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.     

The accessory organ,a scolopidial sensory organ,in the cave cricket Troglophilus neglectus (Orthoptera: Ensifera: Rhaphidophoridae)

Mechanoreceptor organs occur in great diversity in insect legs. This study investigates sensory organs in the leg of atympanate cave crickets (Troglophilus neglectus KRAUSS, 1879) by neuronal tracing. Previously, the subgenual and the intermediate organs were recognised in the subgenual organ complex, lacking the tympanal membranes present for example in the tibial hearing organs of Gryllidae and Tettigoniidae. We document the presence of the accessory organ in T. neglectus. This scolopidial organ is located in the posterior tibia close to the subgenual organ and can be identified by position, innervation and orientation of the dendrites of sensory neurons. The main motor nerve in the leg innervates a part of the subgenual organ and the accessory organ. The dendrites of sensory neurons in the accessory organ are characteristically bent in proximo‐dorsal direction, while the subgenual organ dendrites run distally along the longitudinal axis of the leg. The accessory organ contains 6–10 scolopidial sensilla, and no differences in neuroanatomy occur between the three thoracic leg pairs. Hence, the subgenual organ complex in cave crickets is more complex than previously known. The wider taxonomic distribution of the accessory scolopidial organ among orthopteroid insects is inconsistent, indicating its repeated losses or convergent evolution.     

The fine structure of the cockroach subgenual organ

This paper describes the fine structure of the cockroach subgenual organ, a complex ciliated mechanoreceptor that detects vibrations in the substrate upon which the animal stands. Located beneath the knee in each walking leg, the cockroach subgenual organ is a thin, fan-shaped flap of tissue slung across the dorsal blood space of the tibia at right angles to the leg's long axis. It is innervated by approximately 50 chordotonal sensilla. The fine structure of the chordotonal sensilla is is described in detail ; possible transducer sites are discussed.     

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.     

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.     

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.     

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.     

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.     

Structure of atympanate tibial organs in legs of the cave-living ensifera,Troglophilus neglectus (Gryllacridoidea,Raphidophoridae)

Troglophilus neglectus (Gryllacridoidea, Raphidophoridae) is a nocturnal Ensifera which can be found in caves of Slovenia. The anatomy of the tibial organs in the fore-, mid-, and hindlegs, as well as the external morphology of the proximal fore-tibia and the prothoracic tracheal system, is described comparatively. In the prothorax and in the forelegs, no sound-conducting structures such as an acoustic trachea, enlarged spiracles, or tympana are developed. A group of 8–10 campaniform sensillae is located in the dorsal cuticle of the proximal tibia. In each leg, the tibial organ complex is built up by two scolopale organs, the subgenual organ and the intermediate organ; the structure and the number of scolopidia is similar in each leg. No structure resembling the crista acoustica is found. The subgenual organ contains around 30 scolopidia; the intermediate organ is subdivided into a proximal part containing 8-9 scolopidia and a distal part with 5–6 scolopidia. The two groups of scolopidia are not directly connected to the tracheal system. The tibial organs in the forelegs are insensitive to airborne sound, and they appear to be more primitive compared to those found in members of the Tettigoniidae and the Gwllidae. The results indicate that the complex tibial organs in all legs of T. neglectus are primarily vibrosensitive. © 1995 Wiley-Liss, Inc.     

Embryonic development and evolutionary origin of the Orthopteran auditory organs

Two different types of ears characterize the order of Orthopteran insects. The auditory organs of grasshoppers and locusts (Caelifera) are located in the first abdominal segment, those of bushcrickets and crickets (Ensifera) are found in the tibiae of the prothoracic legs. Using neuron-specific antibody labelling, we describe the ontogenetic origin of these two types of auditory organs, use comparative developmental studies to identify their segmental homologs, and on the basis of homology postulate their evolutionary origin. In grasshoppers the auditory receptors develop by epithelial invagination of the body wall ectoderm in the first abdominal segment. Subsequently, at least a part of the receptor cells undergo active migration and project their out-growing axons onto the next anterior intersegmental nerve. During this time the receptor cells and their axons express the cell-cell adhesion molecule, Fasciclin I. Similar cellular and molecular differentiation processes in neighboring segments give rise to serially homologous sensory organs, the pleural chordotonal organs in the pregenital abdominal segments, and the wing-hinge chordotonal organs in the thoracic segments. In more primitive earless grasshoppers pleural chordotonal organs are found in place of auditory organs in the first abdominal segment. In bushcrickets the auditory receptors develop in association with the prothoracic subgenual organ from a common developmental precursor. The auditory receptor neurons in these insects are homologous to identified mechanoreceptors in the meso- and metathoracic legs. The established intra- and interspecies homologies provide insight into the evolution of the auditory organs of Orthopterans.     

Light- and electron-microscopic analysis of a complex sensory organ: The tegula of Locusta migratoria

Summary Structure and organization of the tegula, a cupola-shaped structure located at the anterior base of the wings of locusts, is described using various morphological methods. Based on histological and cytological criteria, two different sensory systems are distinguished: (1) a field of mechanoreceptive hairs, and (2) a chordotonal organ. The total number of sensory cells corresponds to the number of axons within the nerve supporting the tegula. The hairs are situated at the posterior region of the tegula, and each hair is innervated by only one sensory cell. The complex architecture of the chordotonal organ is analyzed and the attachment of the scolopidia to the cuticle is described. A single scolopidium makes contact with several epidermal cells. The attachment cells run in parallel and are oriented longitudinally within the tegula, being connected to each other and to the epidermal cells by desmosomes. A function in relation to wing movements during flight is suggested for the two sensory systems within the mixed sense organ, tegula.     

Physiology of vibration-sensitive afferents in the femoral chordotonal organ of the stick insect

The femoral chordotonal organ in orthopterans signals proprioceptive sensory information concerning the femur-tibia joint to the central nervous system. In the stick insect, 80 out of 500 afferents sense tibial position, velocity, or acceleration. It has been assumed that the other sensory cells in the chordotonal organ would serve as vibration detectors. Extracellular recordings from the femoral chordotonal organ nerve in fact revealed a sensitivity of the sense organ for vibrations with frequencies ranging from 10 Hz to 4 kHz, with a maximum sensitivity between 200 and 800 Hz. Single vibration-sensitive afferents responded to the same range of frequencies. Their spike activity depended on acceleration amplitude and displacement amplitude of the vibration stimulus. Additionally, 80% of the vibration-sensitive afferents received indirect presynaptic inputs from themselves or from other afferents of the femoral chordotonal organ, the amplitude of which depended on stimulus frequency and displacement amplitude. They were associated with a decrease of input resistance in the afferent terminal. From the present investigation we conclude that the femoral chordotonal organ of the stick insect is a bifunctional sensory organ that, on the one hand, measures position and movement of the tibia and, on the other hand, detects vibration of the tibia. Accepted: 6 November 1998     

Sensory organs of the antennae and mouthparts of beetle larvae (Coleoptera)

The sensilla located on the antennae and maxillary and labial palps of the larvae of 64 beetle species from 22 families were studied using electron microscopy. The larvae of beetles living in different habitats and having different trophic specializations possess a uniform structure of the sensory organs. They are composed of two groups of sensilla on the apical and subapical segments of the antennae, one apical group of sensilla on both maxillary and labial palps, and one or several digitiform sensilla on the lateral surface of the maxillary and, occasionally, labial palp. The external morphology of the sensory organs is adaptive and represents modifications of the initial type. Band-shaped sensilla or placoid sensilla, clearly different from the initial sensory organs, appear in some taxa as rare exceptions, while other groups display either partial reduction of the receptor organs (Gyrinidae) or reduction of the cuticular parts of the sensilla (Cantharidae).     

昆虫弦音器及其声音感受分子机制

弦音器是昆虫类特有的一种机械感受器,亦称弦音感受器或剑梢感受器。它主要具有感知外界声压和体内肌肉运动的听觉功能,研究弦音器的机能结构对揭秘昆虫听觉的神经机制有重要的科学意义。本文从弦音器多样性和进化入手,重点综述了弦音器的微细结构、基因功能定位、声音感受分子机制及其声压增幅分子生物物理学原理,为昆虫听觉仿生学的研究提供了理论依据。     

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.     

The structure of a hair mechanoreceptor in the antennule of crayfish (Crustacea)

Summary In this study we examine the fine structure of mechanosensory hairs in the antennule of crayfish. The sensory hair is a stiff shaft with feather-like filaments. The hair's base is a large expansion of membrane which allows the hair shaft to deflect. The sensory transducing elements are located far from the hair, but are coupled mechanically with the hair shaft by a fine extracellular chorda. The sensory element is a type of scolopidium which consists of a scolopale cell and three sensory cells with a 9 + 0 type ciliary process.This type of scolopidium is characteristic of the chordotonal organ that has no cuticular structure on the surface of the exoskeleton. In this crustacean hair receptor, the deflection of the cuticular hair is transmitted through the chorda to the scolopidium which is a tension-sensitive transducer. The present study reveals that the mechanosensory hair of decapod crustaceans is a chordotonal organ accompanied by a cuticular hair structure. We also discuss comparative aspects of cuticular and subcuticular chordotonal organs in arthropods.     

Selective expression of glionexin,a glial glycoprotein,in insect mechanoreceptors

The distribution of a glial cell-associated glycoprotein, glionexin (GX), on sensory receptors of the adult cricket Acheta domesticus is described, using the monoclonal antibody 5B12 as an immunohistochemical probe. GX was previously shown to be widely distributed in the embryo and to persist in the postembryonic to adult central nervous system. Here we demonstrate that it is restricted in the adult periphery to three subclasses of mechano-receptor sensilla: large socketed hair mechanoreceptors, their associated campaniform sensilla, and chordotonal organs. GX was not detected in photoreceptors, chemoreceptors, or other mechanoreceptors. The pattern of distribution differs significantly within the three subclasses of mechanoreceptors. In the hair and campaniform receptors GX is restricted to the extracellular space among glial cells clustered around the axon hillock region, but in chordotonal organs it surrounds the scolopidium at the tip of dendrites. The highly restricted distribution of GX in the periphery suggests possible functions that include mechanical stability of the sensory apparatus and ionic homeostasis in the respective neuronal spike-generating regions. The developmental modulation of GX expression is taken to imply multiple functions for the molecule during the life of the insect. 1994 John Wiley & Sons, Inc.     

Bimodal innervation of the infrared organ of Merimna atrata (Coleoptera,Buprestidae) by thermo- and mechanosensory units

The pyrophilous Australian “fire-beetle” Merimna atrata approaches forest fires and possesses abdominal infrared (IR) organs. Each round IR organ is centrally innervated by a sensory complex showing two different units: one thermoreceptive multipolar neuron and one mechanosensitive chordotonal organ (CO) consisting of two scolopidia. We investigated the CO and found that the scolopidia are mononematic (the scolopale cap remains below the cuticle) and monodynal (one sensory cell per scolopidium). The dendrites of the scolopidia extend anteriorly and are attached by their caps to the cuticle about in the middle of the absorbing area. Structural features at the site of innervation suggest that the CO measures minute thermal deformations caused by IR absorption. Therefore, an additional photomechanic component which has been described for the IR receptors of pyrophilous jewel beetles of the genus Melanophila can be proposed for the IR organ of Merimna. Because scolopidia can measure displacements in the subnanometer range, the CO may enhance the sensitivity of the IR organ. The sensory complex of the Merimna IR organ shows the same units and similar cuticular modifications as the tympanal organs of some noctuid moths. Therefore, a parallel evolution of insect ears and the Merimna IR organ is discussed.