Pharmacological evidence for the involvement of the cAMP cascade in sensory fatigue in Drosophila

Summary We have investigated the effect of systemic treatment with drugs that affect the cAMP cascade on the sensory response and sensory fatigue in an identified mechanosensory neuron of Drosophila. Forskolin, an activator of adenylate cyclase, decreases the sensory response of the neuron. H7, an inhibitor of protein kinase, inhibits sensory fatigue. Octopaminergic ligands facilitate sensory fatigue. These results, together with our previous neurogenetic analysis of sensory fatigue in Drosophila (Corfas and Dudai 1990), corroborate the hypothesis that the cAMP cascade is involved in the generation and modulation of sensory fatigue.Abbreviations ANP antero-notopleural (neuron) - CDMF chlordimeform - ISI interstimulus interval     

Antennal receptors in the blowfly Calliphora erythrocephala: II. Fine structure of the large pedicellar campaniform sensillum

A large mechanosensory campaniform sensillum (LCS) is found close to the flagellum/pedicellus joint in the antennae of the blowfly Calliphora erythrocephala. The LCS possesses a single sensory cell, enveloping cells and a cuticular stimulus-conducting structure. The distal part of the sensory process is developed as a tubular body and is connected to the two parts of the stimulusconducting apparatus. The sensory cell is characterized by the complete absence of ciliary structures in the transition zone between dendrite and sensory process.     

Molecular neurogenetics of chemotaxis and thermotaxis in the nematode Caenorhabditis elegans

Chemotaxis and thermotaxis in Caenorhabditis elegans are based on the chemical senses (smell and taste) and the thermal sense, respectively, which are important for the life of the animal. Laser ablation experiments have allowed identification of sensory neurons and some interneurons required for these senses. Many mutants that exhibit various abnormalies have been isolated and analyzed. These studies have predicted novel signaling pathways whose components include a putative odorant specific transmembrane receptor (ODR-10) and a cyclic nucleotide-gated channel (TAX-4/TAX-2) functioning in taste and thermosensation as well as in smell. The emerging picture of the mechanisms of sensory transduction in C. elegans seems to be basically similar to what is known of visual and olfactory sensory transduction in vertebrates. Thus, molecular and cellular analyses of chemotaxis and thermotaxis in C. elegans have proved useful and will continue to provide significant implications for the molecular basis of sensory systems in higher animals.     

Sensory cell degeneration in the ontogeny of the chemosensitive sensilla in the labial palp-pit organ of the butterfly,Pieris rapae L. (Insecta,Lepidoptera)

Summary The ontogeny of the chemoreceptive sensilla in the labial palp-pit organ was studied in Pieris rapae by examining twelve successive stages between pupation and emergence of the imago, which takes a period of 160 h under the experimental conditions. Mitoses occur until 20 h after pupation. They lead to anlagen of sensilla, 91% of which are comprised of three sensory cells. However, two sensory cells degenerate in each sensillum during a period of 28 h. The same process occurs in anlagen with four sensory cells resulting in bicellular sensilla. Axons grow out only after the number of sensory cells has been reduced. Further consecutive steps in sensory cell differentiation are: (a) outgrowth of dendritic outer segment and dendrite sheath; (b) outgrowth of trichogen process and change in structure of elongating dendrite sheath; (c) deposition of cuticle and pore tubules in the pegs; (d) retraction of trichogen process; (e) increase in diameter of dendritic outer segment accompanied by increase of microtubule number and appearance of regularly spaced electron-dense bodies at tubular doublets; (f) branching of dendritic outer segment; and (g) transformation of the dendritic branches into curled lamellae and partial destruction of the dendrite sheath. The unique process of sensory cell degeneration is interpreted as an event that revokes a step towards a possible functional improvement of the labial palp-pit organ during further evolutionSupported by the Deutsche Forschungsgemeinschaft (SFB 4/G1)     

Ultrastructure of the sensory palps ofTetranchyroderma papii (Gastrotricha,Macrodasyida)

Summary The sensory palps of the macrodasyoid gastrotrichTetranchyroderma papii contain processes from two types of cell: 22–23 bipolar primary sensory cells and two to three support cells. In the proximal region of the palp each sensory cell contains a short ciliary segment with a basal body and from this ciliary segment a longer distal segment lacking axonemal microtubules extends through the major part of the length of the palp. Each support cell process bears microvilli and contains a conspicuous bundle of microtubules running the entire length of the process. The cell bodies of both cell types are situated in the epidermis of the head region. The palps are interpreted as having a chemosensory function. They are considered to be homologous to the posterior cephalic sensory organ ofTurbanella cornuta, but not the head tentacles ofChordodasys antennatus or nematode amphids.     

Sensory endings of the ascidian static organ (Chordata,Ascidiacea)

Summary The ultrastructure of the static organ is examined in larvae of Diplosoma macdonaldi, a colonial ascidian, and Styela plicata, a solitary ascidian; the results are similar. As previous workers found, the cell body of a unicellular statocyte lies in the lumen of the sensory vesicle and contains the statolith. A narrow neck connects the cell body to an anchoring foot in the floor of the sensory vesicle. Two previously undescribed sensory endings project into the lumen just to the left of the statocyte, one anterior and one posterior to the neck. A network of fine processes from each ending contacts the statocyte body. It is proposed that movements of the statocyte cell body are detected by these endings. They arise from neurons in the ventral wall of the sensory vesicle that project axons to the visceral ganglion. The placement of the sensory endings may allow discrimination of the directon of statocyte deflection.Abbreviations ax axons - bb ciliary basal body - bl basal lamina - c cilium - cr striated ciliary rootlet - ec ependymal cells - en endoderm - h hemocoel - ly lysosome - mv microvilli - n neuron - nf neurofilaments - ns neck of the statocyte - sb statocyte cell body - sd sensory dendrite - sn sensory neuron - sp sensory processes - stf statocyte foot - svl sensory vesicle lumen - zo zonula occludens     

Immunolabeled neuroactive substances in the osphradium of the pond snail Lymnaea stagnalis

The osphradium of molluscs is assumed to be a sensory organ. The present investigation in Lymnaea stagnalis has established two ultrastructurally different types of dendrites in the sensory epithelium. Cells immunoreactive to leucine-enkephalin and FMRFamide send processes to the sensory epithelium. These neurons of the osphradial ganglion are thus considered to be part of the sensory system, as are methionine-enkephalin-immunoreactive cells in the mantle wall in the vicinity of the osphradium. The complexity of the osphradial ganglion is further demonstrated by serotonin-immunoreactive neurons innervating the muscular coat around the osphradial canal and methionine-enkephalin-immunoreactive cells sending projections to the central nervous system.     

Dye-filling of the amphid sheath glia: implications for the functional relationship between sensory neurons and glia in Caenorhabditis elegans

The nervous system is composed of cells including neurons and glia. It has been believed that the former cells play central roles in various neural functions while the latter ones have only supportive functions for neurons. However, recent findings suggest that glial cells actively participate in neural activities, and the cooperation between neurons and glia is important for nervous system functions. In Caenorhabditis elegans, amphid sensory organs in the head also consist of sensory neurons and glia-like support cells (amphid socket and amphid sheath cells). Ciliary endings of some sensory neurons exposed to the environment detect various chemicals, molecules and signals, and the cilia of some neurons can also take up fluorescent dyes such as DiI. Here, we show that the amphid sheath glia are also stained with DiI and that its uptake by the amphid sheath cells correlates with DiI-filling of sensory neurons, suggesting that the amphid sheath glia might interact with sensory neurons. Furthermore, the localization of the amphid sheath cell reporter F52E1.2SP::YFP is abnormal in che-2 mutants, which have defective cilia. These findings imply that sensory neurons might affect amphid sheath glia functions in the amphid sensory organ of C. elegans.     

Development of a unique eye: photoreceptors of the pelagic predator Atlanta peroni (Gastropoda, Heteropoda)

 The eyes of different larval stages and juveniles of Atlanta peroni are generally composed of a cornea, a lens and a retina. In juveniles a distinct pigmented shield is visible and an enormous humour is located behind the lens. Larvae have only two sensory cells and the photoreceptors are of the ciliary type. In juveniles a striking feature is the shape of the retina. It is ribbon-shaped and new sensory cells are present which are arranged in three rows. The photoreceptors are of the ciliary type as well. Contrary to the arrangement in larvae, the ciliary plasmalemma in juveniles forms numerous lamellar stacks. In accordance with the sensory cells the stacks are organized in three parallel rows. The lamellae of adjacent stacks within a row overlap each other. The latter unique feature has not yet been found in any other representative of the Heteropoda. These findings demonstrate that (a) the eyes are altered during the development from larvae into juveniles, (b) the larval sensory cells are reduced and replaced by new sensory cells in juveniles and (c) the eyes of juvenile and adult A. peroni are well adapted for their life as visual predators. Accepted: 20 February 1999     

The multifunctional sensory complex in the antennae ofAllacma fusca (Insecta)

Summary The antennal-tip sensory complex inAllacma fusca (Collembola) was reconstructed from serial ultrathin sections. The complex contains 16 sensory cells which belong to three spatially separated subunits: (1) a sensory hair; (2) a cuticular protrusion, containing two highly-specialized dendritic outer segments from a single sensory cell encapsulated by an enveloping cell and a gland cell (Figs. 4 and 5); and (3) two sensory cells with partly lamellated, double dendritic outer segments located well away from the cuticular surface (Fig. 3). A phylogenetic evaluation reveals a mosaic of apparently primitive characters, and trends toward higher structural complexity as well as toward reduction (Table 1). There is support for a hypothesis that the receptors of the sensory hair are chemosensitive. The functional interpretation of the other components of the complex is problematic due to their unusual structural properties. The sensory cell beneath the cuticular protrusion is considered to be proprioceptive.Supported by the Deutsche Forschungsgemeinschaft (Al 56/6)     

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.     

Otolith shape lends support to the sensory drive hypothesis in rockfishes

The sensory drive hypothesis proposes that environmental factors affect both signalling dynamics and the evolution of signals and receivers. Sound detection and equilibrium in marine fishes are senses dependent on the sagittae otoliths, whose morphological variability appears intrinsically linked to the environment. The aim of this study was to understand if and which environmental factors could be conditioning the evolution of this sensory structure, therefore lending support to the sensory drive hypothesis. Thus, we analysed the otolith shape of 42 rockfish species (Sebastes spp.) to test the potential associations with the phylogeny, biological (age), ecological (feeding habit and depth distribution) and biogeographical factors. The results showed strong differences in the otolith shapes of some species, noticeably influenced by ecological and biogeographical factors. Moreover, otolith shape was clearly conditioned by phylogeny, but with a strong environmental effect, cautioning about the use of this structure for the systematics of rockfishes or other marine fishes. However, our most relevant finding is that the data supported the sensory drive hypothesis as a force promoting the radiation of the genus Sebastes. This hypothesis holds that adaptive divergence in communication has significant influence relative to other life history traits. It has already been established in Sebastes for visual characters and organs; our results showed that it applies to otolith transformations as well (despite the clear influence of feeding and depth), expanding the scope of the hypothesis to other sensory structures.     

Microscopic anatomy and ultrastructure of the introvert of Priapulus caudatus and P. tuberculatospinosus (Priapulida)

Introverts of Priapulus caudatus and P. tuberculatospinosus bear 25 rows of scalids, as well as 8 spines and scattered papillae in the region the circumoral lip. These, as well as the first ring of pharyngeal teeth in P. tuberculatospinosus, are sensory organs. Although superficially they differ between species, they are all characterized by apical and/or subapical openings which are located on tiny cuticular tubules. All sensory organs contain cilia bearing bipolar receptor cells. The 8 sensory spines situated between the circumoral area and the beginning of the scalids are ultrastructurally similar to the scalids. The introvert and pharyngeal body walls, and associated muscles are described. © 1994 Wiley-Liss, Inc.     

The neural connection between the Langerhans receptor cells and the central nervous system in Oikopleura dioica (Appendicularia)

Summary Transmission electron microscopic analysis of serial sections showed that the receptor cells are innervated by only one neuron and not two as previously believed. The neuron's two dendrites constitute the afferent sensory nerves to the caudal ganglion where the neuron's cell body is located. Its neurite was traced a few micrometers, but the synaptic terminals were not identified. This sensory system in Oikopleura is compared with a similar caudal sensory system in the tadpole larva of Diplosoma macdonaldi investigated by Torrence and Cloney. Wiring diagrams are proposed for the two systems. The ganglia, which receive the afferent sensory neurons, are discussed in terms of models for further research on simple integration systems.     

Ultrastructural investigation of the nuchal organs of Pygospio elegans (Polychaeta)

Summary The differentiation of the dorsal organs as well as the structure of the nuchal organs and their relation to the central nervous system in adult Pygospio elegans were studied by electron microscopy and compared to the nuchal organs of the larvae. The nuchal organs are represented by paired ciliary bands on the dorsal side of the first setiger, delimiting a median caruncle that is completely filled with epidermal and nervous tissue. They are composed of ciliated supporting cells and bipolar primary sensory cells constituting the nuchal ganglia, which are integrated into the brain. Microvillus-like processes of the ciliated cells give rise to a secondary covering layer over the sensory epithelium. The size of the nuchal organs is a sexually dimorphic feature.Dorsal organ formation is concomitant with the onset of sexual maturation in the male sex only. They appear as metameric ciliary bands on the dorsal side of the anterior body region and consist of ciliated cells accompanied by lateral accumulations of tubular gland cells. In the gametogenic segments they are structurally associated with the male genital pores and may be involved in reproduction. The results refute previous theories that dorsal organs are sensory and have a common origin to nuchal organs.Abbreviations ac anterior commissure of the brain - ace anterior circumesophageal connective - bb basal body - bl basal lamina - c cuticle - ca caruncle - cc ciliated cell - ci sensory cilium - co microvillar cover - d septate desmosome - db dorsal blood vessel - dn dorsal nerve cord - ea efferent axons - ec epidermal cell - eg elementary granules - g Golgi complex - i filamentous inclusion - lm longitudinal muscles - ly lysosome - mc motile cilia - mv microvillus - n neuron - ng nuchal ganglion - nn nuchal nerve - nu nucleus - oc olfactory chamber - pa palp - pc posterior commissure of the brain - pce posterior circumesophageal connective - rer rough endoplasmic reticulum - sI setiger I - sb sensory bulb - sc sensory cell - sd sensory dendrite - ser smooth endoplasmic reticulum - tf tonofilament bundle - v clear vesicles - za zonula adherens     

Immunohistochemical localization of serotonin,leu-enkephalin,tyrosine hydroxylase,and substance P within the visceral sensory area of cartilaginous fish

Summary We examined the distribution of immunoreactivity to serotonin (5-HT), leu-enkephalin (LENK), tyrosine-hydroxylase (TH), and substance P (SP) within the primary visceral sensory region of cartilaginous fish. Two genera of sharks, Squalus and Heterodontus, a skate, Raja, a ray, Myliobatis, and a holocephalian, Hydrolagus, were used. Cranial nerves, VII, IX, and X enter the visceral sensory complex from the lateral aspect and divide it into lobes. Based on sagittally cut sections, there are four lobes in Hydrolagus and five in Squalus, corresponding to the number of gill arches. The neurochemicals are differentially distributed within each lobe. LENK+ and 5-HT+fibers are located in all regions within the visceral sensory complex. SP+fibers are extremely dense in a dorsolateral subdivision and do not extend as far ventrally as 5-HT+ and LENK+fibers. The lobes lack 5-HT+cells, but contain a few LENK+ and SP+cells. Many TH+cells are distributed in dorsomedial portions of the complex, but there are few TH+fibers. Thus, the visceral sensory area of cartilaginous fish contains several divisions that can be distinguished by their neurochemical content.     

IFT52 plays an essential role in sensory cilia formation and neuronal sensory function in Drosophila

Cilia are microtubule-based, hair-like organelles involved in sensory function or motility, playing critical roles in many physiological processes such as reproduction, organ development, and sensory perception. In insects, cilia are restricted to certain sensory neurons and sperms, being important for chemical and mechanical sensing, and fertility. Although great progress has been made regarding the mechanism of cilia assembly, the formation of insect cilia remains poorly understand, even in the insect model organism Drosophila. Intraflagellar transport (IFT) is a cilia-specific complex that traffics protein cargos bidirectionally along the ciliary axoneme and is essential for most cilia. Here we investigated the role of IFT52, a core component of IFT-B, in cilia/flagellar formation in Drosophila. We show that Drosophila IFT52 is distributed along the sensory neuronal cilia, and is essential for sensory cilia formation. Deletion of Ift52 results in severe defects in cilia-related sensory behaviors. It should be noted that IFT52 is not detected in spermatocyte cilia or sperm flagella of Drosophila. Accordingly, ift52 mutants can produce sperms with normal motility, supporting a dispensable role of IFT in Drosophila sperm flagella formation. Altogether, IFT52 is a conserved protein essential for sensory cilia formation and sensory neuronal function in insects.     

Comparative study of the olfactory epithelium of the three-spined stickleback (Gasterosteus aculeatus) and the nine-spined stickleback (Pungitius pungitius)

Summary The olfactory epithelium of the three-spined stickleback (Gasterosteus aculeatus) and the nine-spined stickleback (Pungitius pungitius) has been studied with a conventional histochemical and a novel immunological staining technique. In both species, the sensory epithelium is arranged in folds separated by non-sensory epithelial tissue. In the nine-spined stickleback, intrinsic folds consisting of non-sensory cells are found in the apical part of the sensory epithelium where they divide the surface of the sensory epithelium into small islets. These non-sensory cells are non-ciliated, flattened and piled on top of each other; they contain numerous electron-translucent vesicles. The intrinsic folds are absent from the sensory epithelium of the three-spined stickleback. In both species, axons of receptor cells form a layer of fibers in the sensory epithelium immediately above the basal cells. In the three-spined stickleback, thick branches of the olfactory nerve are frequently found in this layer. These branches are only occasionally observed in the sensory epithelium of the nine-spined stickleback. Thus, the three-spined stickleback and the nine-spined stickleback show considerable differences in the organization of the sensory regions of the olfactory epithelium.     

Differentiation of the inner ear sensory epithelia of Proteus anguinus (Urodela,amphibia)

The stages of differentiation of the inner ear sensory epithelia of the neotenous cave urodele, Proteus anguinus, was studied with light and electron microscopy. Comparative ultrastructural analysis among specimens of different sizes confirms that new sensory cells may be generated throughout life, particularly along the periphery of the saccular macula. The inner ear of Proteus contains at least four types of sensory cells that differ in their apical ciliary part. The lungs and air-filled buccal cavity may function as transducers of sound pressure in underwater conditions. Sound waves might be transmitted from the buccal cavity to the connected oval window. The very complex orientation of the sensory hair cells of the saccular macula and the large overlying saccular otoconial mass suggest that this macula facilitates orientation of Proteus in its underground aqueous habitat.     

Electron microscopic demonstration of lectin binding sites in the taste buds of the European catfish Silurus glanis (Teleostei)

Summary Taste buds in the European catfish Silurus glanis were examined with electron microscopic lectin histochemistry. For detection of carbohydrate residues in sensory cells and adjacent epithelial cells, gold-, ferritin-and biotin-labeled lectins were used. A post-embedding procedure carried out on tissue sections embedded in LR-White was applied to differentiate between the sensory cells: The lectins from Helix pomatia (HPA) and Triticum vulgare (WGA) bound to N- acetyl-galactosamine and to N-acetylglucosamine residues occurring especially in vesicles of dark sensory cells. This indicates a secretory function of these cells. Most light sensory cells — with some exceptions, probably immature cells —, are HPA-negative. The mucus of the receptor field and at the top of the adjacent epithelial cells was strongly HPA-positive. Pre-embedding studies were performed in order to obtain information about the reaction of the mucus with lectins under supravital conditions. The mucus of the taste bud receptor field exhibited intensive binding to WGA, but not to the other lectins tested. Most lectins bound predominantly to the surface mucus of the nonsensory epithelium and to the marginal cells close to the receptor field. The strong lectin binding to mucins and the relatively weak lectin binding to cell surface membranes in pre-embedding studies suggest that the mucus possibly serves as a barrier which is passed selectively only by a small amount of lectins or lectincarbohydrate complexes. Lectin-carbohydrate interactions may play a role in recognition phenomena on the plasmalemmata of the taste bud sensory cells. Recognition processes directed to bacteria or viruses should be considered as well.Parts of this investigation were presented at the XI. Annual Meeting of the Association for Chemoreception Sciences (AChemS XI), held at Sarasota, Fl, April 12–14, 1989 (Witt and Reutter 1989)