Convergent evolution of the lateral line system in Apogonidae (Teleostei: Percomorpha) determined from innervation

The lateral line system and its innervation were examined in two species of the family Apogonidae (Cercamia eremia [Apogoninae] and Pseudamia gelatinosa [Pseudamiinae]). Both species were characterized by numerous superficial neuromasts (SNs; total 2,717 in C. eremia; 9,650 in P. gelatinosa), including rows on the dorsal and ventral halves of the trunk, associated with one (in C. eremia) and three (in P. gelatinosa) reduced trunk canals. The pattern of SN innervation clearly demonstrated that the overall pattern of SN distribution had evolved convergently in the two species. In C. eremia, SN rows over the entire trunk were innervated by elongated branches of the dorsal longitudinal collector nerve (DLCN) anteriorly and lateral ramus posteriorly. In P. gelatinosa, the innervation pattern of the DLCN was mirrored on the ventral half of the trunk (ventral longitudinal collector nerve: VLCN). Elongated branches of the DLCN and VLCN innervated SN rows on the dorsal and ventral halves of the trunk, respectively. The reduced trunk canal(s) apparently had no direct relationship with the increase of SNs, because these branches originated deep to the lateral line scales, none innervating canal neuromast (CN) homologues on the surface of the scales. In P. gelatinosa, a CN (or an SN row: CN homologue) occurred on every other one of their small lateral line scales, while congeners (P. hayashii and P. zonata) had an SN row (CN homologue) on every one of their large lateral line scales.     

Branching patterns of trunk lateral line nerves in Pleuronectiformes: uniformity and diversity

Branching patterns of the trunk lateral line nerves were studied in 46 pleuronectiform species, representing nine families in two suborders. The dorsal fin longitudinal ramus (DFLR), derived from the main nerve (horizontal septum lateral line nerve), passed closely along the course of the middle trunk lateral line in all specimens examined, the dorsal longitudinal collector nerve (DLCN) partly coalescing with the DFLR along the arched part of the lateral line in Psettodes erumei (Psettodoidei), compared with the entire length of the latter in all other species (Pleuronectoidei). Citharidae, Paralichthyidae, and Pleuronectidae were characterized by having a simple, elongated dorsal ramule; Bothidae was unique in having more than one dorsal ramule, forming a ladder-like network and peripherally giving off numerous minute branches; Poecilopsettidae and Samaridae possessed a few, short dorsal ramules; Soleidae and Cynoglossidae were characteristic in having a dendritic dorsal ramule. Secondary modifications of the course of the middle trunk lateral line were detected by nerve information, the arched part of the lateral line having been secondarily highly elevated in some genera of Pleuronectidae, but secondarily straightened in Samaridae.     

Lateral line system and its innervation in Tetraodontiformes with outgroup comparisons: Descriptions and phylogenetic implications

The lateral line system and its innervation in ten tetraodontiform families and five outgroup taxa were examined. Although some homology issues remained unresolved, tetraodontiforms were characterized by having two types (at least) of superficial neuromasts (defined by the presence or absence of supporting structures) and accessory lateral lines and neuromasts (except Molidae in which “accessory” elements were absent). The preopercular line in Tetraodontiformes was not homologous with that of typical teleosts, because the line was innervated by the opercular ramule that was newly derived from the mandibular ramus, the condition being identical to that in Lophiidae. Within Tetraodontiformes, the number of neuromasts varied between 70 and 277 in the main lines and between 0 and 52 in accessory elements. Variations were also recognized in the presence or absence of the supraorbital commissure, mandibular line, otic line, postotic line, ventral trunk line, and some lateral line nerve rami, most notably the dorsal branch of the opercular ramule, being absent in Aracanidae, Ostraciidae, Tetraodontidae, Diodontidae, and Molidae. Morphological characteristics derived from the lateral line system and its innervation provided some support for a sister relationship of tetraodontiforms with lophiiforms. J. Morphol., 2010. © 2009 Wiley‐Liss, Inc.     

Innervation of the lateral line system in Rhyacichthys aspro: the origin of superficial neuromast rows in gobioids (Perciformes: Rhyacichthyidae)

The lateral line system and its innervation were examined in the most primitive gobioid taxon, Rhyacichthys aspro (Rhyacichthyidae). The infraorbital canal was present, whereas superficial neuromast rows a and c, typically present on the cheek of gobioids, were absent. Because the infraorbital canal (absent in other gobioids) and the two rows were commonly innervated by the buccal ramus, the latter were categorized as replaced rows from canal neuromasts. On an innervation basis, rows b and d on the cheek were considered to comprise superficial neuromasts only in all gobioids. The trunk lateral line system comprised canal and superficial neuromasts, the former being included in the lateral line scales (each bearing 1–7 neuromasts arranged longitudinally along the direction of a groove). Absence of bony roofs in the lateral line system was proposed as a synapomorphy of Gobioidei, and a progressive neotenic shift in the lateral line system of the suborder discussed.     

Peripheral nervous system of the ocean sunfish Mola mola (Tetraodontiformes: Molidae)

Dissection of peripheral nerves in the ocean sunfish Mola mola showed the lateral line system to comprise 6 cephalic and 1 trunk lateral lines, all neuromasts being superficial. The trunk line was restricted to the anterior half of the body, the number of neuromasts (27) being fewer than those previously recorded in other tetraodontiforms. The lateral ramus of the posterior lateral line nerve did not form a “serial collector nerve” along the body. The number of foramina in the neurocranium, serving as passages for the cranial nerves, was fewer than in primitive tetraodontiforms, the reduction being related to modifications in the posterior cranium. Some muscle homologies were reinterpreted based on nerve innervation patterns. The cutaneous branch innervation pattern in the claval fin rays was clearly identical with that in the dorsal and anal fin rays, but differed significantly from that in the caudal fin rays, providing strong support for the hypothesis that the clavus comprises highly modified components of the dorsal and anal fins.     

The innervation of head neuromast rows in eleotridine gobies (Teleostei: Gobioidei)

The innervation of free neuromast (sensory papillae) rows is described from Sihler wholemount preparations of four species of eleotridine gobies, one ( Perccottus glenii ) representing the 'longitudinal' type of neuromast arrangement, the others ( Butis buits, Bostrychus urophthalmus, B. marmoratus ) the 'transverse' arrangement. In the latter, the characteristic transverse cheek rows (1–7) are innervated from the infraorbital trunk of the anterior lateral-line nerve. Longitudinal cheek rows b and d , and the three opercular rows, ot, os and oi , common to all species, are innervated by rami of the hyomandibular trunk of the same nerve. Two neuromast groupings are shown to have a mixed nerve supply. For the median preorbital snout rows, there is innervation from the infraorbital ( s ³ and r ) as well as the supraorbital ( s ¹ and s ²) trunks of the anterior lateral line nerve. The anterior dorsal rows are supplied both by the posterior lateral-line supratemporal ramus (rows g and m ) and the anterior lateral-line supraorbital trunk (rows o and n ). The neuromast rows, under the designations of Sanzo, are tabulated according to innervation and their putative origin in the phyletic replacement of a complete head canal system seen in more generalized percomorph fishes.     

Description and innervation of the lateral line system in two gobioids, <Emphasis Type="Italic">Odontobutis obscura</Emphasis> and <Emphasis Type="Italic">Pterogobius elapoides</Emphasis> (Teleostei: Perciformes)

Components of the lateral line system and their innervation were studied in Odontobutis obscura (Odontobutidae) and Pterogobius elapoides (Gobiidae), which are benthic and pelagic species, respectively. Innervation of the superficial neuromasts constituting the trunk lateral line system by way of three continuous longitudinal series (dorsal, middle, and ventral series: ld, lm, and lv series, respectively) became apparent for the first time. Innervation patterns indicated that the ld and lv series represented a mixture of displaced rows (from lm series) and new additional rows. In O. obscura, the ld and lv series were poorly developed, whereas both series were well developed in the pelagic P. elapoides, possibly as an adaptation to receive stimuli from above and below. Two extremely elongated nerve branches derived from the lateral ramus of the posterior lateral line nerve innervated the ld and lv series, respectively, in P. elapoides. Homologies of the neuromast rows on the head and body were discussed on the basis of their innervation patterns.     

Transplantation of Xenopus laevis Tissues to Determine the Ability of Motor Neurons to Acquire a Novel Target

The evolutionary origin of novelties is a central problem in biology. At a cellular level this requires, for example, molecularly resolving how brainstem motor neurons change their innervation target from muscle fibers (branchial motor neurons) to neural crest-derived ganglia (visceral motor neurons) or ear-derived hair cells (inner ear and lateral line efferent neurons). Transplantation of various tissues into the path of motor neuron axons could determine the ability of any motor neuron to innervate a novel target. Several tissues that receive direct, indirect, or no motor innervation were transplanted into the path of different motor neuron populations in Xenopus laevis embryos. Ears, somites, hearts, and lungs were transplanted to the orbit, replacing the eye. Jaw and eye muscle were transplanted to the trunk, replacing a somite. Applications of lipophilic dyes and immunohistochemistry to reveal motor neuron axon terminals were used. The ear, but not somite-derived muscle, heart, or liver, received motor neuron axons via the oculomotor or trochlear nerves. Somite-derived muscle tissue was innervated, likely by the hypoglossal nerve, when replacing the ear. In contrast to our previous report on ear innervation by spinal motor neurons, none of the tissues (eye or jaw muscle) was innervated when transplanted to the trunk. Taken together, these results suggest that there is some plasticity inherent to motor innervation, but not every motor neuron can become an efferent to any target that normally receives motor input. The only tissue among our samples that can be innervated by all motor neurons tested is the ear. We suggest some possible, testable molecular suggestions for this apparent uniqueness.     

The innervation and adaptive significance of extensively distributed neuromasts in <Emphasis Type="Italic">Glossogobius olivaceus</Emphasis> (Perciformes: Gobiidae)

Components of the lateral line system and their innervation were examined in Glossogobius olivaceus (Gobiidae), with almost all of the trunk scales bearing a row of superficial neuromasts, the latter comprising some 2,900 of the total (ca. 4,800) neuromasts on the body. The relationship between orientation and innervation of the superficial neuromasts on the head showed the buccal and mandibular rami to be clearly separated. On the trunk, the lateral ramus detached a number of branches, typically comprising dorsal, lateral and ventral ramules, to innervate neuromasts. Extensively distributed neuromasts were considered as an adaptation to a nocturnal habit, compensating for reduced vision.     

The trigeminofacial innervation of the cephalic lateral line organs and photophores of the lantern fish Tarletonbeania crenularis (Myctophidae)

The trigeminofacial innervation of the cephalic photophores and lateral line organs of Tarletonbeania crenularis has been studied from gross dissections. The facial and trigeminal roots leave the brainstem separately, but later intermingle forming a trigemino‐facial complex. The seventh nerve gives rise to the hyomandibular trunk and sends a branch rostrad to join the trigeminal forming the supra‐ and infraorbital trunks. The supraorbital trunk innervates the Dn photophore, the snout, the iris, the supraorbital lateral line organs and part of the olfactory sacs. The infraorbital trunk supplies the infraorbital lateral line organs, the Vn photophore and the tissues surrounding the premaxillaries. The hyomandibular trunk passes to the opercular photophores and lateral line organs, and together with a branch from the infraorbital trunk supplies the branchiostegal photophores and lateral line organs of the mandible.     

Morphology of the brain and sense organs in the snailfish Paraliparis devriesi: Neural convergence and sensory compensation on the Antarctic shelf

The Antarctic snailfish Paraliparis devriesi (Liparidae) is an epibenthic species, inhabiting depths of 500–650 m in McMurdo Sound. Liparids are the most speciose fish family in the Antarctic Region. We examine the gross morphology and histology of the sense organs and brain of P. devriesi and provide a phyletic perspective by comparing this morphology to that of four scorpaeniforms and of sympatric perciform notothenioids. The brain has numerous derived features, including well-developed olfactory lamellae with thick epithelia, large olfactory nerves and bulbs, and large telencephalic lobes. The retina contains only rods and exhibits a high convergence ratio (82:1). Optic nerves are small and nonpleated. The tectum is small. The corpus of the cerebellum is large, whereas the valvula is vestigial. The rhombencephalon and bulbospinal junction are extended and feature expanded vagal and spinal sensory lobes as well as hypertrophied dorsal horns and funiculi in the rostral spinal cord. The lower lobes of the pectoral fins have taste buds and expanded somatosensory innervation. Although the cephalic lateral line and anterior lateral line nerve are well developed, the trunk lateral line and posterior lateral line nerve are reduced. Near-field mechanoreception by trunk neuromasts may have been compromised by the watery, gelatinous subdermal extracellular matrix employed as a buoyancy mechanism. The expanded somatosensory input to the pectoral fin may compensate for the reduction in the trunk lateral line. The brains of P. devriesi and sympatric notothenioids share well-developed olfactory systems, an enlarged preoptic-hypophyseal axis, and subependymal expansions. Although the functional significance is unknown, the latter two features are correlated with habitation of the deep subzero waters of the Antarctic shelf. J. Morphol. 237:213–236, 1998. © 1998 Wiley-Liss, Inc.     

Ambiguities in the identification of batoid lateral line systems clarified by innervation

Innervation of the lateral line canal system in seven batoid species (representing seven families in three orders) provided a reliable basis for the identification of each canal element. Previous topographic definitions of the canal elements have failed to recognize homologies within batoids for the scapular and hyomandibular canals. The former is innervated by the posterior lateral line nerve and the latter is innervated by an external mandibular branch of the anterior lateral line nerve. This indicates that the scapular canal is represented only by the scapular loop in Myliobatoidei.     

The lateral line system and its innervation in the boxfish Ostracion immaculatus (Tetraodontiformes: Ostraciidae): description and comparisons with other tetraodontiform and perciform conditions

The lateral line system and its innervation were examined in the ostraciid Ostracion immaculatus (Tetraodontiformes), and compared with those in the triacanthodid Triacanthodes anomalus (Tetraodontiformes) and the acropomatid Malakichthys wakiyae (Perciformes). The carapace of O. immaculatus was composed of 6 cephalic and 2 trunk lateral lines, all neuromasts being categorized as “superficial.” Triacanthodes anomalus was identical with O. immaculatus in the absence of the mandibular line and its innervating ramus, whereas in M. wakiyae the line and ramus were present. All neuromasts were “superficial” in the former two, but “canal” in the latter. Judging from the essentially identical lateral line topography and innervation patterns in all three species, the superficial neuromasts in the two tetraodontiforms were considered to have resulted from replacement of canal neuromasts. The number of neuromasts in the cephalic lateral lines of O. immaculatus (106) and T. anomalus (91) were similar, being significantly higher than in M. wakiyae (30). However, the reverse was true for the trunk lateral lines, the two tetraodontiforms having fewer neuromasts (39 in O. immaculatus, 47 in T. anomalus) compared with M. wakiyae (59).     

Waveform generation of the electric organ discharge inGymnotus carapo

Summary The electric organ (EO) ofGymnotus carapo was studied using different neurohistological techniques including conventional electron microscopy. The electric tissue extends along the fish body from the pectoral girdle to the tip of the tail, constituting a single, undivided organ. However, taking into account the number, arrangement, and innervation of the electrocytes, it is possible to divide the EO into three different portions. The more rostral portion is included within the ventral wall of the abdominal cavity. It consists of singly and doubly innervated electrocytes arranged in two rows at each side of the midline. Innervation of this zone is supplied by the first 5–7 segmental nerves and by the anterior electromotor nerves. Segmental nerves terminate on the rostral faces of doubly innervated electrocytes; axons stemming from the anterior electromotor nerves end on the caudal faces of both doubly and singly innervated electrocytes. There is an intermediate body-tail region in which the electrocytes are arranged in four dorsoventral tubes (tubes 1 to 4) on each side of the midline. In this zone, doubly innervated electrocytes (confined within tube 1) coexist together with singly innervated ones, receiving nerve terminals on their caudal faces (tubes 2, 3, and 4). The innervation characteristics appear modified at more distal portions of the tail where the doubly innervated electrocytes of tube 1 are replaced by singly innervated units. The most distal portion of the EO (approximately its terminal 30%) consists of numerous, homogeneously innervated electrocytes with nerve endings distributed exclusively on their caudal faces. Nerve supply to the intermediate and distal regions derives from the posterior electromotor nerves (PENs) which appear as well-defined anatomical entities beyond the level of metamere XXVII. At the bodytail and more distal regions the innervation pattern of the EO is particularly complex. Thin nerve trunks arise from the PENs and project ventrally toward the electrocyte tubes. Before reaching the electric tissue the electromotor axons branch frequently. Our anatomical studies indicate that the EO is heterogeneous, a feature consistent with most recent electrophysiological and biophysical experiments.Abbreviations AEN anterior electromotor nerve - EMN electromotoneurons - EO electric organ - EOD electric organ discharge - LLN lateral line nerve - PEN posterior electromotor nerve     

The lateral line system and its innervation in <Emphasis Type="Italic">Lateolabrax japonicus</Emphasis> (Percoidei <Emphasis Type="Italic">incertae sedis</Emphasis>) and two apogonids (Apogonidae), with special reference to superficial neuromasts (Teleostei: Percomorpha)

The lateral line system and its innervation were examined in a generalized perch-like species, Lateolabrax japonicus (Percoidei incertae sedis), and compared with those in two species of Apogonidae (Fowleria variegata in Apogonichthyini and Ostorhinchus doederleini in Ostorhinchini) characterized by proliferated superficial neuromasts (SNs) on the head, trunk lateral line scales and caudal fin. The total number of SNs differed greatly between the two groups, being 271 in the former, and 2,403 and 4,088 in the latter. The mandibular ramus (MDR) was extensively ramified in the head of the apogonids, with three additional branches that were absent in L. japonicus, innervating 1,117 SNs in F. variegata and 1,928 in O. doederleini. In the apogonids, the additional anterodorsal branch of the MDR coursed parallel to the buccal ramus anteriorly (on the interorbital space) and to the supratemporal ramus posteriorly (on the temporal region). The two parallel portions supplied numerous SN rows forming a characteristic crosshatch pattern, the branch and two rami distributing to transverse and longitudinal rows, respectively. In the two groups, the trunk lateral line scales each housed a canal neuromast (CN; partly replaced by an SN in F. variegata). In addition, one to four (in L. japonicus) and three to 55 (in the apogonids) SNs occurred on each lateral line scale, the pattern of SN innervation being identical in having two types of branches; one innervated a CN and SNs, and the other SN(s) only. The latter type extended only to a limited number of scales in L. japonicus, but to nearly all or all scales in the apogonids. Compared with F. variegata, branches of the respective types were more finely ramified with greater number of SNs in O. doederleini.     

Activity of lateral line efferents in the axolotl (Ambystoma mexicanum)

Summary Activity of efferent fibers was recorded from the ramus ophthalmicus superficialis of the head lateral line nerve and the ramus medialis of the trunk lateral line nerve of the axolotl Ambystoma mexicanum. Baseline activity and activity evoked by sensory stimuli were examined. Electrical stimulation of selected branches was used to determine the conduction velocity and the branching pattern of efferent fibers. The influence of lesions at different levels in the CNS on efferent activity was studied.Up to 5 units with baseline activity were found in a single ramus of the lateral line nerve. Discharge rates were variable and highly irregular; they differed between units of the same branch. Bursting activity occurred in 62% of the units. Movements of the animal were accompanied by activity in up to 8 efferent units in a single nerve.Efferent activity could be elicited or modified by stimulation of visual, labyrinthine, somatosensory, and lateral line systems. Stimulation of the electrosensory system had no effect. Individual efferent neurons innervated different fields in the lateral line periphery. Conduction velocities of efferent fibers ranged from 5 to 12 m/s.Efferent units received input from various sources at different brain levels up to the diencephalon. These in puts determined the baseline activity. The mechanosensory input was mediated at the medullary level.Abbreviations r.m. ramus medialis - r.o.s. ramus ophthalmicus superficialis - r.s. ramus superior     

Innervation and cytochemistry of the neuroepithelial bodies in the ciliated epithelium of the toad lung (Bufo marinus)

Summary Neuroepithelial bodies (NEB) were identified in the lung of Bufo marinus. The characteristics of the cells and their innervation were studied with electron and fluorescence microscopy before and after close vagosympathetic denervation. The bodies consist of low columnar cells which rest on the epithelial basal lamina. The majority of the cells do not reach the lumen of the lung (basal cells); the few which do (apical cells) are bordered by microvilli and possess a single cilium. The neuroepithelial cell cytoplasm contains a variety of organelles the most characteristic of which are dense cored vesicles. Microspectrofluorometry and electron microscopic cytochemistry indicate significant quantities of 5-hydroxytryptamine in these cells. The neuroepithelial bodies could be divided into three groups on the basis of their innervation: 1) About 60% of the NEBs are innervated solely by nerve fibres containing agranular vesicles which form reciprocal synapses; 2) about 20% are innervated solely by adrenergic nerve fibres which form distinct synaptic contacts; and 3) the remaining 20% are innervated by both types of nerve fibres. It is proposed that the NEBs are receptors monitoring intrapulmonary P_{CO 2} and so leading to modulation of activity in afferent nerve fibres (type containing agranular vesicles). The presence of NEBs solely with an adrenergic (efferent) innervation poses a problem with this interpretation.     

Morphology and function of the lateral line of juvenile steelhead trout in relation to gas-bubble disease*

General morphology of the lateral line of juvenile steelhead trout, Salmo gairdneri, is described. Through electrophysiological monitoring of individual nerve fibres, control patterns for spontaneous activity and reaction to sensory receptor stimulation were established. Spontaneous activity has a positive correlation with temperature and number of receptors innervated. Presence of directional sensitivity and response to near field water displacement at different frequencies is similar to that found in other fishes and amphibians. Normal lateral line response to a standardized set of stimuli was compared with the response of fish affected by gas-bubble disease. Results show that as gas emboli formed in the scale pockets of the trunk lateral line of stressed fish, the ability to respond to stimuli was either diminished or completely disappeared. Further testing demonstrated that this sensory loss was reversible and that upon return to equilibrated water gas emboli disappeared and normal function was regained. This sublethal effect of gas-bubble disease on the lateral line sensory system may be an important element contributing to indirect mortality.     

Homologies of cephalic lateral line canals in <Emphasis Type="Italic">Pseudorhombus pentophthalmus</Emphasis> and <Emphasis Type="Italic">Engyprosopon grandisquama </Emphasis>(Pleuronectiformes): innervation and upper eye floor formation

Cephalic lateral line canals in two pleuronectiforms, Pseudorhombus pentophthalmus (Paralichthyidae) and Engyprosopon grandisquama (Bothidae), were studied and their homologies between the ocular and blind sides assessed on the basis of position and innervation patterns. A blind side canal, comprising small ossicles in a line lateral to the upper eye floor, was confirmed as the infraorbital line because the canal was not innervated by a ramus associated with the upper nasal (i.e., the superficial ophthalmic ramus innervating the supraorbital line). Consequently, the ramus innervating the canal was identified as the buccal ramus (associated with the infraorbital line). The blind side frontal forming the posterior half of the upper eye floor was identified as that part bearing the anteriormost otic canal in the ocular side, hypertrophy of the blind side component being evident. The supraorbital line of the blind side was represented by the upper nasal only in E. grandisquama.