The scolopidial accessory organ in the Jerusalem cricket (Orthoptera: Stenopelmatidae)

Multiple mechanosensory organs form the subgenual organ complex in orthopteroid insects, located in the proximal tibia. In several Ensifera (Orthoptera), a small chordotonal organ, the so-called accessory organ, is the most posterior part of this sensory complex. In order to document the presence of this accessory organ among the Ensifera, the chordotonal sensilla and their innervation in the posterior tibia of two species of Jerusalem crickets (Stenopelmatidae: Stenopelmatus) is described. The sensory structures were stained by axonal tracing. Scolopidial sensilla occur in the posterior subgenual organ and the accessory organ in all leg pairs. The accessory organ contains 10–17 scolopidial sensilla. Both groups of sensilla are commonly spatially separated. However, in few cases neuronal fibres occurred between both organs. The two sensillum groups are considered as separate organs by the general spatial separation and innervation by different nerve branches. A functional role for mechanoreception is considered: since the accessory organ is located closely under the cuticle, sensilla may be suited to detect vibrations transferred over the leg's surface. This study extends the known taxa with an accessory organ, which occurs in several taxa of Ensifera. Comparative neuroanatomy thus suggests that the accessory organ may be conserved at least in Tettigoniidea.     

The scolopidial accessory organs and Nebenorgans in orthopteroid insects: Comparative neuroanatomy,mechanosensory function,and evolutionary origin

Scolopidial sensilla in insects often form large sensory organs involved in proprioception or exteroception. Here the knowledge on Nebenorgans and accessory organs, two organs consisting of scolopidial sensory cells, is summarised. These organs are present in some insects which are model organisms for the physiology of mechanosensory systems (cockroaches and tettigoniids). Recent comparative studies documented the accessory organ in several taxa of Orthoptera (including tettigoniids, cave crickets, Jerusalem crickets) and the Nebenorgan in related insects (Mantophasmatodea). The accessory organ or Nebenorgan is usually a small organ of 8–15 sensilla located in the posterior leg tibia of all leg pairs. The physiological properties of the accessory organs and Nebenorgans are so far largely unknown. Taking together neuroanatomical and electrophysiological data from disparate taxa, there is considerable evidence that the accessory organ and Nebenorgan are vibrosensitive. They thus complement the larger vibrosensitive subgenual organ in the tibia. This review summarises the comparative studies of these sensory organs, in particular the arguments and criteria for the homology of the accessory organ and Nebenorgan among orthopteroid insects. Different scenarios of repeated evolutionary origins or losses of these sensory organs are discussed. Neuroanatomy allows to distinguish individual sensory organs for analysis of sensory physiology, and to infer scenarios of sensory evolution.     

Structure and sensory physiology of the leg scolopidial organs in Mantophasmatodea and their role in vibrational communication

Individuals of the insect order Mantophasmatodea use species-specific substrate vibration signals for mate recognition and location. In insects, substrate vibration is detected by mechanoreceptors in the legs, the scolopidial organs. In this study we give a first detailed overview of the structure, sensory sensitivity, and function of the leg scolopidial organs in two species of Mantophasmatodea and discuss their significance for vibrational communication. The structure and number of the organs are documented using light microscopy, SEM, and x-ray microtomography. Five scolopidial organs were found in each leg of male and female Mantophasmatodea: a femoral chordotonal organ, subgenual organ, tibial distal organ, tibio-tarsal scolopidial organ, and tarso-pretarsal scolopidial organ. The femoral chordotonal organ, consisting of two separate scoloparia, corresponds anatomically to the organ of a stonefly (Nemoura variegata) while the subgenual organ complex resembles the very sensitive organs of the cockroach Periplatena americana (Blattodea). Extracellular recordings from the leg nerve revealed that the leg scolopidial organs of Mantophasmatodea are very sensitive vibration receptors, especially for low-frequency vibrations. The dominant frequencies of the vibratory communication signals of Mantophasmatodea, acquired from an individual drumming on eight different substrates, fall in the frequency range where the scolopidial organs are most sensitive.     

Central projections of sensory cells of the midleg of the locust,Schistocerca gregaria

The central projections of trichoid hairs and of some scolopidial organs of the mesothoracic leg of the locust Schistocerca gregaria were studied by using nickel chloride backfilling and single cell recording. Trichoid hair sensilla on different parts of the legs project somatotopically in the ventral part of the ipsilateral neuropile of the mesothoracic ganglion. Generally, distally located receptors have their terminal arborizations in ventro-lateral areas of the neuropile, and proximally located receptors in ventro-medial areas. The axons of the subgenual organ and tarsal chordotonal organs project into the intermediate neuropile.     

Biophysics of the subgenual organ of the honeybee, Apis mellifera

The subgenual organ of the honeybee (Apis mellifera) is suspended in a haemolymph channel in the tibia of each leg. When the leg is accelerated, inertia causes the haemolymph (and the subgenual organ) to lag behind the movement of the rest of the leg. The magnitude of this phase lag determines the displacement of the subgenual organ relative to the leg and to the proximal end of the organ, which is connected to the cuticle. Oscillations of the subgenual organ are visualised during vibration stimulation of the leg, by means of stroboscopic light. Video analysis provides fairly accurate values of the amplitude and phase of the oscillations, which are compared with the predictions of a model.   The model comparison shows that the haemolymph channel can be described as an oscillating fluid-filled tube occluded by an elastic structure (probably the subgenual organ). The mechanical properties of the subgenual organ and haemolymph channel resemble those of an overdamped mass-spring system. A comparison of the threshold curve of the subgenual organ determined using electrophysiology with that predicted by the oscillating tube model suggests that the sensory cells respond to displacements of the organ relative to the leg. Accepted: 10 May 1997     

Spatial organization of tettigoniid auditory receptors: Insights from neuronal tracing

The auditory sense organ of Tettigoniidae (Insecta, Orthoptera) is located in the foreleg tibia and consists of scolopidial sensilla which form a row termed crista acustica. The crista acustica is associated with the tympana and the auditory trachea. This ear is a highly ordered, tonotopic sensory system. As the neuroanatomy of the crista acustica has been documented for several species, the most distal somata and dendrites of receptor neurons have occasionally been described as forming an alternating or double row. We investigate the spatial arrangement of receptor cell bodies and dendrites by retrograde tracing with cobalt chloride solution. In six tettigoniid species studied, distal receptor neurons are consistently arranged in double‐rows of somata rather than a linear sequence. This arrangement of neurons is shown to affect 30–50% of the overall auditory receptors. No strict correlation of somata positions between the anterio‐posterior and dorso‐ventral axis was evident within the distal crista acustica. Dendrites of distal receptors occasionally also occur in a double row or are even massed without clear order. Thus, a substantial part of auditory receptors can deviate from a strictly straight organization into a more complex morphology. The linear organization of dendrites is not a morphological criterion that allows hearing organs to be distinguished from nonhearing sense organs serially homologous to ears in all species. Both the crowded arrangement of receptor somata and dendrites may result from functional constraints relating to frequency discrimination, or from developmental constraints of auditory morphogenesis in postembryonic development. J. Morphol. © 2012 Wiley Periodicals, Inc.     

Functional morphology of the subgenual organ of the carpenter ant

Using light microscopy, confocal microscopy, electron microscopy and histochemistry, the subgenual organ (SGO) of an ant, Camponutas ligniperda, is investigated. Sensory units and attachment cells together enclose a large extracellular cavity, which is filled by acid mucopolysaccharides, as revealed by staining with ruthenium red. Due to this cavity, the whole SGO has the shape of a deformed sphere and the scolopidia exhibit a distribution of angles between 0 degrees and 60 degrees with the tibial long axis (as is shown by phalloidin-rhodamin staining of the actin filaments of the scolopale, viewed in situ by laser scanning confocal microscopy). The subgenual organ is innervated by a branch of the tibial nerve, which splits within or shortly distal to the femur-tibia joint. The other features of the SGO of Camponotus ligniperda are similar as in other insects: the SGO of Camponotus ligniperda contains about 35 scolopidial sensilla; it is fixed to the subgenual nerve on its proximal end, by its attachment cells to the opposite part of the cuticle; the fixation by the attachment cells is accomplished by a vast quantity of cytoplasmic microtubules; the construction of the sensory units is the same as in other mononematic scolopidial organs. The role of the extracellular lumen inside the organ and the special shape of the SGO of Camponotus ligniperda in mechanical transmission is discussed.     

Johnston's organ in Neodiprion sertifer (Insecta: Hymenoptera)

The fine structure of Johnston's organ in the pine sawfly, Neodiprion sertifer, was studied by electron microscopy to determine if there exists a dimorphism in this organ corresponding to the sexual dimorphism in antennal shape and surface area. The organ is made up of scolopidia that are ultrastructurally similar to those of other insects. The scolopidia, identical in both sexes, comprise three sensory cells bearing two types of sensory processes: Two are shorter and smaller in diameter than the third, which extends into the cuticle of the membrane connecting pedicel and flagellum and terminates at an epicuticular invagination. The dendrites and sensory processes are surrounded by two types of enveloping (glial) cells-a scolopale cell and an attachment cell. Other enveloping cells occur at different levels of the scolopidium. Sexual dimorphism is evident only in the numbers of scolopidial groups: Males have more groups with fewer scolopidia, but both sexes possess about the same total number of scolopidia.     

The hair-peg organs of the shore crab,Carcinus maenas (Crustacea,Decapoda): Ultrastructure and functional properties of sensilla sensitive to changes in seawater concentration

Summary The hair-peg organs of the shore crab, Carcinus maenas, are modified hair-sensilla. A small hair shaft (peg) is surrounded by a tuft of solid cuticular bristles (hairs). Each hair-peg organ is innervated by 6 sensory neurons, 2 of which have scolopidial (type-I) dendrites. The outer segments of all dendrites pass through a cuticular canal extending to the articulated hair base in which the 2 type-I dendrites terminate. The other 4 (type-II) dendrites reach the clavate tip of the hair shaft and have access to a terminal pore and a large sickle-shaped aperture. Three inner and 8–12 outer enveloping cells belong to a hair-peg organ. The innermost enveloping cell contains a scolopale, which has desmosomal connections to the ciliary rootlets of the type-I dendrites. An inner and an outer sensillum lymph space are present. The ultrastructural features of the dendrites and the cuticular apparatus indicate that the hair-peg organs are bimodal sensilla, comprising 2 mechano- and 4 chemosensitive sensory neurons. Extracellular recordings from the leg nerve indicate that the chemosensitive neurons of the hair-peg organs respond to changes in seawater concentration in the physiological range of Carcinus maenas.Supported by the Deutsche Forschungsgemeinschaft (SFB 45/A1; W. Gnatzy)     

Modelling the subgenual organ of the honeybee, Apis mellifera

In a recent study on the honeybee (Apis mellifera), the subgenual organ was observed moving inside the leg during sinusoidal vibrations of the leg (Kilpinen and Storm 1997). The subgenual organ of the honeybee is suspended in a haemolymph channel in the tibia of each leg. When the leg accelerates, the inertia causes the haemolymph and the subgenual organ to lag behind the movement of the rest of the leg. To elucidate the biophysics of the subgenual organ system of the honeybee, two mathematical models to simulate the experimentally observed mechanical response are considered. The models are a classical mass-spring model and a newly developed tube model consisting of an open-ended, fluid-filled tube occluded by an elastic structure midway. Both models suggest that the subgenual organ included in the haemolymph channel resembles that of an overdamped system. In resembling the biophysics of the subgenual organ system in the honeybee, we consider the tube model to be the better of the two because it simulates a mechanical response which complies best with the experimental data, and the physical parameters in the model can be related to the␣constituent parts of the subgenual organ included in the haemolymph channel. Received: 25 July 1997 / Accepted in revised form: 8 December 1997     

Histology and ultrastructure of the olfactory organ of the freshwater pulmonate Helisoma trivolvis

Summary The olfactory organ of Helisoma trivolvis is located on the surface of the body at the base of the cephalic tentacles. An evagination of skin, the olfactory plica, at the base of the tentacle extends over the olfactory organ dorsally. The epithelium of the olfactory organs contains unspecialized epithelial cells, ciliated epithelial cells, basal cells, mucous secretory cells, and sensory dendrites. The surface of the epithelium has a complex brush border of thick plasmatic processes, which branch to form several terminal microvillar twigs. Long slender cytoplasmic processes form a dense spongy layer among the plasmatic processes beneath the level of the terminal twigs. Bipolar primary sensory neurons clustered beneath the epithelium of the olfactory organ send dendrites through the epithelium to the free surface. Some sensory endings have a few short cilia, but most bear only microvilli. Cilia of sensory endings and epithelial cells extend beyond the brush border of the epithelium. Small axons arise from the perikarya of the sensory neurons and enter a branch of the olfactory nerve. HRP tracing indicates that the axons pass to the cerebral ganglion without interruption. Histochemical tests indicate that the sensory neurons are neither aminergic nor cholinergic.     

The coxo-trochanteral muscle receptor organ of locusts

Summary The coxo-trochanteral muscle receptor organ of the hind leg of the locust Locusta migratoria migratorioides (R.&F.) has been investigated by use of scanning and transmission electron microscopy with special emphasis on its distal attachment site. The overall morphology of the receptor muscle, the sensory neuron and its dendrites was found to share many common features with other arthropod sense organs of that type with two important differences: (1) the connective tissue segment (= intercalated tendon) is extremely short compared to that of other muscle receptor organs; (2) the naked dendritic terminals of the non-ciliated, multipolar sensory neuron of the organ contain clusters of microtubules, interconnected by an amorphous matrix, that resemble the tubular bodies of ciliated, epithelial receptor cells.Abbreviation MRO muscle receptor organ Supported by the Deutsche Forschungsgemeinschaft (Br 882 and Hu 223)     

Functional morphology and development of tibial organs in the legs I,II and III of the bushcricketEphippiger ephippiger (Insecta,Ensifera)

Summary The anatomy of the complex tibial organs in the pro-, meso- and metathoracic legs of adults and larvae of the bushcricketEphippiger ephippiger is described comparatively. The subgenual organ and the intermediate organ are differentiated in the same way in legs I, II and III; the anatomy of the crista acustica and the tracheal morphology are significantly different. The final number of scolopidia in the tibial organ of each leg is present at the time of hatching. In the subgenual organ, the number of scolopidia is the same in all legs; in the intermediate organ, and especially in the crista acustica, the number of scolopidia decreases from leg I to legs II and III. In the first larval instar, the morphology of the tibia, the course of the trachea and the anatomy of accessory structures are developed in the same way in each leg. The specific differentiations forming the auditory receptor organ in leg I, such as the acoustic trachea, the tympana and tympanal cavities, develop step by step in subsequent instars. The auditory threshold recorded from the tympanal nerve in the prothoracic leg of adults is remarkably lower than in the meso- and metathoracic legs. Morphometrical analyses of structures that are suggested to play a role in stimulus transduction on scolopidia of the crista acustica reveal significant differences in the three legs.     

The development of the sensory organs of the legs in the blowfly,Phormia regina

Summary The development of the sensory neurons of the legs of the blowfly,Phormia regina has been described from the third instar larva to the late pupa using immunohistochemical staining. The leg discs of the third instar larva contain 8 neurons of which 5 come to lie in the fifth tarsomere of the developing leg. Whereas 2 neurons persist at least to the late pupa, the other cells degenerate. The first neurons of gustatory sensilla arise in the fifth tarsomere at about 1.5 h after formation of the puparium. Most of these sensilla, however, appear within a short time period beginning at about 18 h. The femoral chordotonal sensory neurons first appear at the time of formation of the puparium, as a mass of cells situated in the distal femur. During later pupal development 2 groups of these cells come to lie at the femur-trochanter border, where they become the proximal femoral chordotonal organ of the adult; the remaining cells become the distal femoral chordotonal organ. Other scolopidial neurons appear later in development. The nerve pathways of the late pupal leg are established either by the axons of the cells that are present in the larval leg disc or by new outgrowing processes of sensory neurons. In the tibia, the initial direction of new outgrowth differs in different regions of the segment: proximal tibial neurons grow distally, while distal tibial neurons grow initially proximally.     

Development of leg chordotonal sensory organs in normal and heat shocked embryos of the cricket Teleogryllus commodus (Walker)

This paper describes the embryonic development of some parts of the sensory peripheral nervous system in the leg anlagen of the cricket Teleogryllus commodus in normal and heat shocked embryos. The first peripheral neurons appear at the 30% stage of embryogenesis. These tibial pioneer neurons grow on a stereotyped path to the central nervous system and form a nerve which is joined by the growth cones of axons that arise later, including those from the femoral chordotonal organ, subgenual organ and tympanal organ. The development of these organs is described with respect to the increase in number of sensory receptor cells and the shape and position of the organs. At the 100% stage of embryogenesis all three organs have completed their development in terms of the number of sense cells and have achieved an adult shape. To study the function of the tibial pioneer neurons during embryogenesis a heat shock was used to prevent their development. Absence of these neurons has no effect on the development of other neurons and organs proximal to them. However, the development of distal neurons and organs guided by them is impaired. The tibial pioneer neurons grow across the segmental boundary between femur and tibia early in development, and the path they form seems to be essential for establishing the correct connections of the distal sense organs with the central nervous system.     

On the cavity receptor organ (X-organ or organ of Bellonci) of Artemia salina (Crustacea: Anostraca)

Summary The cavity receptor organ (previously X-organ or organ of Bellonci) of Artemia salina consists of ciliated neurons whose cilia protrude into a cavity beneath the cuticle. The neuronal dendrites penetrate a giant accompanying cell and epidermal cells before entering the cavity. The cavity beneath the cuticle, the ciliated neurons and the connexion with the medulla terminalis justifies a homologization with the frontal filament organ of cirripeds and the third unit of copepods. The term cavity receptor is suggested for this organ. It is hardly homologous with the second unit of copepods and the organs described for many malacostracans under the names of sensory pore X-organ or organ of Bellonci. The latter organs are very similar to the cavity receptor but have an internal cavity formed by glial cells.The cavity receptor organ was previously considered neurosecretory but in the light of the present knowledge it is rather sensory although a double function cannot be denied.This investigation was supported by grants (to R. E.) 2760-3 and 2760-4 from the Swedish Natural Science Research Council. One of us (P. S. L.) was on sabbatical leave from the University of Tasmania.     

Comparison of auditory sense organs in parasitoid Tachinidae (Diptera) hosted by Tettigoniidae (Orthoptera) and homologous structures in a non-hearing Phoridae (Diptera)

The dipteran parasitoids Therobia leonidei and Homotrixa alleni (Tachinidae) use acoustic cues to locate their calling tettigoniid (Ensifera, Orthoptera) hosts. The sexually dimorphic tympanal organs of both fly species are located at the prosternum. For comparison a homologous chordotonal organ in the non-hearing fly Phormia regina, Meigen (Phoridae) is also described. The scolopidial sense organs of the ears have approximately 180 sensory cells in Th. leonidei and 250 cells in H. alleni. Interspecific analysis indicates that the cell number and arrangement might be genus specific in Tachinidae. The mononematic scolopidia, each with one sensory cell, are of different sizes and insert at the tympanal membrane. Large scolopidial units (diameter of sensory cells up to 50 μm) extend longitudinally from the centre of the sensory organ towards the ligament, whereas small units (sensory cell diameter up to 10 μm) are arranged sequentially within the sensory organ. This arrangement is discussed to be a possible basis for frequency discrimination. The ultrastructure of the scolopidia is similar in the hearing and non-hearing flies. In both groups, the majority of scolopales has a diameter from 2 to 2.9 μm, although hearing species have additionally wider scolopales. The homologous chordotonal organ of Ph. regina consists of approximately 55 sensory cells of uniform direction. The data are discussed in comparison to the ears of other Diptera.     

Sensory organs of the thoracic legs of the moth Manduca sexta

Summary The thoracic legs of the moth Manduca sexta acquire a new form and develop a new complement of sensory organs and muscles during metamorphosis from larva to adult. Because of our interest in the reorganization of neural circuitry and the acquisition of new behaviors during metamorphosis, we are characterizing sensory elements of larval and adult legs so that we may determine the contribution of new sensory inputs to the changes in behaviors. Here we describe the sensory structures of adult legs using scanning electron microscopy to view the external sensilla and cobalt staining to examine innervation by underlying sensory neurons. We find that, in contrast to larval legs, the adult legs are covered with a diverse array of sensilla. All three pairs of thoracic legs contain scattered, singly innervated scalelike sensilla. Campaniform sensilla occur singly or in clusters near joints. Hair plates, consisting of numerous singly innervated hairs, are also present near joints. Other more specialized sensilla occur on distal leg segments. These include singly innervated spines, two additional classes of singly innervated hairs, and three classes of multiply innervated sensilla. Internal sensory organs include chordotonal organs, subgenual organs, and multipolar joint receptors.