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Morphology, axonal projection pattern, and response types of tectal neurons in plethodontid salamanders. I: tracer study of projection neurons and their pathways.
In three salamander species (Hydromantes italicus, H. genei, Plethodon jordani), the tectobulbospinal and tectothalamic pathways and their cells of origin were studied by means of anterograde and retrograde biocytin and tetramethylrhodamine tracing. In plethodontid salamanders, five types of tectal projection neurons were identified. TO1 neurons have widefield dendritic trees that arborize in the layers of retinal afferents and form a neuropil in the superficial layer; axons constitute the crossed tectospinal tract. Dendrites of TO2 cells have the largest dendritic trees that arborize in the intermediate and deep layers of retinal afferents; axons constitute a lateral uncrossed tectospinal tract. TO3 cells have widefield dendritic trees that arborize in the deep layer of retinal afferents and in the layer of tectal efferents; axons constitute a superficial uncrossed tectospinal tract. TO4 cells have slender primary dendrites and small-field dendritic trees that arborize in the intermediate layers of retinal afferents; axons constitute another lateral uncrossed tectospinal tract. TO2, TO3, and TO4 cells also have ascending axons that run to the ventral and dorsal thalamus. TO5 cells have slender primary dendrites and small-field dendritic trees that extend into the superficial layers of retinal afferents; their fine axons constitute the bulk of the pathways ascending to the ipsilateral and contralateral thalamus. These morphological types of projection neurons and their ascending and descending axonal pathways closely resemble those found in frogs, reptiles, and birds. Their role in visual and visuomotor functions is discussed.
Morphology, axonal projection pattern, and response types of tectal neurons in plethodontid salamanders. II: intracellular recording and labeling experiments.
In the plethodontid salamanders Plethodon jordani and P. glutinosus, the morphology and axonal projections of 140 tectal neurons and their responses to electrical optic nerve stimulation were determined by intracellular recording and biocytin labeling. Six types of neurons are distinguished morphologically. TO1 neurons have wide dendritic trees that arborize mainly in tectal layers 1 and 3; they project bilaterally to the tegmentum and contralaterally to the medulla oblongata. TO2 neurons have very wide dendritic trees that arborize mainly in layers 2 and 3; axons project bilaterally or unilaterally to the pretectum and thalamus and ipsilaterally to the medulla oblongata. TO3 neurons have very wide and flat dendritic trees confined to layers 3-5; some have the same axonal projection as TO2 neurons, whereas others have descending axons that reach only the level of the cerebellum. TO4 neurons have narrower dendritic trees that arborize in layers 2 and 3; they project to the ipsilateral pretectum, thalamus, and medulla oblongata. TO5 neurons have dendritic trees that arborize in layers 1 and 2 or 1-3 and project bilaterally or unilaterally to the pretectum and thalamus. TO-IN are interneurons, with a number of subtypes with respect to variations in dendritic arborization pattern. TO1-TO5 neurons generally have short latencies of 2-16 ms (average = 8.4 ms) at electrical optic nerve stimulation; first responses are always excitatory, often followed by inhibition. They are likely to be mono- or oligosynaptically driven by retinal afferents. TO-IN interneurons have long latencies of 20-80 ms (average = 38.6 ms) and appear to receive no direct retinal input. With their specific dendritic arborization, consequent dominant retinal input, specific axonal projections, the different types of tectal projection neurons constitute separate ascending and descending visual pathways. Hypotheses are presented regarding the nature of the information processed by these pathways.
Species, sex, and seasonal differences in VNO size.
Differences in the sizes of sensory and neural structures are used as an indication of differences in the function of those structures. Large VNOs often are interpreted to mean that this sense is particularly important in the life history of the animal. They also are assumed to be associated with more primitive animals. I examined VNO sizes across mammalian, reptilian, and amphibian lineages while attempting to account for total body size, because VNO and total body sizes are related. Most descriptions of VNO size and development are not quantified and often ambiguous. Large VNOs in a lineage should not be interpreted necessarily as primitive. Comparisons across smaller taxonomic ranges are easier to interpret. Plethodontid salamanders are a diverse set of species for which VNO descriptions show trends in size associated with habitat, sex, and season. Semiaquatic species tend to have proportionately larger VNOs than terrestrial species, males have larger organs than females, and VNOs can show increases and decreases in size that may be associated with seasonal activities. Salamanders may use their VNOs to locate and identify mates, as part of the courtship sequences, or to identify and assess neighboring territory holders.
The problem of replacement and differentiation of the intestinal epithelium: its relation to squamous metaplasia in the uterine cervix.
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Neural crest-like cells originate from the spinal cord during tail regeneration in adult amphibian urodeles.
Using in vitro cell-marking experiments and transplantation in tail regenerates, we have recently shown (Benraiss et al., 1996) that clonal cells derived from adult newt spinal cord (SC) cultures could find suitable cues in blastemal mesenchyme to enable them to differentiate into melanocytes or Schwann cells. This led to the question of whether neural crest-like cell derivatives might emerge from the ependymal tube as tail regeneration proceeded. To address this question we used the biolistic method for in situ transfection of caudal SC cells. These cells were transfected with an alkaline phosphatase marker gene. The potentialities of transfected cell derivatives in tail regenerates were analyzed using histochemistry or immunohistochemistry. As early as eight days after transfection, labeled cells were detected in the regenerating SC and around its "terminal vesicle" (TV). Two to four weeks following transfection, most of the labeled cell derivatives could be identified either by dark granules as melanocytes or by galactocerebroside staining as Schwann cells. Electron microscopic investigations revealed the incompletely organized cytoarchitecture of the TV, suggesting that an exit of cells was possible at this level, at least from its "open" dorsal part. Furthermore, the localization of ciliated cells in the blastemal mesenchyme, especially around the TV, supported this view by suggesting that they might be ependymal cells detached from it. Our findings therefore led us to believe that in the newt, during tail regeneration, neural crest-like cells emerging from the TV could participate in the formation of the peripheral nervous system, especially by providing Schwann cells and melanocytes.
Sperm storage in the spermatheca of the red-back salamander, Plethodon cinereus (Amphibia: Plethodontidae).
In northern Indiana, the mating season of Plethodon cinereus occurs after hibernation from March until June, when oviposition begins. During the mating season, a female stores sperm in its spermatheca, a compound tubular gland in the roof of the cloaca. The apical cytoplasm of the spermathecal epithelium is filled with large secretory vacuoles whose product is released while sperm are stored. Females induced to oviposit in June and July by injections of human chorionic gonadotropin (hCG) still retain much sperm 1 month after oviposition, but secretory vacuoles are absent in all specimens sacrificed in July and August. Instead, some sperm are embedded in the spermathecal epithelium with resultant spermiophagy involving lysosomes. A female sacrificed in September 2 months after oviposition possesses scant sperm, but spermiophagy alone does not seem extensive enough to account for the decrease in sperm numbers. Females sacrificed in October prior to hibernation lack sperm in their spermathecae; some secretory vacuoles are present, but they are not as numerous or as enlarged as in specimens collected in March and May. Inter- and intrafamilial differences in the cytology of sperm storage may not be phyletically informative at the family level but related to species-specific reproductive adaptations.
Primary and secondary somatosensory projections in direct-developing plethodontid salamanders.
In three species of plethodontid salamanders (Plethodon jordani, Hydromantes italicus, and Bolitoglossa subpalmata), primary and secondary somatosensory pathways were investigated by means of tract-tracing in vivo and in vitro using biocytin, horseradish peroxidase, and neurobiotin. Afferent sensory fibers of cranial nerves V, VII, and X and the brachial nerve run in the dorsal funiculus of the medulla oblongata and spinal cord. Fibers ascend to the level of, but do not enter, the cerebellum. In the caudal medulla oblongata, sensory tracts of the cranial nerves descend in a dorsal and a dorsolateral bundle and reach the level of the fourth spinal nerve. Two bundles are likewise formed by spinal afferent fibers, which descend to the level of the seventh spinal nerve. Secondary somatosensory projections ascend in contralateral ventral, contralateral lateral, and ipsilateral lateral tracts, the latter two corresponding to the spinal lemniscal tracts of Herrick. These tracts reach the cerebellum, mesencephalic, and diencephalic targets (tegmentum, torus, tectum, tuberculum posterius, pretectum, and ventral thalamus) ipsi- and contra-laterally. The projection to the tectum is confined to fiber layer 4. Fibers of the ascending tracts cross in the cerebellar and tectal commissure. Our study demonstrates that the ascending secondary somatosensory pathways of plethodontid salamanders differ remarkably from those of other amphibians.
Anuran postnasal wall homology: an experimental extirpation study.
The nasal placode was extirpated unilaterally in Gosner stage 18-20 embryos of Rana sylvatica, R. palustris and R. pipiens, in order to test alternative proposed schemes of homology for the ethmoidal attachment of the palatoquadrate in anurans and urodeles. Absence of the nasal sac has no pronounced effect on the formation of larval chondrocranial structures. In contrast, in metamorphosed animals the lamina orbitonasalis and inferior prenasal process are the only nasal capsule structures present on the operated side. The medial nasal branch of the deep ophthalmic nerve passes forward over the dorsal surface of the lamina orbitonasalis, rather than through an orbitonasal foramen. Comparison with previous experimental work on urodeles supports the traditional homology of the anuran lamina orbitonasalis with the antorbital process of urodeles and other vertebrates.
Description of the postcloacal glands of Plethodon cinereus, the red-backed salamander, during bouts of scent marking.
Plethodon cinereus, the red-backed salamander, is a small territorial vertebrate that defends refugia located on the forest floor. As a component of territorial defense, these animals use scent marks to advertise their refugia. Behavioral evidence indicates that scent marks are produced by the postcloacal glands located on the ventral surface of the tail just posterior to the cloaca. We placed animals on unmarked substrates and recorded changes in serous acini from the postcloacal and shoulder region over a 48-h period. Within the first hour there was an increase in the number of acini filled with secretory product in the postcloacal region. At 12 h the number of full acini decreased and the number of empty acini increased. By 24 h the number of empty acini had decreased and the number of renewing acini containing secretory cells producing product had increased. By 48 h the ratio of full to empty to renewing acini was similar to those observed at the start of the study. In the shoulder region, no significant changes in the ratio of full to empty to renewing acini were observed. Observations of the serous acini within the postcloacal region and the shoulder region indicate that the mode of secretory production is holocrine. These findings are additional evidence that the postcloacal glands are the site of scent mark production.
Early origins of modern birds and mammals: molecules vs. morphology.
Recent claims from molecular evidence that modern orders of birds and mammals arose in the Early Cretaceous, over 100 million years (Myr) ago, are contrary to palaeontological evidence. The oldest fossils generally fall in the time range from 70-50 Myr ago, with no earlier finds. If the molecular results are correct, then the first half of the fossil record of modern birds and mammals is missing. Suggestions that this early history was played out in unexplored parts of the world, or that the early progenitors were obscure forms, are unlikely. Intense collecting over hundreds of years has failed to identify these missing fossils. Control experiments, in the form of numerous Cretaceous-age fossil localities which yield excellently preserved lizards, salamanders, birds, and mammals, fail to show the modern forms. The most likely explanation is that they simply did not exist, and that the molecular clock runs fast during major radiations.
Morphology, axonal projection pattern, and responses to optic nerve stimulation of thalamic neurons in the salamander Plethodon jordani.
In the salamander Plethodon jordani, the morphology and axonal projections of thalamic (TH) neurons and their responses to electrical optic nerve stimulation were determined by intracellular recording and biocytin labeling under in vitro, whole-brain conditions. Based on their axonal projections, labeled neurons (n = 76) were divided into the following groups: TH1 neurons, with mostly ipsilateral projections to the striatum; TH2 neurons, with ipsilateral or bilateral projections to the medial amygdala and nucleus accumbens; TH3 neurons, with bilateral projections to the medial and dorsal pallium; TH4 neurons, with mostly ipsilateral projections to the striatum and ipsilateral projections to the tectum opticum, tegmentum, and rostral medulla oblongata; and TH5 neurons, with ipsilateral projections to the tegmentum, medulla oblongata, and rostral spinal cord without (TH5.1) or with (TH5.2) additional projections to the optic tectum. TH1-TH4 neurons are found in the dorsal thalamus and around the sulcus medialis, and TH5 neurons are found in the ventral thalamus. Labeled neurons with ascending projections, i.e., the more dorsally situated TH1-TH4 neurons, are mostly inhibited by electrical stimulation of the optic nerve and have significantly longer latencies (mean +/- S.D., 42.1 +/- 11.6 msec) than neurons with exclusively descending projections, i.e., the ventrally located TH5 neurons (8.5 +/- 6.1 msec), which receive the bulk of retinal afferents and show excitation at electrical optic nerve stimulation. Neurons recorded without labeling in the dorsal thalamus likewise exhibit mostly inhibition and have significantly longer latencies (35.7 +/- 18.9 msec) than those recorded in the ventral thalamus (10.9 +/- 7.7 msec), which mostly show excitation. None of the neurons recorded in the dorsal thalamus followed repetitive stimulation of the optic nerve. Thus, neurons situated in the dorsal thalamus and projecting to pallial or subpallial telencephalic targets are unlikely to receive monosynaptic or oligosynaptic, excitatory retinal input. Accordingly, no retino-thalamo-telencephalic pathway homologous to that found in amniotes appears to exist in salamanders.
Ultrastructure of the skin mechanoreceptors of the Chinese giant salamander, Andrias davidianus.
The ultrastructure of two kinds of mechanoreceptive organs, pit organs and neuromasts, in the skin of adult giant salamanders (Andrias davidianus) was studied by transmission electron microscopy. Neuromasts and pit organs differ in their types of synapses, the spatial distribution of kinocilia on sensory cells, and in the degree to which sensory cells are separated by processes of the supporting cells; the two organs probably serve complementary functions. The neuromasts in A. davidianus differ from those of other salamanders in the orientation of kinocilia, in the extent of intrusion of supporting cells into the sensory layer, in the degree of thickening of the synaptic membranes, in the distribution of synaptic spheres, and by the absence of a cupula.
Mandibular arch musculature of anuran tadpoles, with comments on homologies of amphibian jaw muscles.
This study analyzes the structure of the mandibular arch musculature in larval, metamorphic, and postmetamorphic anurans of 26 species and makes comparisons with larvae of three caudate and one gymnophione species. Major transformations in early evolution of anuran larvae comprise, for example, the powering of the larval upper jaw cartilages by relocating insertion sites of mandibular arch levators; splitting of some larval muscles into two muscles or muscle heads (m. intermandibularis, m. lev. mand. externus, m. lev. mand. longus); evolution of a muscle invading the lower lip of the oral disk (m. mandibulolabialis), and shift of origin of the internus and longus muscles from dorsal on the cranium to sites on the ventral otic capsule and palatoquadrate, respectively. In all these characters, Ascaphus truei shares the plesiomorphic conditions with caudates. The larva of Xenopus laevis is remarkable because the insertion pattern of three larval mandibular muscles anticipates the postmetamorphic condition of frogs in general and also resembles the caudate condition. Discoglossids, bombinatorids, pelobatids, and neobatrachians are largely similar in their muscle arrangements. The filter-feeding microhylids, however, have most clearly modified the general neobatrachian pattern. Past conflicts in the interpretation and naming of muscles can be attributed to the implicit or explicit homology assumptions used. In particular, the muscles' relations to the branches of the trigeminal nerve have been the dominant criteria for inferring homology and has led to inconsistencies. This concept is questioned herein. It is observed that the relative position of the ramus mandibularis (V(3)) is more variable interspecifically in anuran larvae than previously thought. The relations of the nerve branches and muscles in larvae are maintained during metamorphosis. Considering the muscle pattern to be more conserved in interspecific comparisons than the position of the nerve branches results in a new interpretation of muscle homologies and a hypothesis of jaw muscle evolution in amphibians that is more parsimonious than earlier views. A new, simplified terminology for the jaw musculature is proposed that is applicable for larvae and adults. It maximizes information content and reflects the hypothesized homologies of amphibian jaw muscles.
Developmental basis of limb homology in urodeles: heterochronic evidence from the primitive hynobiid family.
The vertebrate limb is a classic example of homology, long assumed to be underpinned by a developmental 'bauplan' of the type proposed in the Shubin/Alberch branching and segmenting model. In the anuran/amniote pattern skeletogenesis proceeds in a proximodistal direction with digits forming from the posterior to the anterior. But in free-living larvae of 'advanced' urodeles, the pattern of skeletogenesis is distinctly different with digits 1 and 2 and the basal commune developing early, in an anterior/distal position. This different pattern is cited as evidence for a diphyletic theory of tetrapod evolution. Reassessing this problem, we analysed the pattern of early skeletogenesis of three genera (Salamandrella, Ranodon, Onychodactylus) of the 'basal' family of hynobiids, using immunofluorescence to localize chondroitin-6-SO4 in Salamandrella. Here the developmental sequence was more proximodistal (intermedium preceding basal commune; early formation of the digital arch). This pattern, also found in direct developing urodeles such as Bolitoglossa subpalmata, resembled that in anurans/amniotes. Uniquely amongst tetrapods, urodeles use their developing limbs for locomotion. We attribute the unusual pattern in 'advanced' urodeles to adaptive modification of the developing limb. Differences in the pattern between 'basic' and 'advanced' urodeles and between urodeles and anuran/amniotes are interpreted as heterochronic within an overall single tetrapod developmental bauplan.
Topography and topology in functional recovery of regenreated sensory and motor systems.
Motor and sensory nerves can re-establish coordinated movement and accurate sensation when they regrow into denervated tissues of some lower vertebrates. Motor nerves achieve their end by a competitive process in which each motoneuron innervates many muscle fibres but, in the presence of many applicants, only those synapses from motoneurons most appropriate to a muscle cell, with respect to the original pattern of development, are retained in a functional state. The discharge pattern of a motoneuron, determined by its connections with the network of central interneurons, is not sensitive to the location of the muscles in which the axon terminates, but the efficacy of transmission from the terminals is. Sensory nerves re-establish their functional specificity as to receptor type by an inductive process occurring at the terminals along with the cessation of growth. However, in the case of cutaneous nerves they can terminate anywhere over the skin surface. The return of correctly localized reflex behaviour therefore demands a restructuring of the central nervous system in response to local position-specific signals, presumably of developmental origin, that are supplied to the sensory nerves by the skin. The re-arrangement of the central nervous connections made by the central processes of the sensory neurons probably uses the same competitive mechanism of enabling and disabling formed synaptic connections as is used in sorting out the correct site of functional termination of the peripheral processes of motoneurons.
THE STRUCTURE OF THE FUNCTIONAL PRONEPHROS IN LARVAE OF AMBYSTOMA OPACUM AS STUDIED BY LIGHT AND ELECTRON MICROSCOPY.
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Fine structure of nerves in the regenerating limb of the newt Triturus.
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