A possible proprioceptor in Ceriantheopsis americanus (cnidaria,ceriantharia)

Summary A new type of sensory cell in the body wall of Ceriantheopsis americanus is described. Its dendrite bears a cilium within a circle of stereocilia which are surrounded by a sheath-like projection of the dendrite. The sensory apparatus is embedded in the soma of a muscle cell which forms two sheaths that interdigitate with that of the dendrite. The sensory cell receives an efferent innervation, presumably inhibitory, from the same type of nerve cell that innervates the musculature. It is suggested that the sensory cell is a mechanoreceptor sensitive to body wall distortion due to mechanical stimulation and to tilt of the body relative to gravity.This work was supported by grant MH-11218 from the U.S. Public Health Service.     

Ultrastructure of the abdominal sense organ of the scallop <Emphasis Type="Italic">Mizuchopecten yessoensis</Emphasis> (Jay)

The sensory epithelium of the abdominal sense organ (ASO) of the scallop Mizuchopecten yessoensis is composed of three cell types, sensory cells, mucous cells, and multiciliated cells. Sensory cells bear a single long (up to 250 microm) cilium surrounded by an inner ring of nine modified microvilli and an outer ring of ordinary microvilli paired with modified microvilli. Sensory cells make up about 90% of the total number of cells in the sensory epithelium. Mucous cells, which are much wider than sensory cells, bear only ordinary microvilli on their apical surface. Rare multiciliated cells with short (4-6 microm) cilia are scattered in the periphery of the sensory epithelium sheet. All hairs, cilium, and microvilli of each sensory cell are interconnected by a fibrous network. Nine modified microvilli of a single cell are interconnected by prominent laterally running fibrous links. Membrane-associated electron-dense material of modified microvilli is connected to the ciliary membrane-associated electron-dense material by fine string-like links. These links mechanically bridge the space between the cilium and modified microvilli, as do mechanical links, described for the stereocilia and kinocilium of vertebrate vestibular and cochlear hair cells. The proximal portion of a sensory cilium is about 100 microm long and has a typical 9 x 2+2 axoneme arrangement. The distal portion of a cilium is approximately 2 times thinner than the proximal one and is filled with homogeneous electron-dense material. Along the distal portion, diffuse material associated with the external surface of the membrane is found. The rigidity of distal portion of a cilium is much less than that of the proximal one.     

Fine structure of the sensilla of Peripatopsis moseleyi (Onychophora)

Summary Three types of sensilla occurring on the lips and on the antennae of Peripatopsis moseleyi have been investigated by scanning and transmission electron microscopy. On the lips sensory spines can be found which contain numerous cilia originating from bipolar receptor cells. They reach the tip of the spine where the cuticle is modified. The perikarya of the sensory cells, a large supporting cell with a complicated surface and a second type of receptor, form a bud-like structure and are surrounded by a layer of collagen fibrils. The second receptor cell bears apical stereocilia as well as a kinocilium which are directed towards the centre of the animal — thus the cell appears to be turned upside down. The sensilla of the antennae are 1) sensory bristles containing two or three kinds of receptor cells, one of which bears an apical cilium and one kind of supportive cell and 2) sensory bulbs located within furrows consisting of receptor cells with branched cilia and two kinds of supportive cells which are covered by a modified thin cuticle. According to the electron microscopical findings the sensory spines on the lips are presumably chemoreceptors. The sensory bristles on the antennae can be regarded as mechanoreceptors and the sensory bulbs as chemoreceptors.Supported by the Deutsche Forschungsgemeinschaft (Sto 75/3)     

Head sensory organs of Dactylopodola baltica (Macrodasyida, Gastrotricha): a combination of transmission electron microscopical and immunocytochemical techniques

The anterior and posterior head sensory organs of Dactylopodola baltica (Macrodasyida, Gastrotricha) were investigated by transmission electron microscopy (TEM). In addition, whole individuals were labeled with phalloidin to mark F-actin and with anti-alpha-tubulin antibodies to mark microtubuli and studied with confocal laser scanning microscopy. Immunocytochemistry reveals that the large number of ciliary processes in the anterior head sensory organ contain F-actin; no signal could be detected for alpha-tubulin. Labeling with anti-alpha-tubulin antibodies revealed that the anterior and posterior head sensory organs are innervated by a common stem of nerves from the lateral nerve cords just anterior of the dorsal brain commissure. TEM studies showed that the anterior head sensory organ is composed of one sheath cell and one sensory cell with a single branching cilium that possesses a basal inflated part and regularly arranged ciliary processes. Each ciliary process contains one central microtubule. The posterior head sensory organ consists of at least one pigmented sheath cell and several probably monociliary sensory cells. Each cilium branches into irregularly arranged ciliary processes. These characters are assumed to belong to the ground pattern of the Gastrotricha.     

Kinocilia mediate mechanosensitivity in developing zebrafish hair cells

Mechanosensitive cilia are vital to signaling and development across many species. In sensory hair cells, sound and movement are transduced by apical hair bundles. Each bundle is comprised of a single primary cilium (kinocilium) flanked by multiple rows of actin-filled projections (stereocilia). Extracellular tip links that interconnect stereocilia are thought to gate mechanosensitive channels. In contrast to stereocilia, kinocilia are not critical for hair-cell mechanotransduction. However, by sequentially imaging the structure of hair bundles and mechanosensitivity of individual lateral-line hair cells in?vivo, we uncovered a central role for kinocilia in mechanosensation during development. Our data demonstrate that nascent hair cells require kinocilia and kinocilial links for mechanosensitivity. Although nascent hair bundles have correct planar polarity, the polarity of their responses to mechanical stimuli is initially reversed. Later in development, a switch to correctly polarized mechanosensitivity coincides with the formation of tip links and the onset of tip-link-dependent mechanotransduction.     

Dynamical control of the shape and size of stereocilia and microvilli

We discuss theoretically the shape of actin-based protrusions such as stereocilia or microvilli that have important functions in many biological systems. These linear protrusions are dynamical structures continuously renewed by treadmilling: actin polymerizes at the tip of the cilium and depolymerizes in its bulk. They also often have a well-controlled length such as in the hair bundles of the inner ear cells where they appear in a graded staircase structure. Recent experimental results by another group of researchers show that the treadmilling velocity of the hair cell stereocilia is proportional to their length. We use generic arguments to describe the physics of stereocilia taking into account the effect of many individual proteins at a coarse-grained level by a few phenomenological parameters. At the tip of the cilium, we find that actin polymerization induces an effective pressure. Below the tip, the shape of the cilium is determined by depolymerization: Agreement with the observed shape requires that depolymerization occurs at least in two steps. Under these conditions, we calculate the cilium shape and provide physical grounds for the proportionality between treadmilling velocity and cilium length. We also calculate the penetration of the stereocilium in the actin cortical layer.     

THE FINE STRUCTURE OF COCKROACH CAMPANIFORM SENSILLA

Campaniform sensilla on cockroach legs provide a good model system for the study of mechanoreceptive sensory transduction. This paper describes the structure of campaniform sensilla on the cockroach tibia as revealed by light- and electron-microscopy. Campaniform sensilla are proprioceptive mechanoreceptors associated with the exoskeleton. The function of each sensillum centers around a single primary sense cell, a large bipolar neuron whose 40 µ-wide cell body is available for electrophysiological investigation with intracellular microelectrodes. Its axon travels to the central nervous system; its dendrite gives rise to a modified cilium which is associated with the cuticle. The tip of the 20 µ-long dendrite contains a basal body, from which arises a 9 + 0 connecting cilium. This cilium passes through a canal in the cuticle, and expands in diameter to become the sensory process, a membrane-limited bundle of 350–1000 parallel microtubules. The tip of the sensory process is firmly attached to a thin cap of exocuticle; mechanical depression of this cap, which probably occurs during walking movements, effectively stimulates the sensillum. The hypothesis is presented that the microtubules of the sensory process play an important role in mechanoelectric transduction in cockroach campaniform sensilla.     

Use of a monoclonal antibody to classify neurons isolated from the head region of Hydra

A mouse monoclonal antibody (JD1) to Hydra attenuata using the peroxidase-antiperoxidase (PAP) method revealed unipolar, bipolar, and multipolar sensory and ganglion cells in the head region of H. littoralis. Neurons isolated from macerated hypostomes and tentacles were classified according to the number of their cytoplasmic processes and the position of the cilium, when present, relative to the perikaryon. PAP-stained sensory cells had an apical ciliary cone, whereas ganglion cells did not. Neurons with cytoplasmic processes longer than 50 microns stained faintly, whereas those with processes shorter than 50 microns in length stained mainly dense brown. Unipolar neurons had an oval, crescent, round, or elliptic perikaryon with a single short axon. The perikaryal shape of bipolar neurons varied from round to tall triangular, short triangular, crescent, oval, or elliptic with two oppositely directed symmetric or asymmetric processes. Asymmetric processes were present in a bipolar sensory cell with a long apical cilium typical of gastrodermal sensory cells. One type of bipolar ganglion cell had a short perikaryal cilium. Another type had neurites longer than 50 microns. We found seven morphological variations of multipolar neurons, including one with an apical knob, two with a short perikaryal cilium, two with cytoplasmic loops near the perikaryon, one with perpendicular processes projecting from the major neurites, and one with a branched process longer than 50 microns opposite a tangled mass of neurites.     

Numbers, distribution, and types of neurons in the pedal disk of Hydra based on a serial reconstruction from transmission electron micrographs

The numbers, distribution, and types of neurons in a pedal disk of Hydra littoralis were determined from electron micrographs of 567 serial sections approximately 0.12 micron thick. Of 248 neurons counted, we found 234 ganglion cells in the epidermis and 14 in the gastrodermis. No sensory cells with surface projecting cilia were observed in either epithelial layer of the foot region. We found ciliary structures in 196 (84%) of the epidermal neurons: 55 had a well defined cilium-stereociliary complex, 30 had a cilium lacking stereocilia, and 111 could not be classified. In contrast, 38 epidermal neurons lacked evidence of ciliary structures; 10 of the 14 gastrodermal neurons had one or more centrioles, some with an elaborate pericentriolar rootlet system, but no cilium or stereocilia. Neuronal perikarya could be classified into those with dense heterochromatic nuclei and those with light granular nuclei; often these two nuclear variations were observed in paired or triad arrangements of epidermal neurons. In addition, 68 (29%) of the epidermal neurons were characterized by the presence of small dense granules (115-178 nm in diameter) in the cytoplasm around the periciliary space. Although 32 pairs and 5 triads of contiguous neuronal perikarya were present in the epidermis, only two paired neuronal perikarya were present in the gastrodermis. The major concentration of neurons was approximately midway between the basal surface and the region of transition of epitheliomuscular cells into glandulomuscular cells. There was no evidence of large neuronal aggregations suggestive of ganglia in the pedal disk.     

Actin pegs and ultrastructure of presumed sensory receptors of Beroë (Ctenophora)

Summary We have investigated the actin content and ultrastructure of two kinds of presumed sensory projections on the lip epidermis of beroid ctenophores. Transmission electron microscopy showed that conical pegs contain a large bundle of densely packed, parallel microfilaments. Rhodamine-phalloidin brightly stained the pegs, confirming that they contain filamentous actin. Epidermal cells with actin pegs also bear a single long cilium with an onion-root structure, previously described as arising from a different type of cell. The actin peg and onion-root cilium project side-by-side, defining a polarized axis of the cell which is shared by neighboring cells. The onion-root body is surrounded by a flattened membranes sac which lies immediately below the plasma membrane. The perimeter of the membrane sac is encircled by aggregates of dense material. An extra layer of dense material is found along the side of the membrane sac facing the peg; this material often makes direct contact with the adjacent actin filament bundle. Cells with actin pegs and onion-root cilia synapse onto adjacent neurites and secretory gland cells, indicating that one or both types of projections are sensory elements. Since the feeding responses of beroids are reported to depend on chemical and tactile stimuli to the lips, the cells bearing pegs and cilia may function as both mechanoreceptors and chemoreceptors, that is, as double sensory receptors.     

Antennal sensory organs in the millipede Eurypauropus ornatus: Fine structure of the flagella and globulus

On the antennal tip of Eurypauropus ornatus are 3 threadlike sensilla—the flagella, and a single spheroid sensillum—the globulus. Each of the 3 flagella is innervated by 2 groups of sensory cells. One group contains 4 cells, the other, 5. All cells of the “four group” and 3 of the “five group” are comprised of single cilia and unbranched dendrites which extend along the lumen of the flagellum. Two cells of the “five group” have double cilia and pairs of unbranched dendrites. One pair also enters the flagellum and the other pair terminates beneath the flagellar base to form a concentric array of lamellae. No pores are present in the cuticular wall. Eight sensory cells innervate the globulus. They are arranged in 3 groups, one triplet and 2 pairs, in addition to a single cell. The single cell contains a pair of cilia whose unbranched dendrites differentiate into tubular bodies that are inserted into the base of the globulus. Each of the other 7 sensory cells has a single cilium. Their unbranched dendrites penetrate into the globulus in 3 groups as described for the sensory cells. The dendrites in each group terminate in an individual pore channel at the globulus tip and completely fuse with the electron-dense material that plugs the pore channel. Based on structural similarities to sensilla having known functions, it is probable that the flagella and the globulus are chemoreceptors, the former responding to odors, the latter sensitive to substances in aqueous solution.     

Ultrastructure of the Epithelium and the Sensory Receptors in the Body Wall, the Proboscis and the Pharynx of Gyratrix hermaphroditus (Turbellaria, Rhabdocoela)

The epidermis of Gyratrix hermaphroditus can be described as semi-syn-cytial. Its ultrastructure is characterized by microvilli and cilia with two strong rootlets perpendicular to each other. The apical part of the epithelium contains mitochondria and vacuoles. The basal synthesizing layer is provided with cell boundaries, at least between the type II penetrating receptors in the anterior and posterior end of the worm. Four different types of sensory receptors are described. The type I receptor has a protruding cilium-bearing process and is found all over the body. The type II receptor is found in the anterior and posterior end and has a retracted process with a kinocilium surrounded by eight stereocilia. The type III receptor bears a balloon-shaped modified cilium and is located at the anterior end. The type IV receptor has a short cilium with an unstable ciliary membrane and occurs in the proboscis epithelium as well as in the pharynx epithelium. Phylogenetical aspects of the semi-syncytial epithelium and functional aspects of the sensory receptors are discussed.     

Organization of the sensory hairs in the gravity receptors in utricule and saccule of the squirrel monkey

Summary The structural organization of the sensory hairs of the gravity receptors is mainly characterized by the presence of one kinocilium and 40–110 stereocilia on each sensory cell. The spatial arrangement of the kinocilia in relation to the stereocilia presents a polarization, similar to that in the sensory epithelia of the cristae. This polarization, however, is not uniform in the maculae. The direction of polarization varies between groups of several hundred sensory cells. Within one group the sensory cells are all polarized in the same main direction and these groups are considered as functional units.The apparent stiffness and low metabolic activity of the stereocilia suggest their mechanical transmitter function between the otolithic membrane and the sensory cells.The presence of modified kinocilia and basal bodies in other sensory systems raises the question of their significance in sensory receptors. Their unmodified structure in the maculae, however, where the basal bodies are almost identical with centrioles, and the presence of one kinocilium with a basal body and an associated centriole in the supporting cells as well, illustrate their unspecific nature. The centrioles, which later probably become basal bodies, are in close relation to the differentiation of apical cytoplasmic structures such as the kinocilium and the cuticula. This is demonstrated by the appearance of those structures at the bottom of the sensory cell, when the centrioles are situated in this part of the cell.This work was supported by NASA Research Grant NsC 268—62 to the Harvard University Medical School at the Dept. of Otolaryngology, Massachusetts Eye and Ear Infirmary, Boston, Mass, and by U.S.P.H.S. National Institute of Neurological Diseases and Blindness, Grant nos. B 3447 and B. 3779.     

High voltage electron stereomicroscopy of the cilium-stereociliary complex of perioral sensory cells in Hydra

The cilium-stereociliary complex in perioral neurons of Hydra was examined by electron microscopy, with emphasis on stereomicrographs of serial, 0.5 micron thick, longitudinal and transverse sections. Longitudinal sections revealed (1) flat-topped cones in which the cilium was bent and the ciliary chamber appeared heart-shaped, and (2) pointed cones in which the cilium was straight and the ciliary chamber appeared triangular. Transverse sections revealed 10-12 stereocilia forming a cone over a central cilium with nine peripheral doublets of microtubules but with often more than two central microtubules. The ciliary membrane was fluted; fine filaments connected the outfoldings of membrane with the center of the microtubule doublets. Thin sections revealed 7 nm microfilaments in the stereocilia cores which branched basally into thick and thin roots; the thick roots surrounded the base of the central cilium. The cilium-stereociliary complex was enveloped by an epitheliomuscular cell sheath with a free margin distally and a septate junction proximally. In flat-topped cones the free margin of the enveloping epitheliomuscular cell was closely applied to the top of the cilium-stereociliary complex, whereas in pointed cones the cilium-stereociliary complex projected above the free margin of the sheath. Thus, the 7 nm actin-like filaments in the stereocilia might function to contract and open the complex in response to favorable stimuli so that the cilium is in contact with the aqueous environment.     

Ultrastructural study of sensory cells of the proboscidial glandular epithelium of Riseriellus occultus (Nemertea,Heteronemertea)

Only one sensory cell type has been observed within the glandular epithelium of the proboscis in the heteronemertine Riseriellus occultus. These bipolar cells are abundant and scattered singly throughout the proboscis length. The apical surface of each dendrite bears a single cilium enclosed by a ring of six to eight prominent microvilli. The cilium has the typical 9×2 + 2 axoneme arrangement and is equipped with a cross-striated vertical rootlet extending from the basal body. No accessory centriole or horizontal rootlet was observed. Large, modified microvilli (stereovilli) surrounding the cilium are joined together by a system of fine filaments derived from the glycocalyx. Each microvillus contains a bundle of actin-like filaments which anchor on the indented inner surface of a dense, apical ring situated beneath the level of the ciliary basal body. The tip of the cilium is expanded and modified to form a bulb-like structure which lies above the level where the surrounding microvilli terminate. In the region where the cilium emerges from the microvillar cone, the membrane of the microvillar apices makes contact with a corresponding portion of the ciliary membrane. At this level microvilli and cilium are apparently firmly linked by junctional systems resembling adherens junctions. The results suggest that these sensory cells may be mechanoreceptors. © 1996 Wiley-Liss, Inc.     

The ultrastructure of the paratympanic organ (Vitali) in Gallus domesticus: preliminary studies

The sensory epithelium of the paratypanic organ (Vitali) was studied by means of the electron microscope. Two kinds of cells are present. One type extends from the basement membrane to the surface of the epithelium; their nuclei are arranged close to the connective tissue and are surrounded by a pale cytoplasm. The distal part of these cells, which are denser and richer in organelles, possess microvilli. The cells of the second type are located above the basement membrane and are found between the upper parts of the cells of the first type. Their cytoplasm is rich in small round vesicles, free ribosomes and cisternae of rough endoplasmic reticulum are present especially in the infranuclear zone. The apical part contains a Golgi apparatus lysosomes and multive sicular bodies. At the apex each cell possesses a cuticular plate numerous stereocilia and one kinocilium. The stereocilia become increasingly longer from one side of the cell surface to the other and the kinocilium is situated on the side where the stereocilia are longest. Nervous fibers are present in the epithelium and are in close contact with the cells of the second type. The cells we have described are remarkably similar to the supporting and hair cells of the vestibular sensory epithelium.     

A study on the fine structure of the saccular macula of the gold fish

Summary The fine structure of the saccular macula of the gold fish has been studied by means of the electron microscope.The sensory epithelium of the macula consists of sensory cells and supporting cells. The surface of the sensory cell is studded with a group of sensory hairs consisting of one kino-cilium and 50–60 stereocilia. In the dorsal half of the macula, the kino-cilium is located at the dorsal end of the sensory hair group. In the ventral half of the macula, the kino-cilium is located at the ventral end of the sensory hair group. In the intermediary portion of the macula, the sensory cells with opposite polarities are situated side-by-side. The relation between the microphonic potential and the position of the kino-cilium has been discussed.Two types of nerve terminals are found situated on the basal surface of the receptor cells. The one contains no synaptic vesicle and the other contains a cluster of synaptic vesicles and a few cored vesicles. It is considered that the former corresponds to the afferent nerve terminal and the latter to the efferent one.This investigation was supported by NIH Grant NB-06052.The author is very grateful to Prof. Taro Furukawa, Osaka City University for his invaluable advice and discussion.     

Monociliary receptors in interstitial Proseriata and Neorhabdocoela (Turbellaria Neoophora)

Summary The ultrastructure of monociliary receptors in 10 species of the Proseriata and Neorhabdocoela is described, with particular reference to the epidermal dendritic part.Sensory cells with a single kinocilium situated at the level of the distal epidermis membrane are considered as mechano- or chemoreceptors.There exist sensory cells with a dendrite penetrating one epidermis cell and bearing an embedded kinocilium and a collar of 8 stereocilia or ridges with a fribrillose substructure. These collared receptors probably function as mechanoreceptors.In comparison with collared sensory cells in species of other turbellarian orders, the embedded receptors in the Proseriata and Neorhabdocoela are more advanced and possess synapomorphous characteristics. With the embedded receptors a new evidence is given for the close phylogenetic relationship between the Proseriata and Neorhabdocoela.The distribution of collared cells in the animal system and their phylogenetic implication for a choanoflagellate origin of the Metazoa are briefly discussed.List of abbreviations ar annular rootlet - bm basement membrane - cb crystalline body - cc collar cell - cw cell web - cwt cell web-thickening - d dendrite - kc kinocilium - lm longitudinal musculature - mv microvilli - n nerve - nt neurotubuli - pb parenchymal branches - r rootlet - rd ridges - rh rhabdite - rm ring musculature - sc stereocilia - sd septate desmosomes - tm transversal musculature - u ultrarhabdites - za zonula adhaerens     

Fine structure of ocelli of an anthomedusan,Nemopsis dofleini,with special reference to synaptic organization

Summary An ocellus of an anthomedusan, Nemopsis dofleini, is composed of sensory and pigment cells and underlain by a nerve plexus and a muscle sheet. A sensory cell is divided into three parts: an apical part from which a single cilium arises, a slender middle part with numerous microtubules and an enlarged basal part that contains an oval nucleus but does not send out an axon. The ocellar cup is occupied by variously remodelled ciliary sheaths that are covered by a few lysosomal projections from the pigment cells. Three modes of synaptic connections — centripetal, centrifugal and two-way — are found between sensory cells and either dendrites or somata of second order neurons. Synaptic vesicles in sensory cells are larger in number, smaller in size and more uniform in shape than those of second order neurons. The soma of a second order neuron lies below the surface layer of an ocellar cup and gives rise to a single cilium that lacks rootlets and the second centriole. The possibility of multimodal sensory perception in and around the ocellar region is discussed.The work was supported by research grants from the Ministry of EducationFormerly Tamano Marine Laboratory     

Ultrastructure of presumptive light sensitive ciliary organs in larvae of Poecilochaetidae,Trochochaetidae, Spionidae,Magelonidae (Annelida) and its phylogenetic significance

Larvae of Poecilochaetus serpens, Trochochaeta multisetosum and Polydora ciliata possess almost identical unpigmented, ciliary, presumptive light sensitive organs within the prostomium. The data corroborate hypotheses on the close relationship of Poecilochaetidae, Trochochaetidae and Spionidae and are even congruent with inclusion of Poecilochaetidae and Trochochaetidae within Spionidae. The organs in P. serpens, T. multisetosum and P. ciliata are composed of one monociliary receptor cell, one supportive cell and several associated flask shaped bipolar sensory cells. The receptor cell cilium enters the supportive cell cavity through a thin pore, dilates and then branches into a high number of disordered projections. The associated sensory cells bear one or occasionally two cilia, which run horizontally beneath or within the cuticle. The supportive cell cavity is not sealed by any cell contact from the subcuticular extracellular space. The organs in Magelona mirabilis are composed of a single supportive cell, but several receptor cells. No further sensory cells are associated. Each receptor cell sends one cilium into an own invagination of the supportive cell, and the ciliary branches are highly ordered. The examined organs in P. serpens, T. multisetosum and P. ciliata exhibit a unique organization amongst polychaetes. The organs of M. mirabilis are most probably homologous. A homology to ciliary organs of Protodrilida is conceivable. In the lineage leading to Protodrilida, primary larval organs may have been integrated into the adult body organization by heterochrony.