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K E Alley

Publications and source records attributed to K E Alley.

17 recordsLinked to original sources

Defining distress.

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Animal Care Committees↗

Neuromuscular remodeling and myofiber turnover in Rana pipiens' jaw muscles.

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.

Animals↗

Reutilization of trigeminal motoneurons during amphibian metamorphosis.

Indirect evidence suggests that trigeminal motoneurons (Vmns) in Rana pipiens innervate distinct myofiber populations in tadpoles and adult frogs. Redeployment occurs when the larval myofibers die and are replaced during metamorphosis. To directly test this hypothesis, DiI was injected into the larval muscle and Fast Blue into the replacement myofiber population. Over 95% of the Vmns contained both tracers, providing support for the innervation of sequential targets by the same motoneurons.

Animals↗

Jaw muscle development as evidence for embryonic repatterning in direct-developing frogs.

The Puerto Rican direct-developing frog Eleutherodactylus coqui (Leptodactylidae) displays a novel mode of jaw muscle development for anuran amphibians. Unlike metamorphosing species, several larval-specific features never form in E. coqui; embryonic muscle primordia initially assume an abbreviated, mid-metamorphic configuration that is soon remodelled to form the adult morphology before hatching. Also lacking are both the distinct population of larval myofibres and the conspicuous, larval-to-adult myofibre turnover that are characteristic of muscle development in metamorphosing species. These modifications are part of a comprehensive alteration in embryonic cranial patterning that has accompanied life history evolution in this highly speciose lineage. Embryonic 'repatterning' in Eleutherodactylus may reflect underlying developmental mechanisms that mediate the integrated evolution of complex structures. Such mechanisms may also facilitate, in organisms with a primitively complex life cycle, the evolutionary dissociation of embryonic, larval, and adult features.

Animals↗

A scanning electron-microscopic study of tongue development in the frog Rana pipiens.

Feeding behaviour changes drastically during metamorphosis as larval suction feeders become adult lingual feeders. In order to understand this transition, the general morphological development of the floor of the buccal cavity in embryonic and larval Rana pipiens was studied, up to the completion of metamorphosis, by scanning electron microscopy. Rana pipiens specimens were collected, anaesthetized with tricaine methanesulphonate, staged by the methods of Shumway and Taylor and Kollros, and fixed in 0.1 M phosphate-buffered 2.5% glutaraldehyde. The oropharyngeal floors were dissected and routinely prepared for scanning. The late embryonic period (Shumway stages 21-25) is marked by the appearance on the oropharyngeal floor of two midline premetamorphic lingual papillae (PMLP), located on the second branchial arch just caudal to the hyomandibular groove. The larval tongue anlage, which incorporates PMLP along its anterior border, does not appear until stage V of the premetamorphic developmental span (Taylor-Kollros stages I-XI). Prometamorphosis (stages XII-XIX) is marked by the incorporation of the larval tongue into the adult tongue, the disappearance of the PMLP, and the appearance of the true tongue papillae. The metamorphic span (stages XX-XXIV) marks further rapid growth and differentiation of the adult tongue.

Animals↗

Redeployment of trigeminal motor axons during metamorphosis.

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.

Animals↗

Retrofitting larval neuromuscular circuits in the metamorphosing frog.

Maturation of vertebrate neuromuscular systems typically occurs in a continuous, orderly progression. After an initial period of developmental adjustment by means of cell death and axonal pruning, relatively stable relationships, with only subtle modifications, are maintained between motoneurons and their appropriate targets throughout life. However, among a restricted group of vertebrates (amphibians and especially the anuran amphibians) the sequential maturation of neuromuscular systems is altered by an abrupt reordering of the basic body plan that encompasses cellular changes in all tissues from skeleton to nervous system. Many anuran amphibians possess neuromuscular circuits that are remarkable by virtue of their complete reorganization during the brief span of metamorphosis. During this period motor systems initially designed for the behavioral patterns of aquatic tadpoles are adjusted to meet the drastically different motor activities of postmetamorphic terrestrial life. This adjustment involves the deletion of neural elements mediating larval specific activities, the accelerated maturation of neural circuits eliciting adult-specific activities and the retrofitting of larval neuromuscular components to serve postmetamorphic behaviors. This review focuses on the cellular events associated with the neuromuscular adaptation in the jaw complex during metamorphosis of the leopard frog, Rana pipiens. As part of the metamorphic reorganization of the jaw apparatus there is a complete turnover of the myofiber complement of the adductor mandibulae musculature. Trigeminal motoneurons initially deployed to the larval myofibers are redirected to new muscle fibers. Simultaneously the cellular geometry and synaptic input to these motoneurons is revamped. These changes suggest that trigeminal neuromuscular circuitry established during embryogenesis is updated during metamorphosis and reused to provide the basis for adult jaw motor activity that is far different than its larval counterpart.

Animals↗

Myofiber turnover is used to retrofit frog jaw muscles during metamorphosis.

Metamorphic reorganization of the head in anuran amphibians entails abrupt restructuring of the jaw complex as larval feeding structures are transformed into their adult configurations. In this morphometric study, light microscopy wa used to analyze the larval maturation and metamorphic transfiguration of the adductor jaw muscles in the leopard frog (Rana pipiens). Larval jaw muscles, first established during embryogenesis, continue to grow by fiber addition until prometamorphosis, stage XII. Thereafter, fiber number remains stable but additional muscle growth continues by hypertrophy of the individual fibers until metamorphic climax. During metamorphic stages XIX-XXIII, a complete involution of all larval myofibers occurs. Simultaneously, within the same muscle beds, a second wave of myogenesis produces myoblasts which are the precursors of adult jaw myofibers. New muscle fibers continue to be added to these muscles well after the completion of metamorphosis; however, the total duration of the postmetamorphic myogenic period has not been defined. These observations provide clear evidence that the entir population of primary myofibers used in larval oral activity disappears from the adductor muscle beds and is replaced by a second wave of myogenesis commencing during climax. These findings indicate that the adductor jaw muscles are prepared for adult feeding by a complicated cellular process that retrofits existing muscle beds with a completely new complement of myofibers.

Animals↗

Trigeminal motoneurons in frogs develop a new dendritic field during metamorphosis.

During metamorphosis neural systems that regulate larval behavior are altered to adult patterns. Identified strategies used to produce this alteration include neuronal deletions, neuronal additions, and the reconfiguration of existing neural circuits. This investigation focused on the structural alterations that occur in frog trigeminal motoneurons during metamorphic climax. These neurons are of special interest because they mediate the vastly different muscular activities associated with larval and adult food capture. We examined the development of the trigeminal motoneurons in anuran larvae, devoting special attention to the elaboration of different dendritic fields during metamorphic climax. When horseradish peroxidase (HRP) back-filled motoneurons in adults were scrutinized by Sholl analysis, they were found to have two spatially discrete dendritic domains, one extending ventrally and laterally, the other projecting dorsomedially into the periventricular cells. The ventrolateral dendritic field alone is represented in the motoneurons of premetamorphic larvae. The dorsomedial dendritic field first appears at the beginning of metamorphic climax and is rapidly elaborated during the terminal stages of larval development.

Animals↗

Birth dates of trigeminal motoneurons and metamorphic reorganization of the jaw myoneural system in frogs.

Drastic alterations in oral behavior characterize metamorphosis of anuran amphibians. Changes cascade through all components of the jaw apparatus from bone to muscle to nerve. In this investigation, tritiated thymidine autoradiography was used to determine the production schedule of the trigeminal motoneurons in the leopard frog, Rana pipiens. The time of origin of these neurons and their subsequent fate are of special interest given the breakdown of the larval jaw muscles and the de novo generation of adult muscle fibers during metamorphosis. Specifically, we wanted to learn whether trigeminal motoneurons are added, deleted, or reused during metamorphic climax. The entire complement of trigeminal motoneurons was produced over a 4-day span commencing at embryonic stage 13 and terminating at stage 20. Newly formed neurons are added to the primordial trigeminal nucleus in an orderly pattern. Firstborn neurons settle in the ventrorostral region of the nucleus; cells with progressively later birth dates were added in a posterodorsal direction. No additional trigeminal motoneurons are generated during larval maturation or at metamorphosis, thus indicating that the same population of neurons is present throughout the lifespan of the animal. From these observations we suggest that, during metamorphosis, the trigeminal motoneurons that supply the larval muscles switch their allegiance to the newly formed adult jaw muscles. This change of peripheral targets can be viewed as a respecification of the trigeminal motoneurons.

Animals↗

Maturation and recycling of trigeminal motoneurons in anuran larvae.

Development of the trigeminal motor system was analyzed in Rana pipiens larvae and adults. The aim of this investigation was to determine the postmetamorphic fate of the primary motoneurons that innervate the larval jaw muscles. Specifically, we wanted to ascertain whether these neurons were deleted in conjunction with their muscular targets during metamorphosis or reused to innervate the adult jaw muscles. Cell counts and horseradish peroxidase tracer were used to distinguish between these two possibilities. The number of trigeminal motoneurons was relatively constant in premetamorphic and prometamorphic larvae. A small reduction in the cellular complement of the motor nucleus occurred during metamorphic climax, but the majority (approximately equal to 90%) of the primary motoneurons were retained from the larval to the adult nervous system. The cell loss may represent motoneurons that innervated specific larval muscles that have no adult successors and thus the entire myoneural unit degenerates. Retrograde tracers indicated that all trigeminal motoneurons extended axons into the jaw muscles of both premetamorphic larvae and adult frogs. These observations provide further support for the recycling of the trigeminal motoneurons.

Animals↗

Generation of motoneurons in the rabbit brainstem.

Autoradiography of 3H-thymidine incorporation was used to determine the time of origin of motoneurons in the rabbit brainstem. With the exception of the facial nucleus, neurons of the branchial motor column originated earlier (days 9 and 10) than somatic motor column neurons (day 11). Labeling was obtained as early as embryonic day 8 for many motor nuclei and the mesencephalic trigeminal nucleus. The significance of temporal patterns of neurogenesis is discussed.

Abducens Nerve↗

Generation of the ocular motor nuclei and their cell types in the rabbit.

Autoradiography of 3H-thymidine incorporation was combined with horseradish peroxidase (HRP) transport to distinguish the birthdates of motoneurons and internuclear neurons of the abducens nucleus, and of specific motor pools within the oculomotor nucleus. Motoneurons were identified by their retrograde transport of HRP from the extraocular muscles. In other experiments, internuclear neurons of the abducens nucleus were identified by their retrograde transport of HRP from the oculomotor nucleus. We found that motoneurons and internuclear neurons are generated simultaneously in the abducens nucleus, and suggest that the differentiation of these two neuron types may be controlled by the local environment. The motor pools of the oculomotor nucleus are generated sequentially. This may reflect the mechanism whereby nuclei are constructed.

Abducens Nerve↗