Age-Related Changes and Condition-Dependent Modifications in Distribution of Limb Movements During Embryonic Motility

Abstract

It has long been known that the chick initiates spontaneous motility early in embryogenesis, that the distribution of this activity is episodic, and that it varies both quantitatively and qualitatively with age. It is also well established that embryonic motility is controlled by spinal circuits and features of motility at early stages of development are likely the product of immature network properties. Over the course of embryonic development, however, the episodic distribution of motility becomes more variable. Because we are interested in determining whether movement experience in ovo is fundamental to the establishment of adaptive posthatching behaviors, this study examines the normal within-subject variability of episodic activity in embryos across ages under control and several experimental conditions. The distribution of activity, pause, and episode duration was obtained from video recordings of embryos prepared for electromyographic (EMG) and/or kinematic studies of motility in ovo at select ages (E9, E10, E12, E15, E18) under control conditions (control), acute reduction in buoyancy (ARB), ankle restraint (AR), thoracic spinal transection (spinal). Both control and ARB embryos exhibited significant age-related changes in the distribution of motility. Activity duration progressively increased with age and largely accounted for age-related increases in the variability of episodic behavior. Pause duration decreased markedly between E9 and E12 and did not appear to be a critical parameter in accounting for age-related changes in motility distribution. Activity duration was significantly lengthened in ARB embryos and decreased in spinal embryos. Pause duration was selectively lengthened in AR embryos. Collectively, age-related changes and selective effects of experimental preparations suggest that activity and pause duration are controlled by different mechanisms that operate independent of one another by E12. The results also suggest that the spinal network controlling motility becomes increasingly dependent on excitatory drive from supraspinal centers between E9 and E18. It is proposed that age-related increases in activity duration variability and condition-dependent effects on the distribution of activity are indicative of changing inputs weights for descending and sensory pathways and that they significantly impact spinal control of motility as the embryo's movement and posture are increasingly constrained by the fixed volume of the egg.

Fetal Onset of General Movements

“…The motility consists of simple and stereotyped movements. Similar simple and stereotyped movements are reported as first movements in other species like fish (14), chicken (15), and rat (16). Wintrebert (14) in 1920 argued that the earliest forms of motility were purely myogenic, as sideways flexion of the head persisted after removal of the spinal cord.…”

“…Wintrebert (14) in 1920 argued that the earliest forms of motility were purely myogenic, as sideways flexion of the head persisted after removal of the spinal cord. It is nowadays generally recognized that spontaneous activity is a major characteristic of the developing nervous system (15,16). Thus, the earliest fetal movement activity is assumed to be generated by central pattern networks in the spinal cord and brainstem (17) and mediated by the immature muscle fibers of the myotomes (18).…”

Age-related Changes in the Response of Embryonic Motility to Acute Hypoxia During the Third Quarter of Chick Embryogenesis

“…2A) generally agree with the results of earlier studies [7,16,17,26], where these parameters were also used for qualitative and quantitative estimation of the motility. However, note that Bradley [16] and Wu et al [26] found that the APh and IPh durations were close to each other on D10.…”

“…Apparently, some additional factors hindered the rapid restoration of motility. For example, it was previously shown that the structure of the APh changes with age and it is determined by the activity not only of spinal neurons, but also the brain, muscles, and proprioceptors [10,16]. The considerably greater decrease in the APh duration during hypoxia on D15 compared to earlier ages was probably accounted for by switching off of these additional components, which might have been restored under hypoxia more slowly than the activity of spinal motor networks.…”

“…Then the motility character was beginning to gradually change mainly due to the appearance of repetitive limb movements that have been described by Bradley et al [23], and the cyclic character of the motility became less pronounced. Other authors have also reported an increased variation of the parameters of cyclic motility (APh and IPh) with embryonic age [16,24,25]. This prevents the use of these parameters as quantitative estimates of the motility after D15, especially in studying the effects of exogenous factors.…”