The central morphology of mechanoreceptor afferents in the metathoracic leg of the cockroach, Periplaneta americana (Insecta)

The sensory arborizations of the femoral chordotonal organ (FECO), trochanteral campaniform sensilla (CS) and the trochanteral hairplate (THP) are restricted to the ipsilateral hemiganglion and possess large dendritic fields in the dorsal and ventral neuropiles. The efferent projections of the fast (Df) and the slow (Ds) depressor motoneurons project into the same areas. Three groups of trichoid sensilla located on the coxal and trochanteral cuticular walls have central contralateral projections and in one case intersegmental projections. All sensory projections terminate either just lateral of or in the Ventral Association Centre (VAC). Comparisons with the mechanoreceptors of other insects reveal similar projection patterns for some proprioceptors and non-homologous central configurations for others.     

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     

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     

The Anatomy of the Tarsi of Schistocerca gregaria Forskål

Summary The tarsus of S. gregaria is divided into three units (here called segments) and an arolium set between a pair of claws. The first segment bears three pairs of pulvilli in the fore and middle legs, and one pair and two single pulvilli in the hind legs. Segment two bears a pair of pulvilli, segment three one long pulvillus and the arolium a similar pad on the undersurface. The outer layers of the arolium pad differ from those of the pulvilli in possibly lacking an epicuticle and in having a layer of cuticle which, unlike the corresponding layer in the pulvilli, does not stain with protein stains. The claws and dorsal surfaces bear trichoid sensilla, basiconic sensilla and campaniform sensilla. Smaller basiconic sensilla and canal sensilla occur on the proximal part of the pulvilli, and basiconic sensilla on the arolium undersurface. Internally the cuticle is modified in the arolium and pulvilli so that rods of probably chitin and resilin are formed. This would impart flexibility to the undersurfaces whilst retaining some degree of rigidity which might prevent damage to the small and delicate sense organs on the pulvilli. The tip of the arolium is specialised for adhesion, and there are two large neurones internally which could conceivably monitor attachment or detachment of the tip. There are chordotonal organs in segment three, and several other large neurones throughout the tarsus, some of which are associated with the slings of tissue holding the apodeme in a ventral position. Gland cells occurring in the dorsal epidermis of the adult mature male are also briefly described.     

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.     

Central projections of sensory cells of the midleg of the locust,Schistocerca gregaria

The central projections of trichoid hairs and of some scolopidial organs of the mesothoracic leg of the locust Schistocerca gregaria were studied by using nickel chloride backfilling and single cell recording. Trichoid hair sensilla on different parts of the legs project somatotopically in the ventral part of the ipsilateral neuropile of the mesothoracic ganglion. Generally, distally located receptors have their terminal arborizations in ventro-lateral areas of the neuropile, and proximally located receptors in ventro-medial areas. The axons of the subgenual organ and tarsal chordotonal organs project into the intermediate neuropile.     

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     

Two antagonistic functions of neural groups of the femoral chordotonal organ underlie thanatosis in the cricket Gryllus bimaculatus DeGeer

The cricket Gryllus bimaculatus displayed freezing (thanatosis) after struggling while the femoro-tibial joints of the walking legs were forcibly restrained. Myographic recording indicated that strong contraction of the flexor tibia muscle “leg flexion response” occurred under this restrained condition. During thanatosis, when the femoro-tibial joint was passively displaced and held for several seconds, it maintained its new position (catalepsy). Only discharge of the slow flexor units was mechanically indispensable for maintaining thanatosis and catalepsy. Differing roles of identified neuron subgroups of the femoral chordotonal organ were elucidated using this behavioral substrate. Ablation of the dorsal group neurons in the ventral scoloparium strengthened the leg flexion response and the normal resistance reflex, while ablation of the ventral group weakened both motor outputs. Ablation of the dorsal scoloparium neurons, or other main sensory nerves caused no detectable deficiency in femoro-tibial joint control. These results imply that both modes of flexor muscle activation promoted by the ventral group neurons are normally held under inhibitory control by the dorsal group. It is hypothesized that this antagonistic function causes immobilization of the femoro-tibial joint in a wide range of angles in thanatosis and catalepsy. Accepted: 12 November 1998     

Convergence of load and movement information onto leg motoneurons in insects

The interaction of two feedback loops was investigated: one regulating cuticular stress in the stick insect's leg and the other controlling leg posture. Exclusive stimulation of either of the two relevant sense organs, the load-sensitive trochantero-femoral campaniform sensilla (CS) or the position-/movement-sensitive ventral coxal hairplate (cxHPv), elicits resistance reflex responses in the retractor and the protractor coxae motoneuron pools. Concurrent application of both stimulus modalities reveals that the strength of the postural feedback response is dependent on sign and amplitude of the load feedback response and vice versa. This superposition of the two reflex responses appears to be non-linear. The results indicate that the CS information is underlying a force control function in this six-legged animal. It is hypothesized that the force control of each single leg could help to optimize the force distribution of the six-legged system, even - due to the mechanical coupling - without explicit neuronal pathways. On the level of the single leg control it was studied whether the different information provided by the two feedback transducers converge on the level of retractor coxae motoneurons or whether this information is fully preprocessed at the level of premotor interneurons. It is shown here that the hairplate afferents make direct, excitatory connections with the retractor motoneurons. Studies of the motoneurons' membrane conductances during exclusive CS stimulation reveal that both, excitatory as well as inhibitory synaptic drive is delivered onto the retractor motoneurons. Thus, the motoneuronal membrane is shown to be an important stage for the sensor fusion of the two modalities.     

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.     

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

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

Intersegmental transfer of sensory signals in the stick insect leg muscle control system

Intersegmental coordination during locomotion in legged animals arises from mechanical couplings and the exchange of neuronal information between legs. Here, the information flow from a single leg sense organ of the stick insect Cuniculina impigra onto motoneurons and interneurons of other legs was investigated. The femoral chordotonal organ (fCO) of the right middle leg, which measures posture and movement of the femur-tibia joint, was stimulated, and the responses of the tibial motoneuron pools of the other legs were recorded. In resting animals, fCO signals did not affect motoneuronal activity in neighboring legs. When the locomotor system was activated and antagonistic motoneurons were bursting in alternation, fCO stimuli facilitated transitions from flexor to extensor activity and vice versa in the contralateral leg. Following pharmacological treatment with picrotoxin, a blocker of GABA-ergic inhibition, the tibial motoneurons of all legs showed specific responses to signals from the middle leg fCO. For the contralateral middle leg we show that fCO signals encoding velocity and position of the tibia were processed by those identified local premotor nonspiking interneurons known to contribute to posture and movement control during standing and voluntary leg movements. Interneurons received both excitatory and inhibitory inputs, so that the response of some interneurons supported the motoneuronal output, while others opposed it. Our results demonstrate that sensory information from the fCO specifically affects the motoneuronal activity of other legs and that the layer of premotor nonspiking interneurons is a site of interaction between local proprioceptive sensory signals and proprioceptive signals from other legs.     

The peripheral and central nervous organization of the locust coxo–trochanteral joint

The micromorphology of the locust coxo–trochanteral joint was examined in cobalt-stained material. Peripheral nervous system, musculature, and internal proprioceptors—two strand receptors and a muscle receptor organ—of the metathoracic coxa are compared with those of the pro- and mesothoracic legs. The number and position of trochanter levator and depressor motoneurons as well as the central projections of coxal sense organs are described. Evidence for a femoro–tibial strand receptor was obtained by tracing the path of a particular nerve branch.     

The two groups of sensilla in the ventral coxal hairplate of Carausius morosus have different roles during walking

Abstract. The ventral coxal hairplate (cxHPv) of the stick insect Carausius morosus Br. (Phasmida: Bacteriidae) contains two morphologically distinct groups of sensilla designated as group 1 and 2 (Gl, G2). The function of these sensilla during walking was tested by selectively ablating one or both groups on one middle leg in thirty-four animals. It has previously been shown that ablation of the entire hairplate leads to two kinds of errors: the operated leg swings farther forward and the adjacent caudal leg ends its swing more to the rear relative to the operated leg. Following selective ablation of cxHPv Gl on the middle leg, the first kind of error is more pronounced, indicating that this group contributes more to limiting forward protraction during the swing. Following ablation of cxHPv G2, the second kind of error is more evident, indicating that during stance this group contributes more to the target information influencing the swing end-point of the adjacent caudal leg. These results are interpreted to reflect the phasic and phasic-tonic response characteristics of Gl and G2 hairs, respectively.     

Development of leg chordotonal sensory organs in normal and heat shocked embryos of the cricket Teleogryllus commodus (Walker)

This paper describes the embryonic development of some parts of the sensory peripheral nervous system in the leg anlagen of the cricket Teleogryllus commodus in normal and heat shocked embryos. The first peripheral neurons appear at the 30% stage of embryogenesis. These tibial pioneer neurons grow on a stereotyped path to the central nervous system and form a nerve which is joined by the growth cones of axons that arise later, including those from the femoral chordotonal organ, subgenual organ and tympanal organ. The development of these organs is described with respect to the increase in number of sensory receptor cells and the shape and position of the organs. At the 100% stage of embryogenesis all three organs have completed their development in terms of the number of sense cells and have achieved an adult shape. To study the function of the tibial pioneer neurons during embryogenesis a heat shock was used to prevent their development. Absence of these neurons has no effect on the development of other neurons and organs proximal to them. However, the development of distal neurons and organs guided by them is impaired. The tibial pioneer neurons grow across the segmental boundary between femur and tibia early in development, and the path they form seems to be essential for establishing the correct connections of the distal sense organs with the central nervous system.     

Responses of spiking local interneurones in the locust to proprioceptive signals from the femoral chordotonal organ

Summary The responses of spiking local interneurones of a ventral midline population in the metathoracic ganglion of the locust,Schistocerca gregaria, to controlled movements of a proprioceptor, the femoral chordotonal organ (FCO) in a hindleg, were revealed by intracellular recording. Afferents from the FCO which signal specific features of the movement or angle of the femoro-tibial joint, can make direct excitatory synapses with particular interneurones in this population (Burrows 1987a).Some interneurones in this population are excited only by flexion, some only by extension, but others by both flexion and extension movements of the femoro-tibial joint. Interneurones excited by one direction of movement may be either unaffected, or inhibited by the opposite movement. The balance between excitation and inhibition is determined by the range over which the movement occurs, and can increase the accuracy of a representation of a movement.The response of some interneurones has tonic components, so that the angle of the joint over a certain range is represented in the frequency of their spikes. Different interneurones respond within different ranges of femoro-tibial angles so that information about the position of the joint is fractionated amongst several members of the population. These interneurones respond to repetitive movements, similar to those used by the locust during walking, with bursts of spikes whose number and frequency are determined by the repetition rate and amplitude of the movement. A brief movement of the FCO may induce effects which persist for many seconds and outlast the changed pattern of afferent spikes. The sign of such an effect depends upon the preceding history of stimulation.Other interneurones respond only to movement so that their response is more phasic. The velocities to which they respond fall within the range of those generated by twitches of the flexor and extensor tibiae muscles and the movements of the tibia during locomotion. Some interneurones respond only to a specific range of velocities because they are inhibited by all other movements. Some interneurones respond to repetitive movements with reliable bursts of spikes, whilst in others the frequency of spikes may be raised but may contain no cyclical information. All, however, produce the largest number of spikes during the first cycle of a repetitive movement.Inputs from the FCO may sum either with excitation generated by direct inputs from exteroceptors or with inhibition produced by other local interneurones as a result of afferent signals.These spiking local interneurones are essential elements in the integration of local reflexes initiated by signals from the FCO. For example, one ensures that the levator tarsi motor neurone is reflexly inhibited when the FCO signals an extension movement. Exteroceptive inputs from the ventral tarsus suppress the spikes in this interneurone and would prevent expression of the reflex when the tarsus is in contact with ground.Abbreviation FCO femoral chordotonal organ     

Sensory control of leg movement in the stick insect Carausius morosus

Hind legs with crossed receptor-apodemes of the femoral chordotonal organ when making a step during walking often do not release the ground after reaching the extreme posterior position. After putting a clamp on the trochanter (stimulation of the campaniform sensilla) the leg is no longer protracted during walking. However, during searching-movements the same leg is moved very far forwards. The anatomical situation of the campaniform sensilla on the trochanter and the sensory innervation of the trochanter is described. After removal of the hair-rows and continuously stimulating the hair-plate at the thorax-coxa-joint the extreme anterior and posterior positions of the leg in walking are displaced in the posterior direction. Front and middle legs operated in this way sometimes do not release the ground at the end of retraction. In searching-movements the same leg is moved in a normal way. If only one side of a decerebrated animal goes over a step, then on the other side a compensatory effect is observed. The main source of this compensatory information appears to be the BF1-hair-plates. If the animal has to drag a weight the extreme anterior and posterior positions of the middle and hind legs are displaced in the anterior direction. Crossing the receptor-apodeme of the femoral chordotonal organ, when it causes the leg to remain in the protraction phase, displaces the extreme posterior position of the ipsilateral leg in front of the operated one in the posterior direction. Influences of different sources on the extreme posterior position can superimpose. A model is presented which combines both a central programme and peripheral sensory influence. The word programme used here means that it does not only determine the motor output but also determines the reactions to particular afferences. The fact that the reaction to a stimulus depends on the internal state of the CNS is also represented by the model.Supported by Deutsche Forschungsgemeinschaft     

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     

Central organization of common inhibitory motoneurons in the locust: role of afferent signals from leg mechanoreceptors

Intracellular recordings of mesothoracic common inhibitory neurons (CI₁, CI₂ and CI₃) were made while tactile hairs of the middle legs of locusts (Locusta migratoria) were mechanically stimulated. Generally the three common inhibitory neurons were excited by stimulation of tactile hairs on the ventral and dorsal surface of femur and tibia. The response pattern of all three CI neurons was similar suggesting that they work as a functional unit. Touching hairs on the dorsal surface of tibia and tarsus in some cases led to inhibition of CIs. The connection between sensory cells of tactile hairs and common inhibitory neurons is polysynaptic.To identify interneurons which mediate afferent signals, simultaneous intracellular recordings from CIs and interneurons were made. Different spiking interneurons were identified which made excitatory or inhibitory monosynaptic connections with CIs. Interneurons with inhibitory input to CIs belonged to the ventral midline group of spiking local interneurons. Behavioral and electrophysiological results indicate that reflex movements of the leg are accompanied by activity of CI neurons. Further it appears that CI activity is inhibited when reflex movements of the leg are actively suppressed by the animal.Abbreviations CI common inhibitor - IN interneuron - LY Lucifer Yellow