Origin and development of unusual insect muscle tension receptors

This work describes the origin and development of about 200 tension receptor cells located around the anterior attachment site of the locust ovipositor muscle and their migration to their final position on the muscle fibres. The locust ovipositor muscle is the only insect system in which more than 100 tension receptor cells are associated with a single muscle. Neuronal precursors of tension receptors are first detectable by horseradish peroxidase immunohistochemistry in fourth instar larvae. Precursors consist of cell clusters (doublets, triplets and quadruplets) located on the anterior attachment site of the muscle. In the early fifth larval stage, cell clusters are absent, although a few sensory neurons that lie embedded between the muscle fibres are apparent. These neurons send their dendrites towards the anterior end of the muscle fibres and their axons posteriorly. By the fourth day of the fifth larval stage, a large number of cell clusters appears on the anterior muscle attachment site. In addition to these assemblies, cells have been identified that extend long processes running exactly along the lateral margin of the attachment site. These cells are thought to provide navigating cues for migrating tension receptors, since they are absent in later stages. By the end of the fifth larval stage, most of the clusters gradually disappear and increasing numbers of differentiated neurons embedded between the muscle fibres become visible. We conclude that the majority of tension receptors develop during the last larval stage from precursors situated on the muscle apodeme. They then migrate from the apodeme to their final place on the muscle fibres where they assume an appropriate orientation.     

Neural mechanism for generating and switching motor patterns of rhythmic movements of ovipositor valves in the cricket

In adult female crickets (Gryllus bimaculatus), rhythmic movements of ovipositor valves are produced by contractions of a set of ovipositor muscles that mediate egg-laying behavior. Recordings from implanted wire electrodes in the ovipositor muscles of freely moving crickets revealed sequential changes in the temporal pattern of motor activity that corresponded to shifts between behavioral steps: penetration of the ovipositor into a substrate, deposition of eggs, and withdrawal of the ovipositor from the substrate. We aimed in this study to illustrate the neuronal organization producing these motor patterns and the pattern-switching mechanism during the behavioral sequence. Firstly, we obtained intracellular recordings in tethered preparations, and identified 12 types of interneurons that were involved in the rhythmic activity of the ovipositor muscles. These interneurons fell into two classes: ‘initiator interneurons’ in which excitation preceded the rhythmic contractions of ovipositor muscles, and ‘oscillator interneurons’ in which the rhythmic oscillation and spike bursting occurred in sync with the oviposition motor rhythm. One of the oscillator interneurons exhibited different depolarization patterns in the penetration and deposition motor rhythms. It is likely that some of the oscillator interneurons are involved in producing different oviposition motor patterns. Secondly, we analyzed oviposition motor patterns when the mecahnosensory hairs located on the inside surface of the dorsal ovipositor valves were removed. In deafferented preparations, the sequential change from deposition to withdrawal did not occur. Therefore, the switching from deposition pattern to withdrawal pattern is signaled by the hair sensilla that detect the passage of an egg just before it is expelled.     

Superextension and supercontraction in locust ovipositor muscles

A ten times elongation of certain abdominal intersegmental muscles occurs in female locusts during digging prior to oviposition. During and after oviposition the muscles contract, shortening by up to 90% or more, restoring the resting positions of the abdominal segments.Discontinuous Z-discs permit supercontraction at the resting length and then fragment into Z-bodies when the muscle is stretched, so enabling it to superextend without loss of the contractile property. In this superextended state the fibres resemble smooth muscles. After oviposition, the muscle fibres contract but the sarcomeres are not restored completely, some of the Z-bodies being unevenly distributed in the recontracted fibres. Locust ovipositor muscle has the most extreme example of Z-disc disagregation known from the insects and is the insect muscle which approaches most closely the smooth muscle condition.Two types of motor nerve innervate this muscle, one is ordinary and the other, containing granules, resembles an octopaminergic fibre possibly involved in regulating a catch mechanism in the muscle.The physiological requirements for egg-laying with an extensible ovipositor, which is also part of the normally functioning abdomen, are well met by the ultrastructural specializations of locust ovipositor muscles.     

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Mechanosensory activity was recorded extracellularly from branches of the internal pedal nerve in the femur of the horseshoe crab walking leg. The receptors appeared to be associated with the tibial flexor muscles and generally showed little spontaneous activity in the isolated leg. Sensory activity was most easily and reliably elicited by active flexor contraction against a load, and it did not require joint movement. The neurons responsible for this activity appear to be true series tension receptors. Since such cells are likely to be adequately stimulated only by tension developed in muscle fibers with which they are in series, whole muscle tension is not always directly related to the activity of a given receptor. In order to estimate the magnitude of the force at a receptor under study various indirect methods of altering the tension in and spatial relationships between the fibres of a single muscle were employed. These include active stimulation while (a) fixing the muscle at various lengths (joint angles), (b) lengthening or shortening the muscle passively over a wide range and at varying rates. The results obtained are consistent with the suggestion that the sensory cells are series tension receptors.     

Neuroanatomical and electrophysiological studies of identified contact chemoreceptors on the ventral ovipositor valve of 3rd instar larvae of lubber grasshoppers (Taeniopoda eques)

A large number of contact chemoreceptors are located on the ovipositor valves of adult female grasshoppers. These receptors play an important role in many aspects of grasshopper life such as detecting the chemical composition of the soil before and during oviposition. It is surprising, however, to find these types of receptors on the ovipositor valves of instar larvae which are not able to oviposit. Thus, these receptors may serve functions other than to search for a suitable site for egg laying. Observation under the scanning electron microscope revealed the presence of uniporous basiconic contact chemoreceptors in addition to different types of trichoid mechanoreceptors on the ovipositor valve of lubber grasshopper 3rd instar larvae. Neuroanatomical studies have shown that these sensilla are multiply innervated, containing one mechanosensory neuron and four chemosensory neurons that project locally and intersegmentally. The tip recording technique from single basiconic sensilla demonstrated mechanosensory responses to deflections of the sensillum as well as gustatory activity when in contact with different chemical solutions. The electrophysiological studies have shown that these sensilla serve as contact chemoreceptors and not as olfactory receptors.     

Ultrastructural analysis of spinal primary afferent fibers within the circular muscle of the cat lower esophageal sphincter

We have analyzed the ultrastructural characteristics and environment of spinal primary afferent fibers that run within the circular muscle of the cat lower esophageal sphincter. These were selectively labeled by anterogradely transported cholera toxin B subunit conjugated with horseradish peroxidase. Most of the labeled fibers were perpendicular to the muscle cells but some ran sinuously or parallel to the muscle cells. All the labeled fibers were unmyelinated and exhibited relatively rare varicosities. Most of the fibers were in large nerve fiber bundles surrounded by perineurium and probably project to the mucosa. Only some fibers that were in small nerve fiber bundles with no perineurium ran parallel to the musculature and established close relationships with smooth muscle cells. They might be a small subpopulation of the spinal tension receptors, most of the other spinal tension receptors being located in the myenteric plexus area, between the circular and longitudinal muscle. Accepted: 2 December 1999     

Motor control of the mandible closer muscle in ants

Despite their simple design, ant mandible movements cover a wide range of forces, velocities and amplitudes. The mandible is controlled by the mandible closer muscle, which is composed of two functionally distinct subpopulations of muscle fiber types: fast fibers (short sarcomeres) and slow ones (long sarcomeres). The entire muscle is controlled by 10-12 motor neurons, 4-5 of which exclusively supply fast muscle fibers. Slow muscle fibers comprise a posterior and an antero-lateral group, each of which is controlled by 1-2 motor neurons. In addition, 3-4 motor neurons control all muscle fibers together. Simultaneous recordings of muscle activity and mandible movement reveal that fast movements require rapid contractions of fast muscle fibers. Slow and subtle movements result from the activation of slow muscle fibers. Forceful movements are generated by simultaneous co-activation of all muscle fiber types. Retrograde tracing shows that most dendritic arborizations of the different sets of motor neurons share the same neuropil in the subesophageal ganglion. In addition, fast motor neurons and neurons supplying the lateral group of slow closer muscle fibers each invade specific parts of the neuropil that is not shared by the other motor neuron groups. Some bilateral overlap between the dendrites of left and right motor neurons exists, particularly in fast motor neurons. The results explain how a single muscle is able to control the different movement parameters required for the proper function of ant mandibles.     

The role of sensory input in maintaining output from the locust oviposition digging central pattern generator

Summary A quantitative EMG analysis is presented of the effects of deafferentation on the motor program for oviposition digging in the locust Locusta migratoria. We examined the activity of two groups of antagonistic muscles, the opener and closer muscles of the ventral ovipositor valves, in terms of the cycle frequency, burst duration, and relative burst onset times. There were no significant differences between the pattern frequency produced in intact, semi-intact, or deafferented animals within 10 min of the onset of the pattern. Over time, however, the pattern in deafferented animals showed a significant decrease in frequency, which it did not do in intact or semi-intact animals. Seven out of 10 deafferented preparations ceased producing the digging rhythm within 35 min of onset, but none of the semi-intact preparations did so. Mechanosensory hairs cover the ovipositor valves, and are in a position to supply sensory input to the digging pattern generator during the natural behaviour. When nerves carrying sensory axons from these hairs were electrically-stimulated tonically, the motor pattern was restored in deafferented animals. The effects of the stimulation outlasted the stimulation itself for several minutes, and could be repeated several times. We suggest that tonic input is necessary for the maintenance of the digging rhythm, possibly by maintaining levels of some modulatory substance(s) within the CNS.Abbreviations CPG central pattern generator - DUM dorsal unpaired median neuron - EMG electromyogram - LC left ovipositor ventral closer muscle - LCDUR duration of activity of LC - LCFREQ frequency of activity bursts in LC - LCONSET onset of activity in LC relative to LO - LO left ovipositor ventral opener muscle - LODUR duration of activity of LO - LOFREQ frequency of activity bursts of LO - RO right ovipositor ventral opener muscle - RODUR duration of activity in RO - ROFREQ frequency of activityb bursts of RO     

Behavioural evidence for hygro- and mechanoreception by ovipositor sensilla of Dacus tryoni (Diptera: Tephritidae)

ABSTRACT. Gravid female Queensland fruit flies Dacus tryoni (Froggatt) readily oviposit when the ovipositor sensilla are stimulated either by a relatively thick (≥2 mm) surface layer, or by moisture under a relatively thin (<0.5 mm) or thick surface layer. A single layer of Parafilm over dry air elicits almost no oviposition; significantly more oviposition occurs when the underside of the Parafilm is coated with a 2 mm thick layer of petroleum jelly; even more oviposition occurs when the Parafilm is floated on liquid paraffin; greatest oviposition is elicited when moist media (agar gel, water or moist air) are presented under the Parafilm. Hollowed-out domes of apple skin elicit significant oviposition only when sealed basally, to give high internal concentrations of water vapour. The previously identified groove sensilla on the tephritid ovipositor are inferred as being a source of mechanical and chemical information used by the fly in such ovipositional decisions. The ovipositor also has two other types of tactile sensilla. The three types of ovipositor sensilla of tephritids are considered to play roles analogous to those of certain labial receptors of flies with piercing mouthparts.     

Central projections from contact chemoreceptors of the locust ovipositor and adjacent cuticle

Contact chemoreceptors (basiconic sensilla) located on the ovipositor and genital segments of the locust serve to control the chemical features of the substrate before and during oviposition. They occur dispersed and also crowded in fields between mechanosensory exteroceptors sensitive to touch or wind (trichoid and filiform sensilla). The central nervous projections of the four chemosensory and one mechanosensory neurons from single basiconic sensilla were stained selectively, focusing on receptors on the ovipositor valves, which usually contact the substrate during the pre-oviposition probing movements. All axons and neurites from one contact chemoreceptor usually stay close together in most of their projections. Segregation occurs mainly when single axons terminate in one neuromere while the others proceed to a different neuromere or ganglion. For projections from one chemoreceptor, there is evidence neither for functional segregation of mechanosensory from chemosensory afferent terminals nor for specific segregation between different chemosensory afferents. The projections from sensilla of dorsal cuticle tend to project rather uniformly along the midline of the terminal ganglion. Comparative staining of touch- and wind-sensitive hair receptor neurons shows mostly central projections, similar to those of neighbouring contact chemoreceptors. From the typical intersegmental projections of most primary afferents and from the lack of segregation into glomerular structures, we conclude that integration of chemosensory information from the genital segments is distributed in the terminal and the 7th abdominal ganglion.     

Isolation of the abdomen releases oviposition behaviour in females of the cricket, Acheta domesticus

Upon isolation, abdomens of adult female house crickets (Acheta domesticus) produced abdominal and ovipositor movements characteristic of normal oviposition. Oviposition behaviour was thus released even in reproductively mature or immature virgins where under normal conditions it was never observed. Decapitation was not sufficient to release oviposition behaviour but transection of the ventral nerve cord between the thorax and the abdomen of immobilized females evoked the response. These observations indicate that the motor programmes for certain components of the oviposition sequence reside in the abdominal ganglia. Moreover, the prerequisite circuitry for ovipositional posturing of the abdomen and ovipositor appears to be functional prior to sexual maturity and insemination, primed by mating, and subject to inhibition by the thoracic ganglia.     

Sense organs on the ovipositor of Macrocentrus cingulum Brischke (Hymenoptera: Braconidae): their probable role in stinging,oviposition and host selection process

Parasitoid wasps from the insect order Hymenoptera can be deployed successfully as biological control agents for a number of pests, and have previously been introduced for the control of corn pest insect species from the Lepidopteran genus Ostrinia. Organs on the ovipositor of parasitoid wasps have mechanical and tactile senses that coordinate the complex movements of egg laying, and the ovipositor of Hymenopteran insects have evolved associated venom glands as part of their stinging defense. The ovipositor of parasitic wasps has evolved an additional function as a piercing organ that is required for the deposition of eggs within suitable host larvae. The morphology and ultrastructure of sense organs on the ovipositor and sheath of Macrocentrus cingulum Brischke (Hymenoptera: Braconidae) are described using scanning and transmission electron microscopy. Three types of sensilla trichodea were shown to be abundant on the outer sheath of the ovipositor, with types II and III being most distal, and the inner surface of the ovipositor covered with microtrichia, more densely near the apex. Sensilla coeloconica are distributed on both ventral and dorsal valves, while campaniform sensilla and secretory pores are only located on the dorsal valve. The olistheter-like interlocking mechanism, as well as the morphology of the ventral and dorsal valve tips and the ventral valve seal may be important in stinging, oviposition and in the host selection process.     

Functional anatomy of the vagina muscles in the adult western conifer seed bug,Leptoglossus occidentalis (Heteroptera: Coreidae), and its implication for the egg laying behaviour in insects

The anatomy of the female reproductive tract and the nerve-evoked contractions of the vagina muscles and their association with the ovipositor in the western conifer seed bug, Leptoglossus occidentalis (Heidemann) are investigated for the first time. The reproductive tract consists of a set of paired telotrophic ovaries, each containing seven ovarioles, located in the anterior lateral regions of the abdomen. Each ovary is attached to a lateral oviduct which spans most of the abdomen to attach to a relatively short common oviduct that joins the vagina near the rear of the animal. The vagina is associated with a pair of bilaterally symmetrical muscles attached at their posterior ends to lateral extensions of sternite VIII, the valvifer of the Type II ovipositor. From this attachment site, the muscles fan out medially and anteriorly to converge along the dorsal midline of the vagina up to the base of the common oviduct. Vagina muscles respond to a single stimulation of their motor nerves by producing a smooth contraction lasting approximately 1 s. With increasing frequencies of stimulation, the muscle contractions summate to create a tetanic response. The muscles are fatigue resistant being able to maintain the same degree of tension for up to 10 min at 10 Hz stimulation. Visual observation shows that other muscles associated with the valves of the ovipositor behave in a similar fashion to that of the vagina muscles from which the tension recordings were obtained. Fatigue-resistant vagina muscles are discussed in relation to copulation, sperm transport and this insect's ability to deposit a series of eggs directly onto the surface of a conifer needle in a manner by which eight or more blunt-ended eggs are packed end-to-end in a single row.     

Sensillar types of the ovipositor of Dasineura brassicae: structure and relation to oviposition behaviour

ABSTRACT. The distal part of the ovipositor of Dasineura brassicae Winn. (Diptera; Cecidomyiidae) possesses forty to forty-five sensilla of three morphological types. Most are provided with a cuticular bristle, which projects from the surface of the ovipositor; fifteen have a taste/tactile function based on fine structural characteristics; about twenty-five are innervated by a single sensory cell, specialized for mechanoreception. Scolopidial sensory receptors are anchored to the cuticle inside the distal part of the ovipositor, they probably respond to changes in length of the ovipositor. Different sensory systems are involved in the choice of oviposition site; compound eyes and antennae are probably active in the earlier stages, whereas the receptors of the ovipositor appear well suited to govern the last steps in this behaviour.     

An oscillator theory of motor unit recruitment

The phenomenon of systematic recruitment of motor units with increasing demand load is usually explained by the size principle. Though this principle successfully explains the gain-related aspects of muscle force generation, it does not address the need for desynchronization of motor unit activities in order to produce a smooth tension profile at the level of whole muscle, while individual muscle fibers are "twitching." We propose an oscillator model of motor neurons in which a pool of motor neurons fires a bundle of muscle fibers. Although individual muscle fibers have a complicated tension profile, the tension produced by the entire bundle is regulated and follows a command signal accurately. This is shown to be possible because of uncorrelated activity produced by local inhibitory connections among motor neurons. Connections that produce synchronized oscillations result in uncontrolled contractions of the muscle. These results seem to suggest that while synchronized activity indicates pathology and disease, desynchronized activity is the precondition for normal muscle function. Physiological evidence for the proposed theory of motor unit synchronization is presented.     

Passive force generation and titin isoforms in mammalian skeletal muscle.

When relaxed striated muscle cells are stretched, a resting tension is produced which is thought to arise from stretching long, elastic filaments composed of titin (also called connectin). Here, I show that single skinned rabbit soleus muscle fibers produce resting tension that is several-fold lower than that found in rabbit psoas fibers. At sarcomere lengths where the slope of the resting tension-sarcomere length relation is low, electron microscopy of skinned fibers indicates that thick filaments move from the center to the side of the sarcomere during prolonged activation. As sarcomeres are stretched and the resting tension sarcomere length relation becomes steeper, this movement is decreased. The sarcomere length range over which thick filament movement decreases is higher in soleus than in psoas fibers, paralleling the different lengths at which the slope of the resting tension-sarcomere length relations increase. These results indicate that the large differences in resting tension between single psoas and soleus fibers are due to different tensions exerted by the elastic elements linking the end of each thick filament to the nearest Z-disc, i.e., the titin filaments. Quantitative gel electrophoresis of proteins from single muscle fibers excludes the possibility that resting tension is less in soleus than in psoas fibers simply because they have fewer titin filaments. A small difference in the electrophoretic mobility of titin between psoas and soleus fibers suggests the alternate possibility that mammalian muscle cells use at least two titin isoforms with differing elastic properties to produce variations in resting tension.     

Central projections of ovipositor sense organs in the damselfly,Sympecma annulata (Zygoptera,Lestidae)

Central projections of sensilla on different parts of the endophytic ovipositor of the lestid damselfly Sympecma annulata are traced. Sensilla include apical hairs of the stylus (STh), hair rows on the ventral part of the valvula (Vh), and distal campaniform sensilla of upper (ULc) and lower (LLc) ovipositor leaves. Backfilling of afferent fibers, using anterograde cobalt fills, reveals the presence of contralaterally projecting fibers for all organs. The main fiber bundle of the LLc enters the terminal ganglion laterally via the genital nerve, but the fibers from ULc enter via the posterior nerve. Main fiber bundles of both leaves end in a lateral part of the ganglion called the lateral neuromere; they demonstrate that sensory information from the two leaves has the same target area. It is hypothesized that the independent pathways of nerves from upper and lower ovipositor leaves (ULc and LLc) may indicate the phylogenetic origin of these appendages from different abdominal segments—the lower leaf from the 8th and upper from 9th. The convergence of afferent fibers from the sensilla of the different ovipositor parts (median, anterior, and lateral processes) in common ganglionic centers may provide the anatomical basis to account for coordination of the movements of different ovipositor parts during oviposition. © 1994 Wiley-Liss, Inc.     

Different oscillators control the circadian rhythm of eclosion and activity inDrosophila

Summary Anatomical studies on the 6 posterior cirri of the barnacle,Balanus hameri, have revealed the presence of a number of bipolar and multipolar sensory neurons in the coxopodite-basipodite-ramal (CBR) region which appear to function as proprioceptors. The cells are associated with two simple strands which terminate on the surface of the flexor muscles or on the hypodermis.Electrophysiological results suggest that the units show uni-directional responses to movements of the limb segments. No position receptors were identified. The difference in receptor activity to imposed and endogenously generated limb movements suggest that many units normally function as muscle tension receptors.     

Host selection and colonization strategies with evidence for a female-produced oviposition attractant in a longhorn beetle

In longhorn beetles and many other internally feeding insects, oviposition choice by females is critical to the survival of their offspring because their larvae are incapable of moving between hosts. Here we report on the complex host selection and colonization strategies of a longhorn beetle, Glenea cantor (F.) (Coleoptera: Cerambycidae), which is an important pest of kapok trees [Bombax ceiba L.=Gossampinus malabaricus (DC.) Merr.] in southern Asia. It attacks weakened trees, eventually killing them. The typical oviposition behavioral sequence in the laboratory includes the following: oviposition site search and recognition using antennae and palpi, oviposition slit preparation with mandibles, turning body direction 180°, egg deposition with the ovipositor, and oviposition wound covering with a jelly-like material from the ovipositor. Bark moisture content significantly increases from the upper to lower sections in kapok trees. In accordance with this variation female adults select the upper section of trees first for oviposition. As infestation continues and the host becomes more weakened, ovipositing females move further down the tree for oviposition. Consequently, the larvae kill the hosts from the top down. We show that the jelly-like material or eggs or both have an olfactory role in attracting females to oviposit nearby. Our findings are important in terms of increasing our understanding of host selection and colonization mechanisms of internally feeding insects, particularly cerambycids, and the development of environmentally friendly pest management measures.     

Neural control of embryonic acetylcholine receptor and skeletal muscle

The manner by which motor neurons exert control over the distribution and number of acetylcholine receptors, and muscle development was investigated in the superior oblique muscle of white Peking duck embryos. Clusters of receptors in the normally developing muscle first appeared on day 10 of incubation as determined with I125 alpha-bungarotoxin autoradiography. The initial appearance of receptor clusters coincided with the arrival of motor nerve fibers in the muscle. Clusters of receptors also appeared in normal fashion in muscles made aneural by destruction of motor neurons on day 7. But after day 14 these clusters had disappeared and no new clusters were seen thereafter in the aneural muscle. Receptor clusters persisted throughout development in muscle in which neuromuscular transmission was blocked with either curare or botulinum toxin and in muscles denervated on day 10.5, i.e., shortly after the initial nerve-muscle contact but prior to the onset of muscle activity. A progressive increase in the total number of receptors and in the total amount of protein occurred during the course of normal development. However, the specific activity of the receptor protein declined sharply following innervation on day 10. The total number of receptors and the specific activity of the receptor was affected depending on whether the motor neurons were destroyed before or after innervation and following chronic blockade of neuromuscular transmission. The half-life of the receptor protein was similar in normal, aneural, and paralyzed muscles (26, 25, 26 h, respectively). Measurements of total protein indicated that essentially no muscle growth occurred in the complete absence of innervation. Paralyzed muscles continued to develop but at a slower pace.