Quantification of reactive arm responses to a slip perturbation.

The purpose of this study was two-fold: 1) characterize bilateral upper extremity responses during a slip event in both the sagittal and frontal planes, and 2) to examine the utility of using slip onset as the measurement reference for behavioral responses of the upper extremities using EMG latency. Sixteen healthy young adults were exposed to an unexpected slip during walking. Three-dimensional arm kinematics (excursions) and electromyographic onset latencies (bilateral deltoids) were quantified. Thirteen of the 16 participants recovered their balance following the slip perturbation. Of those who recovered, multi-planar arm responses were observed bilaterally. The arm contralateral to the slipping foot demonstrated significantly greater excursion in the frontal plane than the ipsilateral arm (p < 0.001), whereas excursions in the sagittal plane did not differ between arms (p = 0.75). Further, the frontal plane excursion of the contralateral arm was greater than sagittal plane excursion (p < 0.001). The electromyographic onset of deltoid activity was equivalent in both arms (57-76 ms), despite the differences in kinematics. Multi-plane arm motion occurs in response to a slip perturbation. Specifically, frontal plane motion of the arm contralateral to the slipping foot exhibited the greatest amount of excursion.

Ankle muscle tenotomy does not alter ankle flexor muscle recruitment bias during locomotor-related repetitive limb movement in late-stage chick embryos.

In ovo, late-stage chick embryos repetitively step spontaneously, a locomotor-related behavior also identified as repetitive limb movement (RLM). During RLMs, there is a flexor bias in recruitment and drive of leg muscle activity. The flexor biased activity occurs as embryos assume an extremely flexed posture in a spatially restrictive environment 2-3 days before hatching. We hypothesized that muscle afferent feedback under normal mechanical constraint is a significant input to the flexor bias observed during RLMs on embryonic day (E) 20. To test this hypothesis, muscle afference was altered either by performing a tenotomy of ankle muscles or removing the shell wall restricting leg movement at E20. Results indicated that neither ankle muscle tenotomy nor unilateral release of limb constraint by shell removal altered parameters indicative of flexor bias. We conclude that ankle muscle afference is not essential to ankle flexor bias characteristic of RLMs under normal postural conditions at E20.

Differences in flexor and extensor activity during locomotor-related leg movements in chick embryos.

Prior to hatching, chick embryos spontaneously produce repetitive limb movements (RLMs), a developmental precursor to walking. During RLMs, flexor and extensor muscles are alternately active as during stance and swing phases of gait. However, previous studies of RLMs observed that flexor muscles were rhythmically active for many cycles, whereas extensors often failed to be recruited. Thus, we asked if flexor muscles are preferentially recruited during RLMs in chick embryos 1 day before hatching and onset of walking. Using a within-subject design, we compared EMG burst parameters for flexor and extensor muscles acting at the hip or ankle. Findings indicated that flexor burst count exceeded extensor count. Also, flexor muscles were consistently recruited at the lowest levels of neural drive. We conclude that there is a bias favoring flexor muscle recruitment and drive during spontaneously produced RLMs. Potential neural mechanisms and developmental implications of our findings are discussed.

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 study's 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.

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.

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.

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.

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.

Limb movements during embryonic development in the chick: evidence for a continuum in limb motor control antecedent to locomotion.

New imaging technologies are revealing ever-greater details of motor behavior in fetuses for clinical diagnosis and treatment. Understanding the form, mechanisms, and significance of fetal behavior will maximize imaging applications. The chick is readily available for experimentation throughout embryogenesis, making it an excellent model for this purpose. Yet in 40 yr since Hamburger and colleagues described chick embryonic behavior, we have not determined if motility belongs to a developmental continuum fundamental to posthatching behavior. This study examined kinematics and synchronized electromyography (EMG) during spontaneous limb movements in chicks at four time points between embryonic days (E) 9-18. We report that coordinated kinematic and/or EMG patterns were expressed at each time point. Variability observed in knee and ankle excursions at E15-E18 sorted into distinct in-phase and out-of-phase patterns. EMG patterns did not directly account for out-of-phase patterns, indicating study of movement biomechanics will be critical to fully understand motor control in the embryo. We also provide the first descriptions of 2- to 10-Hz limb movements emerging E15-E18 and a shift from in-phase to out-of-phase interlimb coordination E9-E18. Our findings revealed that coordinated limb movements persist across development and suggest they belong to a developmental continuum for locomotion. Limb patterns were consistent with the half center model for a locomotor pattern generator. Achievement of these patterns by E9 may thus indicate the embryo has completed a critical phase beyond which developmental progression may be less vulnerable to experimental perturbations or prenatal events.

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.

Selective effects of light exposure on distribution of motility in the chick embryo at E18.

It is well established that orderly patterns of motor neuron activity, muscle recruitment, and limb movement are generated in chicks during motility by embryonic day (E)9, the midpoint in embryonic development. However, our recent work suggests that some attributes of motility, such as the rhythm of repetitive limb movements and distribution of activity, become less orderly after E9. In this study, we extend these observations by performing continuous force recordings over a 24-h period in ovo at E18 with augmented sampling of synchronized video and electromyogram (EMG) recordings. We report the distribution of three repetitive behaviors, rapid limb movement, respiratory-like movement, and beak clapping, identified in force recordings, and the general distribution of motility. We also test a model recently proposed to account for age-related changes in motility parameters. In the model, we proposed that circadian networks contribute to the age-related changes in distribution of motility. As a first test of this hypothesis, we examine whether light exposure contributes to the variable distribution of motility by comparing motility parameters at E18 for embryos incubated and tested under either a 12-h light/dark cycle or continuous light. Results suggest that exposure to light increases the total amount of activity and hastens the onset of extended respiratory-like movement sequences but does not impact expression of repetitive limb movement or beak clapping at E18. The possible influence of circadian mechanisms on embryonic behavior and insensitivity of repetitive limb movements to light exposure are discussed.