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The development of lateral-line receptors in Eigenmannia (Teleostei, Gymnotiformes). I. The mechanoreceptive lateral-line system.

The South American weakly electric fish of the genus Eigenmannia were induced to spawn by simulating the conditions of the rainy season. Whole animals were viewed using scanning electron microscopy, and skin from embryos and larvae of different ages was prepared for histological examination. Additional live fish were stained with vital dyes. Neuromasts develop within the epidermis and then rise to the surface, at which time a cupula is forming. The first neuromasts appear on the head, forming the temporal, mechanoreceptive lateral line, at 3.5 days after spawning, and 1 day later neuromasts appear on the trunk as a ventral trunk line. On day 8 all the cephalic neuromasts have appeared and a secondary, medial trunk line begins to form. A dorsal trunk line forms when the fish are juvenile. Eight neuromasts of the cephalic lines, 7 neuromasts of the medial trunk line and all neuromasts of the ventral and dorsal trunk lines remain at the surface and do not become enclosed in canals. The opercular neuromasts and 7 neuromasts of the ventral trunk line degenerate later. The formation of the head canals begins on day 17, whereas the canal of the medial trunk line starts to develop on day 25, and both head and trunk canal systems are completed by day 33. The mechanosensory system develops before the electrosensory system. Behavioral observations also indicate that the mechanoreceptive system is functional as early as day 5.

Animals↗

Peripheral encoding of moving sources by the lateral line system of a sit-and-wait predator

Video-tape recordings of prey-capture behaviour were made to demonstrate that stargazers can detect and capture prey in the dark and to determine the range of prey movement velocities that resulted in prey capture. Electrophysiological recording techniques were then used to determine how an artificial source (a sphere), moving at speeds within the range of recorded prey movement velocities, was encoded by anterior lateral line nerve fibres innervating the preopercular-mandibular canals on the head. A vibrating sphere was also used to measure frequency-response characteristics to determine the bandwidth of response and fibre origin (type of neuromast and location). In order to measure the relevant stimulus parameters likely to govern neural responses, the pressure-gradient pattern produced by the moving sphere was characterised with a pair of miniature hydrophones separated by approximately the same distance as head lateral line canal pores on stargazers. At least four different features of neural response patterns, including direction-dependent changes in the overall envelope of the firing rate pattern, could be predicted on the basis of measured pressure-gradient patterns. The dominant features of both the pressure-gradient and neural response patterns were produced by the wake behind the moving sphere, but behavioural observations indicated that stargazers were responding to the bow of an approaching prey, rather than its wake. Although the form of the wake behind the moving sphere is unlikely to be a good match for the stimulus mediating prey detection, these results clearly establish that pressure-gradient patterns are good predictors of neural response patterns. Thus, similar measurements of pressure-gradient patterns produced by more biologically relevant sources can be used to predict peripheral lateral line responses and stimulus features likely to be of key importance.

Journal Article↗

Horseradish peroxidase study of tectal afferents in Xenopus laevis with special emphasis on their relationship to the lateral-line system.

Afferent projections to the tectum opticum of the clawed toad Xenopus laevis were studied by injections of horseradish peroxidase (HRP) into the tectum. Cells were labelled in the following nuclei, listed from rostral to caudal: nucleus entopeduncularis anterior, nucleus anterior thalami, nucleus posterior thalami, nucleus ventromedialis thalami, nucleus ventrolateralis thalami pars dorsalis, nucleus lateralis thalami pars posterodorsalis, nucleus neuropilis postthalamici, nucleus lentiformis mesencephali, nucleus praetectalis, nucleus laminaris tori semicircularis, nucleus principalis tori semicircularis, nucleus magnocellularis tori semicircularis, nucleus profundus mesencephali, nucleus anterodorsalis tegmenti, nucleus posterodorsalis tegmenti, nucleus posteroventralis tegmenti, nucleus isthmi, nucleus lineae lateralis pars rostralis, nucleus lineae lateralis pars caudalis, nucleus intermedius, nucleus lateralis nervi octavi, nucleus descendens nervi trigemini, nucleus reticularis superior, nucleus reticularis medius, nucleus reticularis inferior, nucleus reticularis lateralis, nucleus cuneatus and area dorsalis medullae spinalis. Four of these nuclei can be associated with lateral-line processing: the nuclei lineae lateralis rostralis and caudalis of the medulla and the centrolateral nuclei magnocellularis and principalis of the torus semicircularis. The toric input is particularly prominent; it is topologically organized in that central parts of the torus project to the medial tectum, and lateral parts of the torus project to the rostrolateral tectum. For comparison, the torotectal connection was also examined in several anuran species that lose their lateral line at metamorphosis. In these animals, this projection is less well developed than in Xenopus. Therefore, it is argued that the torotectal connection primarily conveys lateral-line information.

Animals↗

Morphology of the prometamorphic larva of the spadefoot toad, Scaphiopus intermontanus (Anura: Pelobatidae), with an emphasis on the lateral line system and mouthparts.

We provide a detailed description of the larval morphology of the Great Basin spadefoot toad (Scaphiopus intermontanus), a species with documented morphological variability in larval structures associated with feeding. We based our findings on laboratory-raised individuals fed a herbivorous diet. We characterized the morphology of the prometamorphic larva (limited to developmental stages 37 and 38) and then related our findings to the larval ecology of the species. Based on its morphology, such as slightly depressed body, dorsally positioned eyes, anteroventrally oriented oral disc, intermediate tail fin height and slightly attenuated tail tip, relative lack of ventral neuromasts (compared to Xenopus laevis), and pigmentation banding patterns, and habits, such as selection of breeding sites by adults and larval foraging behavior, S. intermontanus can be characterized best as belonging to a (lentic-) benthic guild of anuran larvae. Nevertheless, the larvae are capable of occupying a broader array of ecological niches. Because we characterized individuals raised on a herbivorous diet, our morphological descriptions apply only to the herbivorous S. intermontanus larva (and perhaps to those larvae that are dietary generalists and may feed carnivorously only infrequently). Our findings can serve as a baseline for future morphological and developmental comparisons with the carnivorous morphological variant of this species.

Animals↗

An adaptive filter that cancels self-induced noise in the electrosensory and lateral line mechanosensory systems of fish.

In lateral line and electrosensory systems of fish, the animal's own movements create unwanted stimulation that could interfere with the detection of biologically important signals. Here we report that an adaptive filter in the medullary nuclei of both senses suppresses self-stimulation. Second-order electrosensory neurons in an elasmobranch fish and mechanosensory neurons in a teleost fish learn to cancel the effects of stimuli that are presented coupled to the fish's movements. A model is proposed for how the adaptive filter is realized by the cerebellar-like circuits of the hindbrain nuclei in these senses.

Adaptation, Physiological↗

Comparative view of the central organization of afferent and efferent circuitry for the inner ear.

In all vertebrates, eighth nerve fibres from the inner ear distribute to target nuclei situated in the dorsolateral wall of the rhombencephalon. In amniotes, primary auditory and vestibular nuclei are readily delineated in that acoustic nuclei lie dorsal and sometimes rostral to vestibular nuclei. Fishes and aquatic amphibians have, in addition to labyrinthine organs, hair cell receptors in the lateral line system. Eighth nerve and lateral line fibres from these sense organs project to the octavolateralis region of the rhombencephalon. In this region, the primary nuclei cannot be easily divided into functionally distinct units. However, modality-specific zones seem to be present for auditory as well as lateral line projections lie dorsal and sometimes rostral to those from vestibular organs. Projections from the primary auditory and vestibular nuclei to higher order centres follow pathways which are conservative in their architecture among vertebrates. Ascending auditory fibres project either directly or via relay nuclei to a large midbrain center, the torus semicircularis (inferior colliculus) and hence to the forebrain. In fishes and aquatic amphibians, the lateral line system also sends a projection to the midbrain and information from this system may be integrated with auditory input at that level. The organization of vestibulospinal and vestibulo-ocular pathways shows little variation throughout vertebrate phylogeny. The sense organs of the inner ear of all vertebrates and of the lateral line system of anamniotes receive an efferent innervation. In anamniotes and some reptiles, the efferent supply originates from a single nucleus (Octavolateralis Efferent Nucleus) while that of "higher" vertebrates arises from separate auditory and vestibular efferent nuclei. The biological significance of this innervation for all vertebrates is not yet understood. However, an important feature common to all is the association of the efferent system with the motor centres of the hindbrain.

Animals↗

The amphibian octavo-lateralis system and its regressive and progressive evolution.

The phylogenetic and ontogenetic changes in the octavolateralis system of sarcopterygian fish and tetrapods, presumed to be important for the formation of an amphibian auditory system, are reviewed. The lateral line system shows rudimentation of lines and loss of ampullary electroreceptors in many amphibians; in some amphibians it never develops. The metamorphic changes of the lateral-line system show different patterns in the different amphibian lineages with metamorphic retention in most urodeles and metamorphic loss in most anurans. The multitude of both ontogenetic and phylogenetic changes of the lateral line system among amphibians do exclude any prediction as to how this system might have changed in ancestral amniotes. The most important auditory epithelium of the tetrapod inner ear, the basilar papilla, seems to be primitively present in all tetrapods and Latimeria. In two amphibian lineages there is a trend towards rudimentation and loss of the basilar papilla. Only in the third order, the anurans, a tympanic ear develops and the inner ear shows a progressive evolution of the auditory epithelia. Together with the known differences in the periotic labyrinth of amphibians and amniotes, this scenario suggests a parallel evolution of the amniotic and anuran auditory periphery. All mechanoreceptive hair cells of the lateral line system and the inner ear appear to receive a common and bilateral efferent innervation. Among amphibians this pattern is represented only in some urodeles, whereas anurans show a derived pattern with loss of a bilateral component and presumably also of a common neuromast/inner ear component. Changes in the rhombencephalic nuclei which receive octavo-lateralis afferent fibers show a trend towards development of auditory nuclei only in the anuran lineage. The phylogenetic appearance of an auditory nucleus in this lineage coincides with the complete absence of formation of ampullary electroreceptors. In contrast, the earlier claim of a correlation between a metamorphic loss of the lateral line system and the formation of an auditory nucleus is not supported by more recent data: an auditory nucleus develops in anurans already prior to metamorphosis and is present in all anurans even when they retain the neuromast system. In anurans with a metamorphic loss of the neuromasts, the second order neurons degenerate as well. This independence of the auditory and the second order lateral line nuclei is further substantiated by their separate projection to other brain areas, like the torus semicircularis of the midbrain, and their functional properties.(ABSTRACT TRUNCATED AT 400 WORDS)

Amphibians↗

Central topography of anterior lateral line nerve projections in the channel catfish, Ictalurus punctatus.

Electroreception evolved in the catfishes probably as a specialization of the mechanosensory lateral line system. Fibers of the anterior lateral line nerve in catfishes innervate electrosensory ampullary organs and mechanosensory neuromasts of the head lateral line system. The purpose of this study is to determine the projection patterns of the major principal branches of the ALLN and to investigate the topography within the various nuclei of the terminal fields of these different branches. Fibers of the superficial ophthalmic, buccal and hyomandibular branches of the anterior lateral line nerve terminate in a somatotopic fashion within medullary and cerebellar nuclei. These fibers project to, and terminate within, several discrete nuclei in the medulla and cerebellum, notably the electrosensory lateral line lobe, the medial and caudal octavolateralis nuclei, and portions of a nuclear complex in the cerebellum called the eminentia granularis. Furthermore, the dorsoventral somatotopy in the medullary electrosensory nucleus is a reversed or 'mirror' image of that in the mechanosensory nucleus. This reversed map is similar to that observed in other electrosensory systems and suggests that there may be a common mechanism for the copying and preservation of spatial information as new systems are evolved from primitive sensory pathways.

Afferent Pathways↗