Brachially innervated ectopic hindlimbs in the chick embryo. I. Limb motility and motor system anatomy during the development of embryonic behavior.
The functional status of brachially innervated hindlimbs, produced by transplanting hindlimb buds of chick embryos in place of forelimb buds, was quantified by analyzing the number and temporal distribution of spontaneous limb movements. Brachially innervated hindlimbs exhibited normal motility until E10 but thereafter became significantly less active than normal limbs and the limb movements were more randomly distributed. Contrary to the findings with axolotls and frogs, functional interaction between brachial motoneurons and hindlimb muscles cannot be sustained in the chick embryo. Dysfunction is first detectable at E10 and progresses to near total immobility by E20 and is associated with joint ankylosis and muscular atrophy. Although brachially innervated hindlimbs were virtually immobile by the time of hatching (E21), they produced strong movements in response to electrical stimulation of their spinal nerves, suggesting a central rather than peripheral defect in the motor system. The extent of motoneuron death in the brachial spinal cord was not significantly altered by the substitution of the forelimb bud with the hindlimb bud, but the timing of motoneuron loss was appropriate for the lumbar rather than brachial spinal cord, indicating that the rate of motoneuron death was dictated by the limb. Measurements of nuclear area indicated that motoneuron size was normal during the motoneuron death period (E6-E10) but the nuclei of motoneurons innervating grafted hindlimbs subsequently became significantly larger than those of normal brachial motoneurons. Although the muscle mass of the grafted hindlimb at E18 was significantly less than that of the normal hindlimb (and similar to that of a normal forelimb), electronmicroscopic examination of the grafted hindlimbs and brachial spinal cords of E20 embryos revealed normal myofiber and neuromuscular junction ultrastructure and a small increase in the number of axosomatic synapses on cross-sections of motoneurons innervating grafted hindlimbs compared to motoneurons innervating normal forelimbs. The anatomical data indicate that, rather than being associated with degenerative changes, the motor system of the brachial hindlimb of late-stage embryos is intact, but inactive.
Kitchener
P D
PD
Australian Neuromuscular Research Institute, Queen Elizabeth II Medical Centre, University of Western Australia, Nedlands.
Laing
N G
NG
D000818:Animals; D001522:Behavior, Animal / Q000502:physiology*; D016923:Cell Death / Q000502:physiology; D002467:Cell Nucleus / Q000648:ultrastructure; D002642:Chick Embryo; D004558:Electric Stimulation; D005314:Embryonic and Fetal Development / Q000502:physiology*; D016332:Fetal Tissue Transplantation / Q000502:physiology; D006614:Hindlimb / Q000033:anatomy & histology / Q000196:embryology / Q000294:innervation*; D008854:Microscopy, Electron; D009046:Motor Neurons / Q000502:physiology; D009068:Movement / Q000502:physiology*; D009470:Muscle Spindles / Q000502:physiology; D009469:Neuromuscular Junction / Q000502:physiology; D010525:Peripheral Nerves / Q000648:ultrastructure; D013116:Spinal Cord / Q000033:anatomy & histology / Q000166:cytology / Q000196:embryology*; D013569:Synapses / Q000502:physiology / Q000648:ultrastructure