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     

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     

A strand receptor with a central cell body synapses upon spiking local interneurones in the locust

Summary Movements of the femoro-tibial joint of a locust hind leg are monitored by three classes of proprioceptors; a chordotonal organ (Usherwood et al. 1968), multipolar joint receptors (Coillot and Boistel 1968) and a strand receptor innervated by a single afferent with a central cell body (Bräunig 1985). All three classes are excited by imposed or voluntary extension of the tibia. The strand receptor (fe-tiSR) spikes tonically and at a frequency dependent upon the position of the joint whilst the multipolar joint receptors give overlapping information but for a more restricted range. The afferent from the strand receptor makes an excitatory connection with a spiking local interneurone in the midline group of the metathoracic ganglion. The central latency and consistency with which the EPSP follows each sensory spike suggests that the connection is direct. This interneurone also receives convergent inputs from neurones in the chordotonal organ, but not from multipolar joint receptors. Neither the strand receptor nor the multipolar joint receptors apparently synapse upon leg motor neurones that we have tested, in contrast to receptors in the chordotonal organ.     

A proprioceptor with central cell bodies in the cockroach,Periplaneta americana (Insecta)

Summary A previously undescribed receptor in the coxo-trochantinal region of the metathoracic leg of the cockroach Periplaneta americana was found to have central cell bodies. This cockroach stretch receptor is the second sensory receptor in insects reported to possess somata in the CNS and its remarkable similarity to a locust proprioceptor suggests it to be homologous.     

Glutamatergic transmission between antagonistic motor neurones in the locust

The pharmacology of the direct central connections between the fast extensor and flexor motor neurones of a locust (Schistocerca gregaria) hind leg was studied. A spike in the fast extensor produces an EPSP in the flexor motor neurones. Glutamate depolarized the flexor motor neurones when injected into the neuropil. Quisqualate, but not by kainate or NMDA, also depolarized the flexor motor neurones. The fast extensor was also depolarized by glutamate, and also by kainate, but not by quisqualate, AMPA or NMDA. The glutamate response in the flexor motor neurones and the EPSP evoked by a spike in FETi both had similar reversal potentials. The FETi-evoked EPSP was blocked by bath application of the glutamate antagonist glutamic acid diethyl ester. The responses of extrasynaptic somata receptors to glutamate were compared to the neuropil responses. Glutamate usually hyperpolarized the somata of FETi and the flexor motor neurones. The response of a flexor motor neurone to glutamate was abolished at potentials less negative than -90 mV. The results provide evidence for glutamate transmission at central synapses in the locust, and show that presumed synaptic receptors in the neuropil differ to the extrasynaptic soma response     

Variability of femoral chordotonal organ reflexes in the locust, Locusts miaratoria

Abstract. The femoral chordotonal organ of a locust front, middle or hind leg was stimulated mechanically under open-loop conditions and the forces produced by the muscles moving the tibia were measured. In nearly all cases resistance reflexes were elicited in the inactive animal. However, in rare, but reproducible cases, a positive feedback occurred. In an animal performing active movements the responses were very labile: often no response occurred, sometimes a reaction comparable to the active reaction in stick insects was found, and sometimes resistance reflexes were present.     

Evolutionary adaptation of a reflex system: sensory hysteresis counters muscle ‘catch’ tension

Summary The metathoracic femoral chordotonal organ is a receptor of the locust,Schistocerca, hindleg that encodes the angle of the femoro-tibial joint. However, the discharge of the organ shows considerable hysteresis, in that there is a substantial decline in the level of afferent firing when the tibia is moved and then returned to its initial position. Similar hysteresis is also seen in some joint receptors and interneurons of other invertebrates and vertebrates. When the chordotonal organ is stimulated in freely moving locusts, mimicking sudden changes in joint angle, reflex discharges can be elicited in the tibial extensor muscle that resist apparent joint movement and also show similar hysteresis. This pattern of motoneuron activity is demonstrated to potentially function to eliminate residual, catch muscle tensions that result from increases in motoneuron firing frequency. This adaptation could also serve to produce accurate load compensation.     

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     

The distribution of GABA-like immunoreactivity in the thoracic nervous system of the locust Schistocerca gregaria

Summary An antiserum raised against gamma aminobuyric acid (GABA) was used to stain the thoracic nervous system of the locust. It stained both neuronal somata and processes within the neuropile. Among the stained somata, those of the three pairs of common inhibitory motor neurones could be identified in each of the three thoracic ganglia. In the pro- and mesothoracic ganglia five discrete groups of somata are stained, four ventral and one dorsal. In the metathoracic neuromere, an additional second dorsal group can be identified. In the abdominal neuromeres of the metathoracic ganglion both dorsal and ventral somata are stained but the latter cannot be divided into discrete populations. In each ganglion, dorsal commissures (DC) IV and V are composed of stained neurites, DCVII, the supramedian commissure, the perpendicular tract, and all the longitudinal tracts contain both stained and unstained neurites. DCI, II, III and VI, the T and I tracts are unstained. An abundance of GABA-like immunoreactive processes is found throughout the neuropile except for the anterior ventral association centre where stained processes are sparser. Some of the stained cell groups contain neurones that have been studied physiologically. The function of these neurones is discussed.Beit Memorial Fellow     

The contributions of diverse sense organs to the control of leg movement by a walking insect

Summary During locomotion, stick insectsCarausius morosus, place the tarsus of the rear leg near the tarsus of the ipsilateral middle leg, whatever the position of the latter. This adjustment by the hind leg requires that it receive information on the actual position of the middle leg tarsus. It is shown by ablation experiments that such information is contributed by the following proprioceptors of the middle leg: the ventral and dorsal coxal hairplates, the coxal hair rows, the trochanteral hairplate and the femoral chordotonal organ. Additional information comes from other, as yet unidentified, sense organs. Several alternatives are considered to explain how the signals from the diverse sense organs of the subcoxal joint might be combined in computing the target position for the protracting hind leg. The experimental results support the hypothesis that the signals are added nonlinearly and that a signal deviating from the majority pattern is weighted less.Abbreviations cxHPu ventral coxal hairplate - cxHPd dorsal coxal hairplate - trHP trochanteral hairplate - HR hair row - feCO femoral chordotonal organ - AEP anterior extreme position     

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.     

Interaction between descending input and thoracic reflexes for joint coordination in cockroach: I. Descending influence on thoracic sensory reflexes

Tethered cockroaches turn from unilateral antennal contact using asymmetrical movements of mesothoracic (T2) legs (Mu and Ritzmann in J Comp Physiol A 191:1037–1054, 2005). During the turn, the leg on the inside of the turn (the inside T2 leg) has distinctly different motor patterns from those in straight walking. One possible neural mechanism for the transformation from walking to inside leg turning could be that the descending commands alter a few critical reflexes that start a cascade of physical changes in leg movement or posture, leading to further alterations. This hypothesis has two implications: first, the descending activities must be able to influence thoracic reflexes. Second, one should be able to initiate the turning motor pattern without descending signals by mimicking a point farther down in the reflex cascade. We addressed the first implication in this paper by experiments on chordotonal organ reflexes. The activity of depressor muscle (Ds) and slow extensor tibia muscle (SETi) was excited and inhibited by stretching and relaxing the femoral chordotonal organ. However, the Ds responses were altered after eliminating the descending activity, while the SETi responses remain similar. The inhibition to Ds activity by stretching the coxal chordotonal organ was also altered after eliminating the descending activity.     

Mechanism for range fractionation in chordotonal organs of Locusta migratoria (L) and Valanga sp. (Orthoptera : Acrididae)

The femoral chordotonal organ (FCO) of Locusta migratoria and Valanga sp. (Orthoptera : Acrididae) is a leg stretch receptor containing scolopophorous sensory neurones embedded in a ligament, which emerges distally from the body of the organ and connects to a distal apodeme. The ligament is pulled when the tibia is flexed. Thus the FCO bridges the femur-tibia joint. The ligament is divided into separate strands, each of which is composed of several or more, long attachment cells. These cells link individual scolopidia to the apodeme. An additional unloading strand connects the body of the FCO to a static point on the femoral integument. Because the strands are inserted along the apodeme in a sequential array, and because the unloading strand holds all the tension on the FCO when the ligament is relaxed (tibia extended), a mechanism for gradual, sequential uptake of tension by the ligament strands exists when the ligament is pulled (tibia flexed). This leads to a range fractionation of stretch-sensitive neurone responses during tibial flexion, and of relaxation-sensitive neurone responses during tibial extension. Observations on the ultrastructural distribution of desmosomes suggest that groups of attachment cells may be functionally connected and may collectively transmit force to specific groups of neurones.     

A sensory map based on velocity threshold of sensory neurones from a chordotonal organ in the tailfan of the crayfish

The central projections of sensory neurones innervating a strand chordotonal organ (CO) in the tailfan of the crayfish, Procambarus clarkii (Girard) have been investigated. The CO monitors movement of the exopodite of the tailfan relative to the endopodite. Intracellular recording and staining were used to characterise the response of the sensory neurones to applied stretches of the chordotonal organ and to reveal their morphology. Two gross morphological types of afferents were found: those that terminated in the terminal (6th) abdominal ganglion on the side ipsilateral to the sensory receptor, and those that had branches in the terminal ganglion and an intersegmental axon that ascended rostrally. Afferents responded to position, velocity and direction of imposed CO displacement. Afferents with particular physiological properties had similar morphologies in different crayfish. Irrespective of their directional responses, afferents had central projection areas dependent upon their velocity thresholds. Many afferents responded only during movement of the CO, and those with the lowest velocity thresholds (2°/s) had branches that projected most anteriorly, while those with progressively higher velocity thresholds (up to 200°/s) projected progressively more posteriorly. Afferents that responded to low velocity ramp movements and spiked tonically projected to more posterior areas of the ganglion than those that responded only to movements.Abbreviations A6SCI sixth abdominal sensory commissure I - CO chordotonal organ - DMT dorsal medial tract - G6 sixth abdominal ganglion - LDT lateral dorsal tract - MDT medial dorsal tract - MVT medial ventral tract - R1–4 nerve roots 1–4 - VLT ventral lateral tract - VMT ventral medial tract     

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     

Pre-processing and transfer entropy measures in motor neurons controlling limb movements

Directed information transfer measures are increasingly being employed in modeling neural system behavior due to their model-free approach, applicability to nonlinear and stochastic signals, and the potential to integrate repetitions of an experiment. Intracellular physiological recordings of graded synaptic potentials provide a number of additional challenges compared to spike signals due to non-stationary behaviour generated through extrinsic processes. We therefore propose a method to overcome this difficulty by using a preprocessing step based on Singular Spectrum Analysis (SSA) to remove nonlinear trends and discontinuities. We apply the method to intracellular recordings of synaptic responses of identified motor neurons evoked by stimulation of a proprioceptor that monitors limb position in leg of the desert locust. We then apply normalized delayed transfer entropy measures to neural responses evoked by displacements of the proprioceptor, the femoral chordotonal organ, that contains sensory neurones that monitor movements about the femoral-tibial joint. We then determine the consistency of responses within an individual recording of an identified motor neuron in a single animal, between repetitions of the same experiment in an identified motor neurons in the same animal and in repetitions of the same experiment from the same identified motor neuron in different animals. We found that delayed transfer entropy measures were consistent for a given identified neuron within and between animals and that they predict neural connectivity for the fast extensor tibiae motor neuron.     

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.     

The midline metathoracic ear of the praying mantis,Mantis religiosa

Summary The praying mantis, Mantis religiosa, is unique in possessing a single, tympanal auditory organ located in the ventral midline of its body between the metathoracic coxae. The ear is in a deep groove and consists of two tympana facing each other and backed by large air sacs. Neural transduction takes place in a structure at the anterior end of the groove. This tympanal organ contains 32 chordotonal sensilla organized into three groups, two of which are 180° out of line with the one attaching directly to the tympanum. Innervation is provided by Nerve root 7 from the metathoracic ganglion. Cobalt backfills show that the auditory neuropile is a series of finger-like projections terminating ipsilaterally near the midline, primarily near DC III and SMC. The auditory neuropile thus differs from the pattern common to all other insects previously studied.     

Interneurones participating in the “active reaction” in stick insects

The active reaction upon stimulation of the femoral chordotonal organ in stick insects is known to control velocity and endpoint of flexion movements of the femur-tibia joint (Bässler 1988). This article presents evidence that spiking interneurones in the ventral anterior median part of the adjacent ganglion participate in the generation of the active reaction as well as non-spiking interneurones in the dorsal lateral region do. Three different kinds of experiments lead to this conclusion: