As a consequence of the degeneration and replacement of the jaw muscle fibers in the leopard frog, Rana pipiens, trigeminal motoneurons innervate different targets before and after metamorphosis. This investigation examined the morphological correlates of the reassignment of trigeminal motoneurons during the initial phases of myofiber turnover. Specifically, silver-cholinesterase histochemistry and electron microscopy were used to 1) identify the fate of motor axons within the neuromuscular junctions (NMJs) applied to degenerating larval myofibers and 2) to determine the origin(s) of the motor axons that innervate the postmetamorphic muscle fibers of the jaw. The results demonstrate that the NMJs are retained on larval myofibers throughout their degeneration and are readily identifiable on the residual larval basal laminae that remain after involution of the sarcoplasm. Light and electron microscopic observations provide evidence that both pre- and post-synaptic elements are present on the degenerating fibers. Furthermore, morphometric analyses indicate that the preponderance (86%) of motor axons supplying adult muscle fibers originates from the larval NMJs. This condition suggests that metamorphic redeployment of trigeminal motoneurons occurs through the resumption of growth at the axon terminal supplying larval muscle rather than through the proximal collateralization of these axons and resorption of larval terminals.
Larval jaw myofibers in Rana pipiens degenerate during metamorphosis and are replaced by a second wave of myogenesis that provides for adult jaw function. Trigeminal motoneurons that innervate larval myofibers transfer their preterminal axons to these adult successors where they establish new motor endplates. Silver/acetyl-cholinesterase histochemistry was used to compare innervation patterns in the larval and adult jaw adductor muscles and to plot the time course over which these changes occur. Innervation patterns differ substantially on the pre- and postmetamorphic myofiber populations. Jaw myofibers in the tadpole were unique by virtue of their exceedingly high level of distributed and focal polyinnervation. Each myofiber was innervated by approximately 10 small, junctional zones, most containing multiple axons, diffusely distributed over the length excepting small junctional free zones at either end of the muscle. In juvenile frogs, immediately following redeployment, the replacement myofibers had a polyinnervation pattern that mirrors that observed in the larvae. However, by 12 weeks after metamorphosis there was a clear condensation of the end plates into multiple zones. Moreover, jaw myofibers in adult frogs had a reduced level of distributed and focal polyinnervation, less than 15% show signs of polyinnervation. The pattern of polyinnervation, axonal redeployment and myofiber degeneration is consistent with the hypothesis that the larval jaw muscles serve as a population of primary myofibers, ensuring survival of the trigeminal motoneurons through the prolonged period of larval development, while also providing a scaffold on which secondary jaw myofibers are constructed.
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