

Precocious Locomotor Behavior Begins in the Egg: Development of Leg Muscle Patterns for Stepping in the Chick

Background The chicken is capable of adaptive locomotor behavior within hours after hatching, yet little is known of the processes leading to this precocious skill. During the final week of incubation, chick embryos produce distinct repetitive limb movements that until recently had not been investigated. In this study we examined the leg muscle patterns at 3 time points as development of these spontaneous movements unfolds to determine if they exhibit attributes of locomotion reported in hatchlings. We also sought to determine whether the deeply flexed posture and movement constraint imposed by the shell wall modulate the muscle patterns. Methodology/Principal Findings Synchronized electromyograms for leg muscles, force and video were recorded continuously from embryos while in their naturally flexed posture at embryonic day (E) 15, E18 and E20. We tested for effects of leg posture and constraint by removing shell wall anterior to the foot. Results indicated that by E18, burst onset time distinguished leg muscle synergists from antagonists across a 10-fold range in burst frequencies (1–10 Hz), and knee extensors from ankle extensors in patterns comparable to locomotion at hatching. However, burst durations did not scale with step cycle duration in any of the muscles recorded. Despite substantially larger leg movements after shell removal, the knee extensor was the only muscle to vary its activity, and extensor muscles often failed to participate. To further clarify if the repetitive movements are likely locomotor-related, we examined bilateral coordination of ankle muscles during repetitive movements at E20. In all cases ankle muscles exhibited a bias for left/right alternation. Conclusions/Significance Collectively, the findings lead us to conclude that the repetitive leg movements in late stage embryos are locomotor-related and a fundamental link in the establishment of precocious locomotor skill. The potential importance of differences between embryonic and posthatching locomotion is discussed.

Correcting two-dimensional kinematic errors for chick embryonic movements in ovo

In motor behavior studies of chick embryos in ovo, kinematic recording is limited to a single camera system and produces kinematic data that are distorted if out-of-plane movements are not considered. CONVERT is a rule based algorithm designed to calculate 3D limb movements given 2D kinematic data. CONVERTs calculations are based on a stationary reference point, limited translation of the chick embryos trunk point, a multi-linked model of the body, and approximate limb segment lengths. Simulations indicate CONVERT calculates joint movements from 2D data with a maximum error of 6 degrees compared to a maximum error of 79 degrees if out-of-plane considerations are ignored. The approach used to correct two-dimensional kinematic measurement errors can be readily applied to other experimental conditions that restrict video recording to single camera systems.

Kinematic analysis of overground locomotion in chicks incubated under different light conditions.

Domestic chicks walk within 3-4 hr after hatching following 21 days of incubation. However, differences in light exposure can vary incubation duration. Based on pilot studies, we predicted that there would be a positive relationship between incubation duration and locomotor competence at hatching. Embryos were incubated in one of three conditions that varied light duration and intensity, and overground locomotor performance was tested on the day of hatching. Chicks incubated in continuous bright light hatched 1-2 days earlier than chicks incubated in less or no light. Kinematic findings indicated that locomotor skill was similar across incubation conditions and led us to reject our hypothesis. We propose that light may accelerate locomotor development without adversely affecting skill. Our findings raise two important implications for future studies: whether light exposure accelerates locomotor circuit development; and/or it unmasks adaptive motor skill by accelerating development of other physiological systems.

Fast Locomotor Burst Generation in Late Stage Embryonic Motility

We examined muscle burst patterns and burst frequencies for a distinct form of repetitive leg movement recently identified in chick embryos at embryonic day (E)18 that had not been previously studied. The aim was to determine if burst frequencies during repetitive leg movements were indicative of a rhythm burst generator and if maturing muscle afferent mechanisms could modulate the rhythm. Electromyographic recordings synchronized with video were performed in ovo during spontaneous movement at E15, E18, and E20. Multiple leg muscles were rhythmically active during repetitive leg movements at E18 and E20. Rhythmic activity was present at E15 but less well formed. The ankle dorsi flexor, tibialis anterior, was the most reliably rhythmic muscle because extensor muscles frequently dropped out. Tibialis anterior burst frequencies ranged from 1 to 12 Hz, similar to frequencies during fast locomotor burst generation in lamprey. The distribution in burst frequencies at E18 was greatest at lower frequencies and similar to locomotor data in hatchlings. Relative distributions were more variable at E20 and shifted toward faster frequencies. The shell wall anterior to the leg was removed in some experiments to determine if environmental constraints associated with growth contributed to frequency distributions. Wall removal had minimal impact at E18. E20 embryos extended their foot outside the egg, during which faster frequencies were observed. Our findings provide evidence that embryonic motility in chick may be controlled by a fast locomotor burst generator by E15 and that modulation by proprioceptors may emerge between E18 and E20.

Light accelerates morphogenesis and acquisition of interlimb stepping in chick embryos.

Chicks are bipedal precocious vertebrates that achieve adaptive locomotor skill within hours after hatching. Development of limb movement has been extensively studied in the chicken embryo, but few studies have focused on the preparations leading to precocious locomotor skill. Chicks typically hatch after 21 days of incubation, and recent studies provided evidence that the neural circuits for intralimb control of stepping are established between embryonic days (E) 18–20. It has also been shown that variations in light exposure during embryogenesis can accelerate or delay the onset of hatching and walking by 1 to 2 days. Our earlier work revealed that despite these differences in time to hatch, chicks incubated in different light conditions achieved similar locomotor skill on the day of hatching. Results suggested to us that light exposure during incubation may have accelerated development of locomotor circuits in register with earlier hatching. Thus, in this study, embryos were incubated in 1 of 3 light conditions to determine if development of interlimb coordination at a common time point, 19 days of incubation, varied with light exposure during embryogenesis. Leg muscle activity was recorded bilaterally and burst analyses were performed for sequences of spontaneous locomotor-related activity in one or more ankle muscles to quantify the extent of interlimb coordination in ovo. We report findings indicating that the extent of interlimb coordination varied with light exposure, and left-right alternating steps were a more reliable attribute of interlimb coordination for embryos incubated in constant bright light. We provide evidence that morphological development of the leg varied with light exposure. Based on these findings, we propose that light can accelerate the development of interlimb coordination in register with earlier hatching. Our results lead us to further propose that alternating left-right stepping is the default pattern of interlimb coordination produced by locomotor circuits during embryogenesis.

Drift during overground locomotion in newly hatched chicks varies with light exposure during embryogenesis

In an earlier study of newly hatched chicks we reported that continuous bright light exposure throughout incubation accelerated locomotor development and continuous dark exposure delayed it, compared to less intense, intermittent light exposure. Commonly studied gait parameters indicated locomotor skill was similar across groups. However, dark incubated chicks walked with a greater step width, raising the possibility of differences in dynamic balance and control of forward progression. In this study, we established methods to retrospectively examine the previously published locomotor data for differences in lateral drift. We hypothesized that chicks incubated in darkness would exhibit more drift than chicks incubated in light. Analyses identified differences in forward progression between chicks incubated in the two extreme light conditions, supporting the studys hypothesis. We discuss the significance of our findings and potential design considerations for future studies of light-accelerated motor development in precocial and nonprecocial animals.

Spontaneous locomotor activity in late-stage chicken embryos is modified by stretch of leg muscles

Chicks initiate bilateral alternating steps several days before hatching and adaptively walk within hours of hatching, but emergence of precocious walking skills is not well understood. One of our aims was to determine whether interactions between environment and movement experience prior to hatching are instrumental in establishing precocious motor skills. However, physiological evidence of proprioceptor development in the chick has yet to be established; thus, one goal of this study was to determine when in embryogenesis proprioception circuits can code changes in muscle length. A second goal was to determine whether proprioception circuits can modulate leg muscle activity during repetitive limb movements for stepping (RLMs). We hypothesized that proprioception circuits code changes in muscle length and/or tension, and modulate locomotor circuits producing RLMs in anticipation of adaptive locomotion at hatching. To this end, leg muscle activity and kinematics were recorded in embryos during normal posture and after fitting one ankle with a restraint that supported the limb in an atypical posture. We tested the hypotheses by comparing leg muscle activity during spontaneous RLMs in control posture and ankle extension restraint. The results indicated that proprioceptors detect changes in muscle length and/or muscle tension 3 days before hatching. Ankle extension restraint produced autogenic excitation of the ankle flexor and reciprocal inhibition of the ankle extensor. Restraint also modified knee extensor activity during RLMs 1 day before hatching. We consider the strengths and limitations of these results and propose that proprioception contributes to precocious locomotor development during the final 3 days before hatching.