Features of the receptors of the alar system of locusts which have lost their ability to fly

Using two species of locusts, Romalia microptera Beavy and Podisma pedestris L., receptors of the wing apparatus are described: campaniform sensillas of the wing, hair receptors of the tegula, chordotonal organ and thorax stretch receptor. A comparative analysis of the receptors mentioned with the homologous sensitive organs, participating in the control of wing movements, is performed in well flying species (Locusta migratoria migratorioides and Schistocerca gregaria). Loss of ability to fly is accompanied with a sharp decrease in the wing campaniform sensillas and in the tegula proprioceptive hairs. Simultaneously, there is loss of connection between the thorax receptors and the wing elements that are present in good flyers. The thorax stretch receptor begins to innervate the longitudinal dorsal muscle, as it is observed in the abdominal segments. The data obtained make it possible to speak about homology of the tergal chordotonal organs and the thorax and abdomen stretch receptors and about the pathways of their evolution, when the insects obtain and loose their ability to fly.     

Proprioceptive activity of the wing-hinge stretch receptor in Manduca sexta and other atympanate moths: a study of the noctuoid moth ear B cell homologue

A multiterminal neurone, recently identified at the wing-hinge of the atympanate moth Manduca sexta, is shown to respond as a proprioceptor monitoring elevatory movements of the hind wing. Extracellular recordings from the individual receptor axon confirm this cell to be the source of the spontaneous and regular discharge observed in previous recordings of peripheral nerve 3N1b1. When the wing is raised, this tonic discharge rate increases proportionally with the angle of elevation. When the wing is displaced sinusoidally at a low frequency, the receptor discharge is modulated throughout the wing beat, increasing steadily to a maximum at the top of the upstroke, then slowly decreasing to a minimum at the bottom of the downstroke. At higher wing-beat frequencies, a phasic burst of activity occurs near the top of the upstroke, followed by a silent period during the down-stroke. Video-microscopic observations of the wing-hinge during active, stationary flight suggest that the receptor is stimulated by the stretching of its peripheral attachment, the subalar membrane. Stretch receptor sensitivity to wing movement is demonstrated in representatives of 4 lepidopteran families, suggesting that the proprioceptive response is widespread among the Lepidoptera. The functional role of the wing-hinge receptor, and its proposed homologous relationship to both the B cell of the noctuoid moth ear, and the locust wing-hinge stretch receptor are discussed.Abbreviations CO chordotonal organ - EGAA Enhanced Graphics Acquisition and Analysis System - HP hair plate - 3N1b1 tympanal nerve - SR stretch receptor     

Recruitment of ectodermal attachment cells via an EGFR-dependent mechanism during the organogenesis of Drosophila proprioceptors

Drosophila proprioceptors (chordotonal organs) are structured as a linear array of four lineage-related cells: a neuron, a glial cell, and two accessory cells, called cap and ligament, between which the neuron is stretched. To function properly as stretch receptors, chordotonal organs must be stably anchored at both edges. The cap cells are anchored to the cuticle through specialized lineage-related attachment cells. However, the mechanism by which the ligament cells at the other edge of the organ attach is not known. Here, we report the identification of specialized attachment cells that anchor the ligament cells of pentascolopidial chordotonal organs (lch5) to the cuticle. The ligament attachment cells are recruited by the approaching ligament cells upon reaching their attachment site, through an EGFR-dependent mechanism. Molecular characterization of lch5 attachment cells demonstrated that they share significant properties with Drosophila tendon cells and with mammalian proprioceptive organs.     

Evolution of the metathoracic tympanal ear and its mesothoracic homologue in the Macrolepidoptera (Insecta)

Two independent methods of comparison, serial homology and phylogenetic character mapping, are employed to investigate the evolutionary origin of the noctuoid moth (Noctuoidea) ear sensory organ. First, neurobiotin and Janus green B staining techniques are used to describe a novel mesothoracic chordotonal organ in the hawkmoth, Manduca sexta, which is shown to be serially homologous to the noctuoid metathoracic tympanal organ. This chordotonal organ comprises a proximal scolopidial region with three bipolar sensory cells, and a long flexible strand (composed of attachment cells) that connects peripherally to an unspecialized membrane ventral to the axillary cord of the fore-wing. Homology to the tympanal chordotonal organ in the Noctuoidea is proposed from anatomical comparisons of the meso- and metathoracic nerve branches and their corresponding peripheral attachment sites. Second, the general structure (noting sensory cell numbers, gross anatomy, and location of peripheral attachment sites) of both meso- and metathoracic organs is surveyed in 23 species representing seven superfamilies of the Lepidoptera. The structure of the wing-hinge chordotonal organ in both thoracic segments was found to be remarkably conserved in all superfamilies of the Macrolepidoptera examined except the Noctuoidea, where fewer than three cells occur in the metathoracic ear (one cell in representatives of the Notodontidae and two cells in those of other families examined), and at the mesothoracic wing-hinge (two cells) in the Notodontidae only. By mapping cell numbers onto current phylogenies of the Macrolepidoptera, we demonstrate that the three-celled wing-hinge chordotonal organ, believed to be a wing proprioceptor, represents the plesiomorphic state from which the tympanal organ in the Noctuoidea evolved. This ’trend toward simplicity’ in the noctuoid ear contrasts an apparent ’trend toward complexity’ in several other insect hearing organs where atympanate homologues have been studied. The advantages to having fewer rather than more cells in the moth ear, which functions primarily to detect the echolocation calls of bats, is discussed. Accepted: 18 June 1999     

Synaptic connections between sensory afferents and the common inhibitory motoneuron in crayfish

The sensory inputs to the common inhibitory motoneuron that innervates every leg muscle of the crayfish Procambarus clarkii (Girard) were analyzed by performing intracellular recordings from its neurite within the neuropil of the 5th thoracic ganglion. Two types of sensory inputs involved in locomotion were studied, those from a movement coding proprioceptor (the coxobasal chordotonal organ) and those from sensory neu rons coding contact forces exerted at the tip of the leg on the substrate (the dactyl sensory afferents). Sinusoidal movements applied to the chordotonal organ strand induced a stable biphasic response in the common inhibitory motoneuron that consisted of bursts of spikes during release and stretch of the strand, corresponding to raising and lowering of the leg, respectively. Using ramp movements imposed on the chordotonal strand, we demonstrated that only movement-coding chordotonal afferents produce excitatory post-synaptic potentials in the common inhibitory motoneuron; these connections are monosynaptic. Mechanical or electrical stimulation of the dactyl sensory afferents resulted in an increase in the tonic discharge of the common inhibitory motoneuron through polysynaptic excitatory pathways. These two types of sensory cues reinforce the central command of the common inhibitory motoneuron and contribute to enhancing its activity during leg movements, and thus facilitate the relaxation of tonic muscle fibres during locomotion.Abbreviations ADR anterior distal root - A Lev anterior levator nerve - CB coxo-basipodite joint - CBCO coxo-basal chordotonal organ - CI common inhibitory motoneuron - Dep depressor nerve - DSA dactyl sensory afferents - EPSP excitatory post-synaptic potential - IN interneuron - MN motoneuron - PDR posterior distal root - P Lev posterior levator nerve - Pro promotor nerve - Rem remotor nerve     

Responses and locations of neurones in the locust metathoracic femoral chordotonal organ

Summary Insect legs possess chordotonal organs which monitor leg angle, and the direction, velocity and acceleration of leg movements. The locust metathoracic femoral chordotonal organ (mtFCO) has previously been studied morphologically and physiologically, but no detailed analysis of the responses of individual neurones, and their location in the organ has so far been produced. By recording from, and staining mtFCO neurones I have been able to compile for the first time such a map. The distribution of neurone somata in the locust mtFCO is more complex than previously thought: receptors sensitive to both stretch and relaxation of the apodeme are distributed throughout the organ. Seventeen response types were encountered. Neurones with a particular response type have somata in comparable locations within the mtFCO. Comparisons are made between the response types found in the stick insect and those in the locust. The possible functions of some of the responses are discussed.Abbreviation (mt)FCO (metathoracic) femoral chordotonal organ - F-T femur-tibia     

Range fractionation in the locust metathoracic femoral chordotonal organ

Summary Insect femoral chordotonal organs are internal proprioceptors which monitor the position and movements of the femur-tibia joint of the leg. The locust (Locusta migratoria) metathoracic femoral chordotonal organ is composed of approximately 100 neurones with a variety of response properties. In this study intracellular recordings were used to examine the range fractionation of phasic and tonic responses to tibial movements. Some neurones responded across the full range of leg angles, while others had restricted response ranges, and could therefore act as labeled lines. Neurones with maximal firing at mid-angles are described for the first time in a locust femoral chordotonal organ. Responses are discussed in terms of underlying structural constraints on signal transduction.Abbreviation (mt) FCO (metathoracic) femoral chordotonal organ     

Innervation of the receptors present at the various joints of the pereiopods and third maxilliped of Homarus gammarus (L.) and other macruran decapods (crustacea)

Summary This paper gives a full account of the number and structure of the chordotonal organs present at all joints between the coxopodite and dactylopodite of the pereiopods and 3rd maxilliped of the macruran Homarus gammarus L. (H. vulgaris M. Ed.). Some comparative data is supplied for other macruran decapods. As the form of the receptors depends to some degree upon the structure of the joint we have included details of musculature, planes of movement and degrees of freedom at each of the joints.The third maxilliped has a smaller number of chordotonal organs than the pereiopod, in particular at the mero-carpopodite and carpopodite-propodite joints where only one organ is present. In some species the propodite-dactylopodite organ is absent from this limb.The electrical activity recordable from the receptors in the 3rd maxilliped shows considerable differences from the corresponding receptors in the pereiopod.The structure of the carpopodite-propodite joint of both limbs is discussed in detail as this joint differs greatly from that of the Brachyura. In the 3rd maxilliped and 2nd pereiopod three muscles are present. In the latter the joint is capable of rotation about the longitudinal axis but the third muscle does not appear to produce this rotation. A small number of units in the CP₂ receptor respond to rotation.A receptor is described in the basipodite of the pereiopod and 3rd maxilliped situated just proximal to the plane through which the limb breaks at autotomy or autospasy. This receptor does not monitor joint movement and may detect cuticular strain, thus preventing accidental autotomy of limbs. A similar receptor has been observed in Carcinus.Cuticular receptor structures (CAP organs) are described as present at the M-C and C-P joints in both limbs, and at the I-M joint of the pereiopod.     

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.     

Proprioceptive reflex interactions with central motor rhythms in the isolated thoracic ganglion of the shore crab

Summary Experiments were carried out on an isolated central nervous system preparation of the shore crab,Carcinus maenas, comprising the fused thoracic ganglion complex with two proprioceptors of one back leg still attached. These, the thoracic-coxal muscle receptor organ and the coxo-basal chordotonal organ, monitor movement and position of the first and second joints, respectively. Motor activity was recorded extracellularly from the central cut ends of the nerves innervating the promotor and remotor muscles of the thoracic-coxal joint, and the levator and depressor muscles of the coxal-basal joint of the same leg. Simultaneous intracellular recordings were made from central processes of individual motoneurones of each muscle.In the absence of any sensory input, the isolated ganglion exhibited rhythmic bursting in the motor nerve roots, with a slow, usually irregular cycle period of 5–50 s.Both receptor organs had both intra-joint and inter-joint effects on the rhythmically active preparation. In most cases the coxo-basal receptor organ had the greater effect.Resistance reflexes initiated by each of the joint proprioceptors were modulated by the rhythmic activity.It may be concluded that, while the isolated thoracic ganglion of the crab is capable of generating rhythmic motor output, proprioceptive feedback from the two basal joints is important in shaping the motor patterns underlying locomotion. Inappropriate reflexes which would impede active movements about these joints are modulated or reversed so as to permit and even reinforce intended locomotory movements.     

The proprioceptive function of a complex chordotonal organ associated with the mesothoracic coxa in locusts

Summary A system of chordotonal organs in the locust mesothorax consists of four subunits one of which connects to the coxa. Proprioceptive afferents from the scoloparia record the rotatory movements of the coxa. Mechanical stimulation of the sensory system by sinusoidal stretch or movements mimicking stretch as in natural walking of the locust elicits reflex activation of coxal motoneurones. Both assistance and resistance reflexes to imposed movements occur, but their intensity can vary from periods of suppression below firing threshold in a motoneurone to recruitment of additional motoneurones to the same muscle. It is concluded that some of these reflexes recorded in isolated preparations can also occur in freely walking animals where they should contribute to the muscular coordination of transitions between antagonistic movements.Abbreviations aCO, cCO, pCO, vCO anterior, coxal, posterior, ventral chordotonal organ - COS chordotonal organ system - pm-al postero-median to anterior-lateral     

Wing receptors of the American cockroach Periplaneta americana]

Wing receptors of the cockroach have been studied using staining technique with methylene blue in living animals. Five types of the receptors were found: trychoid hairs, bristles, complaniform sensillae, chordotonal organs and multiterminal neurons. The majority of the receptors is located at the lower surface of the wing, especially along its ribs. Together with primitive features in the structure (polyneuronal origin of hairs and bristles, poor content of chordotonal organs, absence of distinct groups of companiform sensillae), some specialization of wing receptors with respect to flight function is noted (concentration of proprioceptors along the main mechanical axis of the wing and formation of distinct rows by the companiform sensillae).     

The structure and properties of an abdominal chordotonal organ in Carausius morosus and Blaberus discoidalis

Each side of the abdominal segments of the stick insect Carausius morosus contains a chordotonal organ lying longitudinally in a ventro-lateral position. These ventro-lateral chordotonal organs each possess two nerve cell bodies and two scolopales. There is a single attachment strand to the cuticle.Electrical recordings from the receptors show that they respond in a highly phasic manner to both stretching and subsequent relaxation of the attachment strand. They are sensitive to substrate vibration but are activated by ventilatory movements. The effects of ramp and square wave stimulation are examined. The rôle of the ventro-lateral chordotonal organs as ventilatory receptors is discussed and abdominal chordotonal organs of insects in general are reviewed.The ‘ventral phasic receptors’ of the cockroach are re-examined and shown to be chordotonal organs. They are re-named ‘mid-ventral’ chordotonal organs.     

Parallel processing of proprioceptive information in the terminal abdominal ganglion of the crayfish

The processing of proprioceptive information from the exopodite-endopodite chordotonal organ in the tailfan of the crayfish Procambarus clarkii (Girard) is described. The chordotonal organ monitors relative movements of the exopodite about the endopodite. Displacement of the chordotonal strand elicits a burst of sensory spikes in root 3 of the terminal ganglion which are followed at a short and constant latency by excitatory postsynaptic potentials in interneurones. The afferents make excitatory monosynaptic connections with spiking and nonspiking local interneurones and intersegmental interneurones. No direct connections with motor neurones were found.Individual afferents make divergent patterns of connection onto different classes of interneurone. In turn, interneurones receive convergent inputs from some, but not all, chordotonal afferents. Ascending and spiking local interneurones receive inputs from afferents with velocity thresholds from 2–400°/s, while nonspiking interneurones receive inputs only from afferents with high velocity thresholds (200–400°/s).The reflex effects of chordotonal organ stimulation upon a number of uropod motor neurones are weak. Repetitive stimulation of the chordotonal organ at 850°/s produces a small reduction in the firing frequency of the reductor motor neurone. Injecting depolarizing current into ascending or non-spiking local interneurones that receive direct chordotonal input produces a similar inhibition.     

Strand receptors with central cell bodies in the proximal leg joints of orthopterous insects

In various orthopterous insects backfilling of leg nerve 3B regularly stained, in the thoracic ganglia, small cell bodies that resemble those of central sensory neurons reported in the locust (Br?unig and Hustert 1980). Centrifugal cobalt infusion of this nerve revealed the end organs of those neurons in the periphery. In all species investigated one strand receptor is associated with the trochantin, while two others are situated in the coxa. In addition to these sense organs, the coxa contains a multipolar stretch receptor which spans the coxotrochanteral joint. The absence of chordotonal organs is discussed with reference to earlier work in this field.     

Ultrastructure of a muscle spindle-analogous receptor organ in the mandible of Oncopeltus fasciatus (Insecta,Heteroptera) with remarks on the homology of the mandibular muscles

Summary A non-ciliary muscle receptor organ in the first mandibular retractor muscle of Oncopeltus fasciatus is described. The organ consists of two specialized muscle fibres of the first retractor, which are embedded in a thickened layer of connective tissue. The sensory innervation is supplied by three multiterminal sense cells sending several dendrites to the receptor muscle fibres. Naked dendritic terminals are attached to the muscle surface or connective tissue fibrils. The far-reaching analogy of the receptor to the intrafusal chain-fibres of vertebrate muscle spindles is remarkable. The existence of a muscle receptor organ in the first mandibular retractor may serve as an argument in favor of the homology of this muscle with the musculus tentorio-mandibularis of orthopteroid insects.Supported by a grant from the Deutsche Forschungsgemeinschaft     

Morphology of the central projections of physiologically characterised neurones from the locust metathoracic femoral chordotonal organ

Summary The metathoracic femoral chordotonal organ of the locust (Locusta migratoria) is an internal proprioceptor composed of mechanosensory neurones which respond to tibial position, velocity, or acceleration, or to combinations of these parameters. Discriminant function analyses confirmed the visual observation that neurones with different responses to tibial movements had different central branching patterns. Some aspects of the projections were consistent for all neurones (e.g., the path taken by the main neurite through the metathoracic ganglion), whereas other regions of branches were consistently reduced or missing in some response classes. Some position-and-acceleration receptors had no main branches off the main neurite, and must therefore make relatively restricted contact with motor neurones and interneurones. Phasic or tonic neurones which responded in ranges of tibial extension had branches which projected further medial in Dorsal Commissures III and IV than similar neurones which responded in ranges of tibial flexion. I compare my results to previous studies of mapping in the insect CNS.Abbreviations (ms) (mt)FCO (mesothoracic) (metathoracic) femoral chordotonal organ - ANOVA Analysis of Variance     

Nitric oxide modulates presynaptic afferent depolarization of mechanosensory neurons

In crayfish, movement of the tailfan causes stimulation of exteroceptive sensory hairs located on its surface. Movement is monitored by a proprioceptor, the protopodite-endopodite chordotonal organ within the tailfan. Proprioceptive afferents provide indirect presynaptic inhibitory inputs to sensory hair afferents in the form of primary afferent depolarizations (PADs). Bath application of nitric oxide (NO) substrates, donors and scavengers, and nitric oxide synthase (NOS) inhibitors had no effect on the responses of proprioceptive afferents during imposed movements of the chordotonal organ. In contrast, the amplitude of PADs in exteroceptive hair afferents was dependent on NO levels. NO levels were altered by bath-application of the NO-precursor L-arginine, the NO donor SNAP, the NOS-inhibitor L-NAME, and the NO scavenger PTIO, while changes in PAD amplitude were measured. Application of L-arginine or SNAP resulted in consistent decreases in PAD amplitude, whereas L-NAME and PTIO induced increases in PAD amplitude. These results suggest that endogenous NO decreases inhibitory inputs to exteroceptive neurons, thus enhancing transmitter release at their output synapses.     

A locust chordotonal organ coding for proprioceptive and acoustic stimuli

A chordotonal organ in the prothoracic segment of a locust combines features of a proprioceptive mechanoreceptor and an acoustic organ. This organ is closely associated with the tracheal system in the neck. The central nervous projections of the sensory cells contact neuropiles in all thoracic ganglia with the most dense arborizations in the metathoracic ganglion in close proximity, and even with some overlap, to the projections of tympanic fibres. Physiological experiments show that this organ responds to mechanical displacement of its receptor apodeme and, in addition, to acoustic stimulation via either a region of the cervical membrane which may act as a functional tympanic membrane, or via the tracheal system. Accepted: 14 October 1998     

Monosynaptic excitation of lateral giant fibres by proprioceptive afferents in the crayfish

Giant interneurones mediate a characteristic `tail flip' escape response of the crayfish, Procambarus clarkii, which move it rapidly away from the source of stimulation. We have analysed the synaptic connections of proprioceptive sensory neurones with one type of giant interneurone, the lateral giant. Spikes in sensory neurones innervating an exopodite-endopodite chordotonal organ in the tailfan, which monitors the position and movements of the exopodite, are followed at a short and constant latency by excitatory postsynaptic potentials in a lateral giant interneurone (LG) recorded in the terminal abdominal ganglion. These potentials are unaffected by manipulation of the membrane potential of LG, by bath application of saline with a low calcium concentration, or by one containing the nicotinic antagonist, curare. The potentials evoked in LG by chordotonal organ stimulation are thus thought to be monosynaptic and electrically mediated. This is the first demonstration that LG receives input from sensory receptors other than exteroceptors in the terminal abdominal ganglion. Accepted: 7 April 1997