Scolopidial Sensilla Research Articles

The Subgenual Organ Complex in Stick Insects: Functional Morphology and Mechanical Coupling of a Complex Mechanosensory Organ

Leg chordotonal organs in insects show different adaptations to detect body movements, substrate vibrations, or airborne sound. In the proximal tibia of stick insects occur two chordotonal organs: the subgenual organ, a highly sensitive vibration receptor organ, and the distal organ, of which the function is yet unknown. The distal organ consists of a linear set of scolopidial sensilla extending in the tibia in distal direction toward the tarsus. Similar organs occur in the elaborate hearing organs in crickets and bushcrickets, where the auditory sensilla are closely associated with thin tympanal membranes and auditory trachea in the leg. Here, we document the position and attachment points for the distal organ in three species of stick insects without auditory adaptations (Ramulus artemis,Sipyloidea sipylus, andCarausius morosus). The distal organ is located in the dorsal hemolymph channel and attaches at the proximal end to the dorsal and posterior leg cuticle by tissue strands. The central part of the distal organ is placed closer to the dorsal cuticle and is suspended by fine tissue strands. The anterior part is clearly separated from the tracheae, while the distal part of the organ is placed over the anterior trachea. The distal organ is not connected to a tendon or muscle, which would indicate a proprioceptive function. The sensilla in the distal organ have dendrites oriented in distal direction in the leg. This morphology does not reveal obvious auditory adaptations as in tympanal organs, while the position in the hemolymph channel and the direction of dendrites indicate responses to forces in longitudinal direction of the leg, likely vibrational stimuli transmitted in the leg’s hemolymph. The evolutionary convergence of complex chordotonal organs with linear sensilla sets between tympanal hearing organs and atympanate organs in stick insects is emphasized by the different functional morphologies and sensory specializations.

Early postembryogenic development of the subgenual organ complex in the stick insect Sipyloidea sipylus

Stick insects have elaborate mechanosensory organs in their subgenual organ complex in the proximal tibia, particularly the distal organ with scolopidial sensilla in linear arrangement. For early postembryonic developmental stages of Sipyloidea sipylus (Phasmatodea: Necrosciinae), the neuroanatomy of the scolopidial organs in the subgenual organ complex and the campaniform sensilla is documented by retrograde axonal tracing, and compared to the adult neuroanatomy. Already after hatching of the first larval instars are the sensory structures of subgenual organ and distal organ as well as tibial campaniform sensilla differentiated. In the distal organ, the full set of sensilla is shown in all larval stages examined. This finding indicates that the sensory organs differentiate during embryogenesis, and are already functional by the time of hatching. The constancy of distal organ sensilla over postembryonic stages allows investigation of the representative number of sensilla in adult animals as well as in larval instars. Some anatomical changes occur by postembryogenic length increase of the distal organ, and grouping of the anterior subgenual sensilla. The embryonic development of scolopidial sensilla is similar for auditory sensilla in hemimetabolous Orthoptera (locusts, bushcrickets, crickets) where tympanal membranes develop during postembryogenic stages, conferring a successive gain of sensitivity with larval moults.

What determines the number of auditory sensilla in the tympanal hearing organs of Tettigoniidae? Perspectives from comparative neuroanatomy and evolutionary forces

Insects have evolved complex receptor organs for the major sensory modalities. For the sense of hearing, the tympanal organ of Tettigoniidae (bush crickets or katydids) shows remarkable convergence to vertebrate hearing by impedance conversion and tonotopic frequency analysis. The main auditory receptors are scolopidial sensilla in thecrista acustica. Morphological studies established that the numbers of auditory sensilla are species-specific. However, the factors determining the specific number of auditory sensilla are not well understood. This review provides an overview of the functional organization of the auditory organ in Tettigoniidae, including the diversification of thecrista acusticasensilla, a list of species with the numbers of auditory sensilla, and a discussion of evolutionary forces affecting the number of sensilla in thecrista acusticaand their sensitivity. While all species of Tettigoniidae studied so far have acrista acustica, the number of sensilla varies on average from 15–116. While the relative differences or divergence in sensillum numbers may be explained by adaptive or regressive changes, it is more difficult to explain a specific number of sensilla in thecrista acusticaof a specific species (like for the model speciesAncistrura nigrovittata,Copiphora gorgonensis,Gampsocleis gratiosa,Mecopoda elongata,Requena verticalis, orTettigonia viridissima): sexual and natural selection as well as allometric relationships have been identified as key factors influencing the number of sensilla. Sexual selection affects the number of auditory sensilla in thecrista acusticaby the communication system and call patterns. Further, positive allometric relationships indicate positive selection for certain traits. Loss of selection leads to evolutionary regression of the auditory system and reduced number of auditory sensilla. This diversity in the auditory sensilla can be best addressed by comparative studies reconstructing adaptive or regressive changes in thecrista acustica.

The complex tibial organ of the New Zealand ground weta: sensory adaptations for vibrational signal detection

In orthopteran insects, a complex tibial organ has evolved to detect substrate vibrations and/or airborne sound. Species of New Zealand weta (Anostostomatidae) with tympanal ears on the foreleg tibia use this organ to communicate by sound, while in atympanate species (which communicate by substrate drumming) the organ is unstudied. We investigated the complex tibial organ of the atympanate ground weta, Hemiandrus pallitarsis, for vibration detection adaptations. This system contains four sensory components (subgenual organ, intermediate organ, crista acustica homolog, accessory organ) in all legs, together with up to 90 scolopidial sensilla. Microcomputed tomography shows that the subgenual organ spans the hemolymph channel, with attachments suggesting that hemolymph oscillations displace the organ in a hinged-plate fashion. Subgenual sensilla are likely excited by substrate oscillations transmitted within the leg. Instead of the usual suspension within the middle of the tibial cavity, we show that the intermediate organ and crista acustica homolog comprise a cellular mass broadly attached to the anterior tibial wall. They likely detect cuticular vibrations, and not airborne sound. This atympanate complex tibial organ shows elaborate structural changes suggesting detection of vibrational stimuli by parallel input pathways, thus correlating well with the burrowing lifestyle and communication by substrate-transmitted vibration.

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.

Vibrational sensitivity of the subgenual organ complex in female Sipyloidea sipylus stick insects in different experimental paradigms of stimulus direction, leg attachment, and ablation of a connective tibial sense organ

We document the sensitivity to sinusoidal vibrations for chordotonal organs in the stick insect tibia (Sipyloidea sipylus). In the tibia, the scolopidial subgenual organ (~40 scolopidial sensilla), distal organ (~20 scolopidial sensilla), and distal tibial chordotonal organ (~7 scolopidial sensilla) are present. We study the sensitivity of tibial sensory organs in all leg pairs to vibration stimuli as sensory thresholds by recording summed action potentials from Nervus cruris in the femur. The tibia was stimulated with a minishaker delivering vibrational stimuli. Because different experimental procedures may affect the vibration sensitivity, we here analysed possible effects of different experimental conditions: (1) the stimulus direction delivered in either horizontal or vertical direction to the leg; (2) recording responses only from the subgenual organ complex after ablation of the distal tibial chordotonal organ, and (3) the attachment of the leg to the minishaker by plastilin, beeswax-colophony, or freely standing legs. The tibial scolopidial organs give summed responses to vibration stimuli with highest sensitivity between 500 and 1000Hz for all leg pairs. In the different experimental series, we find that (1) thresholds were influenced by stimulation direction with lower thresholds in response to vertical vibrations, (2) ablating the distal tibial chordotonal organ by cutting the distal-most tibia did not change the summed sensory thresholds significantly, and (3) the attachment material between legs and the minishaker (plastilin or beeswax-colophony mixture) did not significant influence the sensory thresholds against free-standing tarsi. The distal tibial chordotonal organ is a connective chordotonal organ attached to a tendon and is likely a proprioceptive organ. These results emphasise that vibrational thresholds are mainly direction-sensitive. Thus, the direction of stimulus delivery during electrophysiological recordings is relevant for comparisons of vibratory sensory thresholds.

How many mechanosensory organs in the bushcricket leg? Neuroanatomy of the scolopidial accessory organ in Tettigoniidae (Insecta: Orthoptera)

The subgenual organ and associated scolopidial organs are well studied in Orthoptera and related taxa. In some insects, a small accessory organ or Nebenorgan is described posterior to the subgenual organ. In Tettigoniidae (Ensifera), the accessory organ has only been noted in one species though tibial sensory organs are well studied for neuroanatomy and physiology. Here, we use axonal tracing to analyse the posterior subgenual organ innervated by the main motor nerve. Investigating seven species from different groups of Tettigoniidae, we describe a small group of scolopidial sensilla (5–9 sensory neurons) which has features characteristic of the accessory organ: posterior tibial position, innervation by the main leg nerve rather than by the tympanal nerve, orientation of dendrites in proximal or ventro-proximal direction in the leg, and commonly association with a single campaniform sensillum. The neuroanatomy is highly similar between leg pairs. We show differences in the innervation in two species of the genus Poecilimon as compared to the other species. In Poecilimon, the sensilla of the accessory organ are innervated by one nerve branch together with the subgenual organ. The results suggest that the accessory organ is part of the sensory bauplan in the leg of Tettigoniidae and probably Ensifera.

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

AbstractMechanoreceptor 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.

Serotonin‐immunoreactive sensory neurons in the antenna of the cockroach Periplaneta americana

The antennae of insects contain a vast array of sensory neurons that process olfactory, gustatory, mechanosensory, hygrosensory, and thermosensory information. Except those with multimodal functions, most sensory neurons use acetylcholine as a neurotransmitter. Using immunohistochemistry combined with retrograde staining of antennal sensory neurons in the cockroach Periplaneta americana, we found serotonin-immunoreactive sensory neurons in the antenna. These were selectively distributed in chaetic and scolopidial sensilla and in the scape, the pedicel, and first 15 segments of the flagellum. In a chaetic sensillum, A single serotonin-immunoreactive sensory neuron cohabited with up to four serotonin-negative sensory neurons. Based on their morphological features, serotonin-immunopositive and -negative sensory neurons might process mechanosensory and contact chemosensory modalities, respectively. Scolopidial sensilla constitute the chordotonal and Johnston's organs within the pedicel and process antennal vibrations. Immunoelectron microscopy clearly revealed that serotonin-immunoreactivities selectively localize to a specific type of mechanosensory neuron, called type 1 sensory neuron. In a chordotonal scolopidial sensillum, a serotonin-immunoreactive type 1 neuron always paired with a serotonin-negative type 1 neuron. Conversely, serotonin-immunopositive and -negative type 1 neurons were randomly distributed in Johnston's organ. In the deutocerebrum, serotonin-immunoreactive sensory neuron axons formed three different sensory tracts and those from distinct types of sensilla terminated in distinct brain regions. Our findings indicate that a biogenic amine, serotonin, may act as a neurotransmitter in peripheral mechanosensory neurons.

Sensory neuroanatomy of stick insects highlights the evolutionary diversity of the orthopteroid subgenual organ complex

The subgenual organ is a scolopidial sense organ located in the tibia of many insects. In this study the neuroanatomy of the subgenual organ complex of stick insects is clarified for two species, Carausius morosus and Siyploidea sipylus. Neuronal tracing shows a subgenual organ complex that consists of a subgenual organ and a distal organ. There are no differences in neuroanatomy between the three thoracic leg pairs, and the sensory structures are highly similar in both species. A comparison of the neuroanatomy with other orthopteroid insects highlights two features unique in Phasmatodea. The subgenual organ contains a set of densely arranged sensory neurons in the anterior-ventral part of the organ, and a distal organ with 16-17 scolopidial sensilla in C. morosus and 20-22 scolopidial sensilla in S. sipylus. The somata of sensory neurons in the distal organ are organized in a linear array extending distally into the tibia, with only a few exceptions of closely associated neurons. The stick insect sense organs show a case of an elaborate scolopidial sense organ that evolved in addition to the subgenual organ. The neuroanatomy of stick insects is compared to that studied in other orthopteroid taxa (cockroaches, locusts, crickets, tettigoniids). The comparison of sensory structures indicates that elaborate scolopidial organs have evolved repeatedly among orthopteroids. The distal organ in stick insects has the highest number of sensory neurons known for distal organs so far.

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.

Putative Chordotonal Organ in the Fore Coxae of Adult Callosobruchus maculatus and C. subinnotatus (Coleoptera: Bruchidae)

A unique chordotonal structure in the fore coxae of adult male and female bruchid beetles, Callosobruchus maculatus (F.) and C. subinnotatus (Pic), is described. The structure is a heavily sclerotized cuticular cone that is recessed within an opening in the medial surface of the coxa. Perpendicular to the cuticular cone is a pair of scolopidial sensilla with bipolar neurons, cap cells, scolopale sheath, and accessory cells. Unlike scolopidia described from other insects, these sensilla have a free distal tip that opens into a crotch in the distal inside surface of the coxa.

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 ° and 60 ° 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.

Structure of the abdominal receptor responsive to internally applied pressure in the blood-feeding insect, Rhodnius prolixus

The sensory receptor responsive to pressure applied internally to the ventral abdominal body wall of the blood-feeding insects, Rhodnius prolixus, is a single sense cell containing, at its distal end, a cilium enclosed within a scolopale, a densely staining structure characteristic of insect scolopidial sensilla. A small spherical structure lies within a dilation near the midregion of the cilium, and contains nine heavily staining bodies, the position of each corresponding to a pair of microtubules in the cilium. Proximal to the dilation, the microtubules are organized in a ring of nine pairs with one microtubule of each pair associated with dyneinlike arms. Dastal to the dilation a central pair of microtubules is present, but dyneinlike arms are absent. The scolopale cell, which gives risc to the scolopale, has cytoplasmic invaginations that form an elaborate array of extracellular compartments surrounding the body wall of the sense cell. These compartments may serve to dampen high frequency vibrations permitting the receptor to respond to pressure exerted by touch, an attribute in keeping with the receptor's proposed function of detecting abdominal distension related to the size and movement of the stomach.

Morphology and fine structure of mouthpart sensilla in the dark-sided cutworm Euxoa messoria (Harris) (Lepidoptera : Noctuidae)

The present study describes the fine structure of sensilla on the maxillary palps, galeae, labial palps, and labrum of the dark-sided cutworm, Euxoa messoria (Harris) (Lepidoptera : Noctuidae). Ten types of sensilla were identified and a total of 144 bipolar sense cells were observed. Each palp bears a group of 8 terminal uniporous pegs, 1 large and 2 small subterminal multiporous plate sensilla and a digitiform sensillum. Also associated with the walls are 3 scolopidial sensilla and a companiform-like sensillum. Each galea bears 2 large segmented uniporous pegs, a campaniform sensillum, 2 aporous papillae, and a small, spike-shaped, aporous peg. Each labial palp bears 2 cone-shaped sensilla. Externally, the labrum bears 12 aporous hairs, and internally, 6 aporous hairs and 1 pair of campaniform sensilla. The ultrastructural evidence suggests that the uniporous pegs and multiporous plate sensilla are chemosensory and that the hairs, aporous papillae, aporous cones, digitiform sensillum, scolopidial sensilla, campaniform, and campaniform-like sensilla are mechanosensory. From the structural evidence, no role could be assigned to the aporous spike-shaped pegs on the galeae. The multiporous plate sensilla resemble olfactory sensilla, and appear to be a new type of sensillum. Two-thirds of the observed neurons innervate the chemosensilla. The maxillary palps have approximately 4 times as many contact chemosensory neurons as the galeae, suggesting that they have an important role in gustation.