The fine structure of the lateral-line organs of larval Ichthyophis (Amphibia: Gymnophiona)

Light and electron microscopic observations of the lateral-line organs of larval Ichthyophis kohtaoensis confirmed earlier reports of the occurrence of two different types of lateral-line organs. One type, the ampullary organ, possesses 15–26 egg-shaped sensory cells. Each sensory cell extends a single kinocilium surrounded by a few microvilli into the ampullary lumen. This is in contrast to the ampullary organs of urodele amphibians that contain only microvilli. The second type of organ, the ordinary neuromast, has 15–24 pear-shaped sensory cells arranged in two to three rows. Each sensory cell shows a kinocilium that is asymmetrically placed with respect to both a basal plate and approximately 60 stereovilli. The sensory cells of ampullary organs are always separated by supporting cells; those of neuromasts are occasionally in contact with one another. Numerous (neuromasts) or few (ampullary organs) mantle cells separate the organs from the epidermal cells. Only afferent synapses are found in the ampullary organs whereas vesicle-filled fibers together with afferent nerve terminals are found in neuromasts. Both organs contain similarly sized presynaptic spheres adjacent to the afferent fibers. It is suggested that the neuromasts have a mechanoreceptive function, whereas the ampullary organs have an electroreceptive one.     

Some evidence for the ampullary organs in the European cave salamander Proteus anguinus (Urodela,Amphibia)

Summary The multicellular epithelial organs in Proteus anguinus, which Bugnion (1873) assumed to be developing neuromasts, have been analyzed by lightand electron-microscopy. Their fundamental structure consists of single ampullae with sensory and accessory cells with apical parts that extend into the pit of the ampulla, and of a short jelly-filled canal connecting the ampulla pit with the surface of the skin. The organs are located intra-epithelially and are supported by a tiny dermal papilla. The cell elements of sensory epithelium are apically linked together by tight junctions. The free apical surface of the sensory cell bears several hundred densely packed stereocilia-like microvilli whereas the basal surface displays afferent neurosensory junctions with a pronounced round synaptic body. The compact uniform organization of the apical microvillous part shows a hexagonal pattern. A basal body was found in some sensory cells whereas a kinocilium was observed only in a single cell. The accessory cells have their free surface differentiated in a sparsely distributed and frequently-forked microvilli. The canal wall is built of two or three layers of tightly coalescent flat cells bordering on the lumen with branching microvilli. The ultrastructure of the content of the ampulla pit is presented.In the discussion stress is laid on the peculiarities of the natural history of Proteus anguinus that support the view that the morphologically-identified ampullary organs are electroreceptive. The structural characteristics of ampullary receptor cells are dealt with from the viewpoint of functional morphology and in the light of evolutionary hypotheses of ampullary organs.     

The lorenzinian ampullae of Polyodon spathula

Summary Light and electron microscopic observations on the ampullary organs of Polyodon spathula (Chondrostei, Osteichthyes) reveal a sensory epithelium similar to that found in the Lorenzinian ampulla, an electroreceptor found in marine Elasmobranchs.The sensory cells have a very small luminal part provided with a cilium. They are innervated by many nerve endings. Each nerve fibre apparently makes synaptic contact with several sensory cells. The synaptic structure in the sensory cell is composed of a flat sheet, the outermost part of which is surrounded by 3 or 4 annuli of densely staining material. The sheet extends into a protrusion of the sensory cell, and there is a corresponding invagination in the nerve terminal.The conclusion that these organs are electroreceptors, is supported by the finding that the fish responds to the introduction of an iron tube in the aquarium, whereas a wooden rod introduced in the same way causes no response.     

The organization of ampullary sense organs in the electric fish, Gymnarchus niloticus

Three types (A, B, and C) of ampullary sense organs occur in the skin of Gymnarchus niloticus. In type A the ampulla is connected to the surface of the skin by an open duct whereas in B and C organs it is closed, though overlain by specialized epidermal cells. In each case the receptor cell surface in contact with the ampullary lumen bears microvilli; these are more highly developed in B and C organs than in type A. Fine structural observations are consistent with the view that the organs are electric receptors of three different types.     

Fine Structure of the Ampullary Organs of the Bichir Polypterus senegalus Cuvier, 1829 (Pisces: Brachiopterygii) With Some Notes on the Phylogenetic Development of Electroreceptors

The ampullary organs of the bichir were examined by light and electron microscopy. Unlike most other ampullary organs, they are exclusively found in the epidermis and are never sunk into the subepidermal connective tissue. The sensory epithelium consists of sensory cells and supporting cells surrounded by mantle cells. The luminal surface of the sensory cell is provided with a cilium surrounded by several microvilli. In the apical cytoplasm are found numerous mitochondria and microtubules. In the basal part of the cell synaptic sheets or synaptic bodies opposite to afferent nerve endings are frequent.     

Morphology of the ampullae of Lorenzini in juvenile freshwater Carcharhinus leucas

Ampullae of Lorenzini were examined from juvenile Carcharhinus leucas (831–1,045 mm total length) captured from freshwater regions of the Brisbane River. The ampullary organ structure differs from all other previously described ampullae in the canal wall structure, the general shape of the ampullary canal, and the apically nucleated supportive cells. Ampullary pores of 140–205 µm in diameter are distributed over the surface of the head region with 2,681 and 2,913 pores present in two sharks that were studied in detail. The primary variation of the ampullary organs appears in the canal epithelial cells which occur as either flattened squamous epithelial cells or a second form of pseudostratified contour‐ridged epithelial cells; both cell types appear to release material into the ampullary lumen. Secondarily, this ampullary canal varies due to involuted walls that form a clover‐like canal wall structure. At the proximal end of the canal, contour‐ridged cells abut a narrow region of cuboidal epithelial cells that verge on the constant, six alveolar sacs of the ampulla. The alveolar sacs contain numerous receptor and supportive cells bound by tight junctions and desmosomes. Pear‐shaped receptor cells that possess a single apical kinocilium are connected basally by unmyelinated neural boutons. Opposed to previously described ampullae of Lorenzini, the supportive cells have an apical nucleus, possess a low number of microvilli, and form a unique, jagged alveolar wall. A centrally positioned centrum cap of cuboidal epithelial cells overlies a primary afferent lateral line nerve. J. Morphol. 276:481–493, 2015. © 2014 Wiley Periodicals, Inc.     

Ultrastructure of the ampullae of Lorenzini of <Emphasis Type="Italic">Aptychotrema rostrata</Emphasis> (Rhinobatidae)

Small epidermal pores of the electrosensory ampullae of Lorenzini located both ventrally and dorsally on the disk of Aptychotrema rostrata (Shaw and Nodder, 1794) open to jelly-filled canals, the distal end of which widens forming an ampulla that contains 6 ± 0.7 alveolar bulbs (n = 13). The sensory epithelium is restricted to the alveolar bulbs and consists of receptor cells and supportive cells. The receptor cells are ellipsoid and their apical surfaces are exposed to the alveolar lumen with each bearing a single central kinocilium. Presynaptic bodies occur in the basal region of the receptor cell immediately proximal to the synaptic terminals. The supportive cells that surround receptor cells vary in shape. Microvilli originate from their apical surface and extend into the alveolar lumen. Tight junctions and desmosomes connect the supportive cells with adjacent supportive and receptor cells in the apical region. The canal wall consists of two cell layers, of which the luminal cells are squamous and interconnect via desmosomes and tight junctions, whereas the cells of the deeper layer are heavily interdigitated, presumably mechanically strengthening the canal wall. Columnar epithelial cells form folds that separate adjacent alveoli. The same cells separate the ampulla and canal wall. An afferent sensory nerve composed of up to nine myelinated nerve axons is surrounded by several layers of collagen fibers and extends from the ampulla. Each single afferent neuron can make contacts with multiple receptor cells. The ultrastructural characteristics of the ampullae of Lorenzini in Aptychotrema rostrata are very similar to those of other elasmobranch species that use electroreception for foraging.     

Ultrastructure of the ampullary organs of Plicofollis argyropleuron (Siluriformes: Ariidae)

The morphology of ampullary organs in Plicofollis argyropleuron, collected from a southeast Queensland estuary, was examined by light and electron microscopy to assess the morphological characteristics of teleost ampullary organs in environments with fluctuating salinities. This catfish possesses both macroampullae and microampullae. Both have the typical teleost arrangement of an ampullary pore linked by a canal to a single ampulla that is lined with receptor and supportive cells. The canal wall of macroampullae consists of a collagen sheath, a basement membrane, and two layers of squamous epithelial cells adjacent to the lumen, joined by desmosomes and tight junctions near the surface of the epithelium. Ampullary pore diameters are similar in range for both the macroampullae and the microampullae, with microampullae always arising from the larger pores within a single region of the head. Canal length of the macroampullae is longer than those of the microampullae. Macroampullae also contain approximately 10 times as many receptor cells compared with the microampullae. In both organs, these pear‐shaped receptor cells alternate with supportive cells along the entire luminal surface of the ampulla. The apical region of receptor cells extends into the lumen and bears numerous microvilli. The basal region of receptor cells adjoins to either individual or multiple unmyelinated neural terminals. The coexistence of two markedly different ampullary organ morphologies within a single species support theories concerning the possible multifunctionality of these sensory organs. J. Morphol., 276:1405–1411, 2015. © 2015 Wiley Periodicals, Inc.     

Special cutaneous receptor organs of fish. IV. Ampullary organs of the nonelectric catfish, Kryptopterus

Ampullary organs of the transparent catfish, Kryptopterus bicirrhus, are present in large numbers on the head and in a regular pattern of lines on the body and fins. The organs lie in the epidermis, and have a pore that opens to the surface. Flattened cells form a roof and walls. On the floor of the organ there are a “sensory hillock,” composed of spherical receptor cells and columnar supporting cells, and a “secretory hillock” composed of columnar secretory cells. The receptor cells are nonciliated and have only afferent innervation. The organ cavity is filled with jelly. The organs are compared with ampullary organs of the weakly electric fish Eigenmannia, ampullae of Lorenzini of Raja, and small pit organs of Amiurus. Structural characteristics of the ampullary organs of Kryptopterus make them especially suitable for electrophysiological studies.     

Distribution and morphology of the ampullary organs of the estuarine long-tailed catfish, <Emphasis Type="Italic">Euristhmus lepturus</Emphasis> (Plotosidae,Siluriformes)

Ampullary organs of Euristhmus lepturus occur in high densities along the head and in four parallel pathways along the trunk of the body. Large ampullary pores (125–130 μm) are easily distinguishable from other sensory epithelial pores due to the differences in size and the presence of a collar-like structure. Simple, singular ampullary organs of the head region consist of an ampullary pore connected to a long canal with a diameter of 115–175 μm before terminating as a simple ampulla with an external diameter of 390–480 μm. The ampullary canal is composed of 1–2 layers of flattened squamous epithelial cells, the basement membrane and an interlocking collagen sheath. The innermost cells lining the canal wall are adjoined via tight junctions and numerous desmosomes, as are those of the receptor and supportive cells. Canal wall tissue gives rise to a sensory epithelium containing between 242 and 285 total receptor cells, with an average diameter of 11.7 ± 5.3 μm, intermixed with medially nucleated supportive cells. Each receptor cell (21.38 ± 4.41 μm, height) has an apically positioned nucleus and a luminal surface covered with numerous microvilli. Neural terminals abut the basal region of receptor cells opposite multiple presynaptic bodies and dense mitochondria. Supportive cells extend from the ampullary lumen to the basement membrane, which is adjacent to the complex system of collagen fibres.     

Anti-tubulin labeling reveals ampullary neuron ciliary bundles in opisthobranch larvae and a new putative neural structure associated with the apical ganglion

This investigation examines tubulin labeling associated with the apical ganglion in a variety of planktotrophic and lecithotrophic opisthobranch larvae. Emphasis is on the ampullary neurons, in which ciliary bundles within the ampulla are strongly labeled. The larvae of all but one species have five ampullary neurons and their associated ciliary bundles. The anaspid Phyllaplysia taylori, a species with direct development and an encapsulated veliger stage, has only four ampullary neurons. The cilia-containing ampulla extends to the pretrochal surface via a long, narrow canal that opens to the external environment through a very small pore (0.1 microm diameter). Cilia within the canal were never observed to project beyond the opening of the apical pore. The ampullary canals extend toward and are grouped with the ciliary tuft cells and remain in this location as planktotrophic larvae feed and grow. If, as has been reported, the ciliary tuft is motile, the pores may be continually bathed in fresh seawater. Such an arrangement would increase sensitivity to environmental chemical stimuli if the suggested chemosensory function of these neurons is correct. In general, ciliary bundles of newly hatched veligers are smaller in planktotrophic larvae than in lecithotrophic larvae. In planktotrophic larvae of Melibe leonina, the ciliary bundles increase in length and width as the veligers feed and grow. This may be related to an increase in sensitivity for whatever sensory function these neurons fulfill. An unexpected tubulin-labeled structure, tentatively called the apical nerve, was also found to be associated with the apical ganglion. This putative nerve extends from the region of the visceral organs to a position either within or adjacent to the apical ganglion. One function of the apical nerve might be to convey the stimulus resulting from metamorphic induction to the visceral organs.     

Fine structure and histochemistry of the ampullary organ of the urodele amphibian Pleurodeles

A morphological study by light and electron microscopy on the lateral line system of the urodele amphibian Pleurodeles waltii demonstrates the presence of sensory organs other than neuromasts in the head. From their morphology, they have been called ampullary organs. The ampullary organs occur in the bottom of a groove and consist of three different types of cells: sensory, supporting and mantle cells. Histochemical analysis indicates that the last two are secretory cells, probably involved in the production of the material filling the ampulla and the groove.     

Ampullary organ morphology of freshwater salmontail catfish, Arius graeffei

Two types of ampullary organs are present in the skin of the freshwater salmontail catfish, Arius graeffei, each consisting of a short canal (0.2-0.5 mm) oriented perpendicular to the basement membrane and ending in an ampulla. Histochemical staining techniques (Alcian blue and Lillie's allochrome) indicate that the ampullary canals contain an acidic mucopolysaccharide gel, which is uniform in its staining properties along the canals. Type II ampullary organs consist of a canal, the wall of which is lined with cuboidal epithelial cells. The canal opens into an ampulla with 50-60 receptor cells. Electron microscopy reveals that the pear-shaped receptor cells bear microvilli on their luminal surface and lie adjacent to an unmyelinated neuron. Type III ampullary organs differ from Type II in that the canal wall consists of cells that possess a protein-rich sac at the luminal apex and have a polymorphic nucleus. The canals of Type III ampullary organs open to an ampulla with 8-30 receptor cells similar in both staining properties and structure to those of the Type II organ. In both types of ampullary organs, supportive cells surround each receptor cell except at the apex of the receptor cell.     

Morphology of the teleost ampullary organs in marine salmontail catfish Neoarius graeffei (Pisces: Ariidae) with comparative analysis to freshwater and estuarine conspecifics

We hypothesized that due to the relative conductivity of the environment, and to maintain sensory function, ampullary organs of marine Neoarius graeffei would differ morphologically from those described previously for estuarine and freshwater conspecifics. Unlike the ampullary systems of N. graeffei from freshwater and estuarine habitats, the ampullary pores of marine specimens occur in two distinct patterns; numerous pores seemingly randomly scattered on the head and ventro‐lateral regions of the body, and pores arranged in distinctive vertical lines above the lateral line on the dorso‐lateral body of the fish. Light and electron microscopy revealed that the ampullary organs also differed morphologically from estuarine and freshwater specimens in the presence of longer ampullary canals, a hitherto unreported canal wall composition, and in the collagen sheath surrounding both the canal and the ampulla proper within dermal connective tissues. Ampullary pores were wider in marine individuals and opened to the longest ampullary canals reported for this species. The canal wall was lined by cuboidal and squamous epithelial cells. Each ampullary canal opened into a single ampulla proper containing significantly more receptor cells than estuarine and freshwater conspecifics. The distribution of ampullary pores as well as the microstructure of the ampullary organs indicates that the electrosensory system of marine N. graeffei differs from those of estuarine and freshwater specimens in ways that would be expected to maintain the functionality of the system in a highly conductive, fully marine environment, and reveals the remarkable plasticity of this species’ ampullary system in response to habitat conductivity. J. Morphol. 276:1047–1054, 2015. © 2015 Wiley Periodicals, Inc.     

Developmental origin of shark electrosensory organs

Vertebrates have evolved electrosensory receptors that detect electrical stimuli on the surface of the skin and transmit them somatotopically to the brain. In chondrichthyans, the electrosensory system is composed of a cephalic network of ampullary organs, known as the ampullae of Lorenzini, that can detect extremely weak electric fields during hunting and navigation. Each ampullary organ consists of a gel-filled epidermal pit containing sensory hair cells, and synaptic connections with primary afferent neurons at the base of the pit that facilitate detection of voltage gradients over large regions of the body. The developmental origin of electroreceptors and the mechanisms that determine their spatial arrangement in the vertebrate head are not well understood. We have analyzed electroreceptor development in the lesser spotted catshark (Scyliorhinus canicula) and show that Sox8 and HNK1, two markers of the neural crest lineage, selectively mark sensory cells in ampullary organs. This represents the first evidence that the neural crest gives rise to electrosensory cells. We also show that pathfinding by cephalic mechanosensory and electrosensory axons follows the expression pattern of EphA4, a well-known guidance cue for axons and neural crest cells in osteichthyans. Expression of EphrinB2, which encodes a ligand for EphA4, marks the positions at which ampullary placodes are initiated in the epidermis, and EphA4 is expressed in surrounding mesenchyme. These results suggest that Eph-Ephrin signaling may establish an early molecular map for neural crest migration, axon guidance and placodal morphogenesis during development of the shark electrosensory system.     

Ampullary organs and electroreception in freshwater Carcharhinus leucas.

The ampulla of Lorenzini of juvenile Carcharhlinus leucas differ histologically from those previously described for other elasmobranchs. The wall of the ampullary canal consists of protruding hillock-shaped epidermal cells that appear to secrete large quantities of a mucopolysaccharide gel. The ampullary organs comprise a long canal sheathed in collagen terminating in an ampulla. Each ampulla contains six alveolar sacs, with each sac containing hundreds of receptor cells. The receptor cells are characteristic of others described for elasmobranchs being pear-shaped cells with a central nucleus and bearing a single kinocilium in the exposed apical region of the cell. The supportive cells differ from general elasmobranch ampullary histology in that some have an apical nucleus. These ampullary structures allow Carcharhinus leucas to detect and respond to artificial electrical fields. Carcharhinus leucas from freshwater habitats respond to electrical signals supplied in freshwater aquaria by abruptly turning towards low voltage stimuli (< or = 10 microA) and either swimming over or biting at the origin of the stimulus.     

Special cutaneous receptor organs of fish: The tuberous organs of Eigenmannia

The special cutaneous receptor organs of the fresh water weakly electric fish have previously been proposed to be electroreceptors. In the gymnotid, E. virescens, two types of special cutaneous receptor organs, ampullary and tuberous, are distinguished from each other, as well as from the ordinary lateral line receptor organs, by their characteristic distribution and size. The tuberous organs usually contain 25 to 35 elongate nonciliated receptor cells within a cellular capsule. A single layer of supporting cells is present between the base of the receptor cells and the base of the capsule. A single thin myelinated nerve fiber innervates each group of organs and branches so that the base of each receptor cell is supplied with a single nerve ending. Synaptic contact is made at many points on each nerve ending. The synapses are characterized by fingers of receptor cell cytoplasm which contain dense presynaptic rods. The organ capsule is open toward the surface of the fish. A cellular plug partly obscures the opening, but continuity is maintained between the intracapsular fluid and the external water. Microvilli, projecting from the surfaces of the receptor cells, maintain an open gap between adjacent receptor cells. About 95% of the surface area of these cells is therefore in contact with the fluid. The functional implications of some of the ultrastructural observations are discussed.     

The Morphology of the Lorenzinian Ampullae of the Sturgeon Acipenser ruthenus (Pisces: Chondrostei)

Jørgensen, J. M. 1980. The morphology of the Lorenzinian ampullae of the sturgeon Acipenser ruthenus (Pisces: Chondrostei). (Zoological Laboratory, University of Aarhus, Denmark.) — Acta zool. (Stockh.) 61 (2): 87–92. The snout of a sturgeon, Acipenser ruthenus (Chondrostei, Osteichthyes) is provided with sensory pores. Light and electron microscopical examination of these reveals that the ampullary organs have a sensory epithelium very similar to what has been found in the Lorenzinian ampullae, which are electroreceptors previously examined at a fine structural level in elasmobranchs and the paddle-fish, Polyodon spathula. The sensory cells are pear-shaped with a very small apical part, in the centre of which there is a short cilium. Basally, the sensory cells make several contacts with button-shaped nerve-endings. The presumed synaptic area in the sensory cell is characterized by a presynaptic sheet surrounded by vesicles. Only one type of nerve ending, an afferent type, has been observed.     

Chemosensory integration in the spiny lobster: Ascending activity in the olfactory-globular tract

Summary In the frog,Rana esculenta, when the influence of the efferent vestibular system was eliminated, the spontaneous activity of single afferent fibres recorded from one branch of the nerve of the horizontal semicircular canal (HC) or of the nerve of the vertical anterior canal (VAC) was inhibited in 16–17% of the cases when stimulating electrically the other branch of the same ampullary nerve. Moreover, the spontaneous activity of about 200 afferent fibres was recorded from the nerves of the HC and VAC in three experimental situations. In the first one, the brain was destroyed, or the left vestibular nerve cut as it enters the brain stem, and all the branches of the left vestibular nerve were cut except for the one recorded (VAC or HC nerve); in the second one, recordings were made on the peripheral end of the ampullary nerve previously cut near the ampulla; in the third situation they were made on the ampullary nerve after having cut the vestibular nerve between the periphery and Scarpa's ganglion close to Scarpa's ganglion. Statistical comparisons of the distribution of the spontaneous frequencies and of the mean activities between the experimental situations show that the activities were greater in the second or third experimental situations than in the first one. These results could be explained by the existence of an inhibitory feedback loop outside the brain including Scarpa's ganglion and mediated by receptor-receptor fibres.Abbreviations HC horizontal semicircular canal - PE peripheral end of the ampullary nerve - VAC vertical anterior semicircular canal This research was supported by a grant from D.G.R.S.T. (Aide à la Recherche n 77.7.1127)     

Immunohistochemical identification of substance P in cutaneous sensory organs (electroreceptors) of gymnotid teleost fish

Summary The distribution of the neuropeptide substance P, which is considered to be a neurotransmitter or neuromodulator of the central nervous system, has been studied in the cutaneous electroreceptor organs (tuberous and ampullary organs) of 3 species of gymnotid fish: Apteronotus leptorhynchus, Eigenmannia virescens and Sternopygus sp. Immunohistochemical data have revealed that substance P is never present in the afferent fibers but is specifically localized in the electroreceptors of the three species examined. Substane P immunoreactivity is strictly localized in the sensory cells of the ampullary organs of all three species and in those of the tuberous organs of Apteronotus leptorhynchus and Sternopygus sp. In contrast, weak substance P immunoreactivity was observed only in certain tuberous sensory cells of Eigenmannia. Substance P immunoreactivity was also found in the accessory cells of certain organs: it was detected in the two types of accessory cells of the tuberous organs of Eigemmannia virescens, in the accessory cells type 2 of the tuberous organs of Sternopygus sp., and in all accessory cells of ampullary organs of Sternopygus sp. and Apteronotus leptorhynchus. In Sternopygus sp., positive staining was only evident if the substance P antibody was used at low concentration. Immunoreactivity for substance P in the sensory cells suggests that it has a transmitter or modulator function in these electroreceptors; the presence of substance P in the accessory cells remains to be explained.