Response characteristics of single trochanteral campaniform sensilla in the stick insect, Cuniculina impigra

ABSTRACT. The campaniform sensilla on the trochanter of the stick insect, Cuniculina impigra Redtenbacher, were stimulated by slightly bending the leg in the horizontal plane. Single sensory units in the nerve were recorded using glass microelectrodes. These units can be classified into tonic and phasic-tonic receptors. In both cases there were units which increased their discharge frequency during forward movement of the femur, and units which responded to backward movement. No purely phasic receptors were found.     

The central connections and actions during walking of tibial campaniform sensilla in the locust

Strain acting on the exoskeleton of insects is monitored by campaniform sensilla. On the tibia of a mesothoracic leg of the locust (Schistocerca gregaria) there are three groups of campaniform sensilla on the proximo-dorsal surface. This study analyses the responses of the afferents from one group, their connections with central neurones and their actions during walking.The afferents of the campaniform sensilla make direct excitatory connections with flexor tibiae motor neurones. They also make direct connections with particular spiking local interneurones that make direct inhibitory output connections with the slow extensor tibiae motor neurone.During walking extension movements of the tibiae during stance produce longitudinal tensile forces on the dorsal tibia that peak during mid stance before returning to zero prior to swing. This decline in tension can activate the campaniform sensilla. In turn this would lead to an inhibition of the extensor tibiae motor neurone and an excitation of the flexor tibiae motor neurones. This, therefore, aids the transition from stance to swing. During turning movements, the tibia is flexed and the dorsal surface is put under compression. This can also activate some of campaniform sensilla whose effect on the flexor motor neurones will reinforce the flexion of the tibia.     

Positive force feedback in development of substrate grip in the stick insect tarsus

The mechanics of substrate adhesion has recently been intensively studied in insects but less is known about the sensorimotor control of substrate engagement. We characterized the responses and motor effects of tarsal campaniform sensilla in stick insects to understand how sensory signals of force could contribute to substrate grip. The tarsi consist of a chain of segments linked by highly flexible articulations. Morphological studies showed that one to four campaniform sensilla are located on the distal end of each segment. Activities of the receptors were recorded neurographically and sensilla were identified by stimulation and ablation of their cuticular caps. Responses were characterized to bending forces and axial loads, muscle contractions and to forces applied to the retractor apodeme (tendon). The tarsal sensilla effectively encoded both the rate and amplitude of loads and muscle forces, but only when movement was resisted. Mechanical stimulation of the receptors produced activation of motor neurons in the retractor unguis and tibial flexor muscles. These findings indicate that campaniform sensilla can provide information about the effectiveness of the leg muscles in generating substrate adherence. They can also produce positive force feedback that could contribute to the development of substrate grip and stabilization of the tarsal chain.     

Encoding of force increases and decreases by tibial campaniform sensilla in the stick insect, <Emphasis Type="Italic">Carausius morosus</Emphasis>

Detection of force increases and decreases is important in motor control. Experiments were performed to characterize the structure and responses of tibial campaniform sensilla, receptors that encode forces through cuticular strains, in the middle leg of the stick insect (Carausius morosus). The sensilla consist of distinct subgroups. Group 6A sensilla are located 0.3 mm distal to the femoro-tibial joint and have oval shaped cuticular caps. Group 6B receptors are 1 mm distal to the joint and have round caps. All sensilla show directional, phasico-tonic responses to forces applied to the tibia in the plane of joint movement. Group 6B sensilla respond to force increases in the direction of joint extension while Group 6A receptors discharge when those forces decrease. Forces applied in the direction of joint flexion produce the reverse pattern of sensory discharge. All receptors accurately encode the rate of change of force increments and decrements. Contractions of tibial muscles also produce selective, directional sensory discharges. The subgroups differ in their reflex effects: Group 6B receptors excite and Group 6A sensilla inhibit tibial extensor and trochanteral depressor motoneurons. The tibial campaniform sensilla can, therefore, encode force increases or decreases and aid in adapting motor outputs to changes in load.     

Dynamic responses of tibial campaniform sensilla studied by substrate displacement in freely moving cockroaches

Responses of the tibial campaniform sensilla, receptors that encode strains in the exoskeleton, were characterized by recording sensory activities during perturbations in freely standing cockroaches. The substrate upon which the animal stood was displaced horizontally using ramp and hold stimuli at varied rates. The sensilla showed short latency responses that were initiated in the first 30 ms of platform movement. Responses of individual receptors depended upon the direction of displacement and the orientation of their cuticular cap. Proximal receptors, whose caps are perpendicular to the long axis of the tibia, responded to displacements directed from the contralateral side of the body and from the head toward the abdomen. The distal sensilla, oriented parallel to the tibia, discharged at longer latency to displacements in opposite directions. Plots of receptor activity versus displacement direction showed that proximal and distal sensilla are activated in non-overlapping ranges of movement direction. Afferent responses also increased as the platform was displaced more rapidly. These results are consistent with a model in which displacements produce forces that result in bending of the tibia. This information could be utilized to detect the direction and rate of forces that occur during leg slipping or in walking on unstable terrains.     

Interruption of searching movements of partly restrained front legs of stick insects,a model situation for the start of a stance phase?

Stick insects (Cuniculina impigra) possessing only one foreleg with restrained coxa performed searching movements. A force transducer was introduced as an obstacle into the plane of movement of femur or tibia. Depending on where it was introduced and whether it was touched for the first time during an upward or a downward movement, different kinds of behaviour of the leg were released. For these different movements, the forces applied to the obstacle and the electrical activity of the depressor, levator, retractor and protractor muscles are described. In addition the alterations occurring after ablation of several sense organs including the trochanteral campaniform sensilla are mentioned. The described movements were similar to the corresponding behaviours during walking at the end of swing phase and the beginning of stance phase. Therefore there is some probability that results obtained by this experimental paradigm can also be applied to the swing-stance transition.     

Sensing the effect of body load in legs: responses of tibial campaniform sensilla to forces applied to the thorax in freely standing cockroaches

Sense organs in the legs that detect body weight are an important component in the regulation of posture and locomotion. We tested the abilities of tibial campaniform sensilla, receptors that can monitor forces in the cockroach leg, to encode variations in body load in freely standing animals. Small magnets were attached to the thorax and currents were applied to a coil below the substrate. Sensory and motor activities were monitored neurographically. The tibial sensilla could show vigorous discharges to changing forces when animals stood upon their legs and actively supported the body weight. Firing of individual afferents depended upon the orientation of the receptors cuticular cap: proximal sensilla (oriented perpendicular to the leg axis) discharged to force increases while distal receptors (parallel to the leg) fired to decreasing forces. Proximal sensillum discharges were prolonged and could encode the level of load when increases were sustained. Firing of the trochanteral extensor motoneuron was also strongly modulated by changing load. In some postures, sensillum discharges paralleled changes in motor frequency consistent with a known interjoint reflex. These findings demonstrate that tibial campaniform sensilla can monitor the effects of body weight upon the legs and may aid in generating support of body load.     

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     

Effects of force detecting sense organs on muscle synergies are correlated with their response properties

Sense organs that monitor forces in legs can contribute to activation of muscles as synergist groups. Previous studies in cockroaches and stick insects showed that campaniform sensilla, receptors that encode forces via exoskeletal strains, enhance muscle synergies in substrate grip. However synergist activation was mediated by different groups of receptors in cockroaches (trochanteral sensilla) and stick insects (femoral sensilla). The factors underlying the differential effects are unclear as the responses of femoral campaniform sensilla have not previously been characterized. The present study characterized the structure and response properties (via extracellular recording) of the femoral sensilla in both insects. The cockroach trochantero-femoral (TrF) joint is mobile and the joint membrane acts as an elastic antagonist to the reductor muscle. Cockroach femoral campaniform sensilla show weak discharges to forces in the coxo-trochanteral (CTr) joint plane (in which forces are generated by coxal muscles) but instead encode forces directed posteriorly (TrF joint plane). In stick insects, the TrF joint is fused and femoral campaniform sensilla discharge both to forces directed posteriorly and forces in the CTr joint plane. These findings support the idea that receptors that enhance synergies encode forces in the plane of action of leg muscles used in support and propulsion.     

Interommatidial sensilla of the praying mantis: Their central neural projections and role in head-cleaning behavior

The compound eye of the praying mantis is covered with approximately 600 bristles and campaniform sensilla. Their afferents project to the brain, and to the suboesophageal and prothoracic ganglia. Cutting the eye branch of the dorsal tegumentary nerve (DTN), the peripheral nerve innervating the corneal sensilla, makes it impossible to initiate head grooming by tactile stimulation of the eye. This stimulus is a strong releaser of grooming behavior in normal animals. Head grooming can be initiated, after cutting the eye branch of the DTN, by stimulation of the frons (the operation leaves the sensory innervation of this part of the cuticle intact). Frame-by-frame analysis of films of head grooming after cutting the nerve reveals a reduction of the speed at which the forelimb is brushed across the surface of the head and eye. The significance of this finding is discussed in terms of a putative feedback loop from the corneal sensilla to the motor neurons controlling the grooming movements.     

Mechanoreception by cuticular sensilla on the pectines of the scorpion <Emphasis Type="Italic">Pandinus cavimanus</Emphasis>

On the pectines of scorpions, several types of cuticular receptors are located. Of these receptors, only the chemo- and mechanosensory peg sensilla have been studied so far while the response characteristics of the long, straight hair sensilla are unknown. As these sensilla protrude in the walking direction and to the ground, we assume that these receptors are most likely involved in observed reflex behaviours. The sensilla constitute rather robust shafts, comparable to other touch-receptors. Their innervation pattern reveals that 5-6 sensory cells are associated with one sensillum. It was possible to record up to three different spike classes (units) which could be distinguished by size, response characteristics and conduction velocity. Two units were analysed in more detail. The response characteristics showed two phasic units, one large and one small, coding the velocity of a stimulus. One medium-sized unit showed phasic-tonic characteristics, coding also the duration of a stimulus. Taking together the morphological and electrophysiological results, we suggest that these sensilla belong to the group of long hair sensilla distributed all over the scorpion body. Furthermore, their response characteristics and the timing between sensory and motor activity within the pectine nerve enable them to be involved in reflex behaviours.     

Properties of the trochanteral hair plate and its function in the control of walking in the cockroach.

1. The physiological properties of the group of long hair sensilla of the trochanteral hair plate in the cockroach metathoracic leg were studied. The sensilla were divided into type I and type II according to their responses to imposed displacements. 2. Type I hair sensilla responded to dynamic displacements whereas type II hair sensilla responded to both dynamic and static displacements. The hair sensilla are normally excited by phasic flexion movements of the femur near the end of leg protraction. 3. Activity in the trochanteral hair plate afferents had a short latency excitatory effect on the motoneurone producing slow extension movements of the femur and an inhibitory effect on the femur flexor motoneurones. 4. Removal of the trochanteral hair plate in one leg caused overstepping of that leg in a walking animal due to exaggerated flexion of the femur. This change in leg movement can be explained by the removal of the inhibitory influence from the hair plate afferents to the femur flexor motoneurones. 5. We conclude that one function of the trochanteral hair plate is to limit femur flexion during a step cycle.     

The fine structure of sense organs in the ovipositor of the parasitic wasp, Orgilus lepidus Muesebeck

Three types of sensilla were observed in the ovipositor, including a multicellular sensillum presumed to respond to both chemical and mechanical stimuli, plus two types of campaniform sensilla. Four or five bipolar chemosensory cells innervate each multicellular sensillum, witln the dendrites terminating at an 800 ,Å dia. pore in the cuticular wall. The dendrite of an associated mechanosensory neuron is inserted upon a slender shaft of cuticle which extends inward from the wall of the ovipositor. This mechanosensory neuron may he activated by stretching when the ovipositor is bent. The dendrite of each campaniform sensillum ends in a cavity in the wall of the ovipositor, and are probably activated by stresses and vibrations as the wasp probes for a host. Sensilla of each type are present in the medial and lateral stylets of the ovipositor. Earlier behavioral studies indicated that the parasite probably uses these sense organs to locate hosts and distinguish healthy from already parasitized hosts.     

Proprioceptors involved in stinging response of the honeybee, Apis mellifera

Two types of mechanosensitive proprioceptor organ are present on the stinging apparatus of the honeybee: campaniform sensilla and mechanosensory hairplates. The campaniform sensilla are located on the surface of the tapering sting-shaft, which comprises an unpaired stylet and paired lancets. Each sensillum on the lancet differs from that on the stylet in terms of their topography and external morphology. The sensory afferents of the campaniform sensilla display slow-adapted firing responses to deformation of the cuticle that would be caused by the action of inserting the sting into a substrate, and their afferent signals induce and/or prolong the stinging response. By contrast, the mechanosensory hairplates are located at basal cuticular plates and on the posterior surface of the lancet valves. Two fields of hairplates on the second ramus at the ventral edge of the groove and on the antero-lateral edge of the oblong plate respond synchronously to protraction of the lancet. During the stinging response, these hairplates are likely to detect any sliding movement of the lancet and its position relative to the stylet. Afferent signals produced by them are likely to provide important information to the neuronal circuit for the generation and modulation of the stinging motor pattern.     

Proprioceptor organs in Cicadella viridis (L.) (Homoptera : Cicadellidae)

The external proprioceptor organs of Cicadella viridis (L.) (Homoptera: Cicadellidae) are identified and localized. They are composed of hair and campaniform sensilla grouped together and located in or near the joint areas of various parts of the body or in cuticular areas, which come into contact with moving parts. The hair sensilla, 8–75 μm long, are arranged in hair plates or in hair rows; they detect relative movement between parts of the body. Proprioceptor organs of this kind, localized in proximity to joint areas, were found on the legs and on the abdomen. Proprioceptor organs composed of hair sensilla located far from the articular areas were found on the 3rd pair of legs, the thorax, the hind wings, and the abdomen. The campaniform sensilla, which are arranged in fields and groups, in cuticular areas subject to deformations, are of 2 types: with raised caps (type I) and with flat caps (type II). Organs with campaniform sensilla were found on the legs, thorax and wings.     

Nonspiking pathways antagonize the resistance reflex in the thoraco-coxal joint of stick insects

In the stick insect (Carausius morosus) imposed forward and backward movements of the coxa of the middle leg induce resistance reflexes in the retractor or protractor coxae muscles, depending on the direction of movement. The hairs of the ventral coxal hairplate (cxHPv) function as the primary transducer of the retractor part of the underlying feedback loop: bending of the hairs of the cxHPv during an imposed forward movement of the coxa leads to a reflex activation of the retractor motoneurones, whereas releasing of the hairs causes an inhibition of these motoneurones. Local nonspiking interneurones were investigated, which transmit information from the cxHPv onto the retractor motoneurones: 1) they are depolarized during bending of the hair sensilla of the cxHPv and 2) they decrease the activities of retractor motoneurones. In addition, four of the interneurones drive a protractor motoneurone, when they are depolarized. As bending stimuli at the cxHPv (mimicking an imposed forward movement of the leg) induce reflex activation of the retractor motoneurones and reflex inhibition of the protractor motoneurones, the physiology of the recorded interneurones appears to antagonize the resistance reflex in the thoraco-coxal joint. The results indicate that these nonspiking interneurones take part in the shaping of the reflex response and that furthermore these interneurones are involved in the organization of the motor output to the two antagonistic sets of motoneurones. The possible role of these interneurones might be the adjustment of the gain and of the time constant in the thoraco-coxal feedback loop.     

Axonal degeneration within the tympanal nerve of Schistocerca gregaria

This study describes time course and ultrastructural changes during axonal degeneration of different neurones within the tympanal nerve of the locust Schistocerca gregaria. The tympanal nerve innervates the tergit and pleurit of the first abdominal segment and contains the axons of both sensory and motor neurones. The majority of axons (approx. 97%) belong to several types of sensory neurones: mechano- and chemosensitive hair sensilla, multipolar neurones, campaniform sensilla and sensory cells of a scolopidial organ, the auditory organ. Axons of campaniform sensilla, of auditory sensory cells and of motor neurones are wrapped by glial cell processes. In contrast, the very small and numerous axons (diameter <1 microm) of multipolar neurones and hair sensilla are not separated individually by glia sheets. Distal parts of sensory and motor axons show different reactions to axotomy: 1 week after separation from their somata, distal parts of motor axons are invaded by glial cell processes. This results in fascicles of small axon bundles. In contrast, distal parts of most sensory axons degenerate rapidly after being lesioned. The time to onset of degeneration depends on distance from the lesion site and on the type of sensory neurone. In axons of auditory sensory neurones, ultrastructural signs of degeneration can be found as soon as 2 days after lesion. After complete lysis of distal parts of axons, glial cell processes invade the space formerly occupied by sensory axons. The rapid degeneration of distal auditory axon parts allows it to be excluded that they provide a structure that leads regenerating axons to their targets. Proximal parts of severed axons do not degenerate.     

The walking-(and searching-) pattern generator of stick insects,a modular system composed of reflex chains and endogenous oscillators

Stick insects (Cuniculina impigra) possessing only one front leg with restrained coxa performed searching movements or walked on a treadband. The movements are described. Ablation, surgical manipulation or experimental stimulation of different sense organs (femoral chordotonal organ, campaniform sensilla on trochanter and femur basis, proprioceptors at the coxatrochanter joint) were performed, and the resulting changes in motor output were recorded. These experiments demonstrate that the walking- and searching-pattern generators cannot be separated, at least not for the movements investigated. This walking- and searching-pattern generator consists of central modules, each of which produces irregular alternation of the activity of motor neurones of antagonistic muscles of a single joint, and of reflex loops. At least some of these reflex loops are only present in the active animal. They are responsible either for the control of a single joint or for the coordination of the movements of separate joints. The performance of these reflexes does not only depend on the state of activity of the animal; some of them additionally seem to depend on the context signalled by other sense organs.     

Encoding of forces by cockroach tibial campaniform sensilla: implications in dynamic control of posture and locomotion

Forces exerted by a leg in support and propulsion can vary considerably when animals stand upon or traverse irregular terrains. We characterized the responses of the cockroach tibial campaniform sensilla, mechanoreceptors which encode force via strains produced in the exoskeleton, by applying forces to the leg at controlled magnitudes and rates. We also examined how sensory responses are altered in the presence of different levels of static load. All receptors exhibit phasico-tonic discharges that reflect the level and rate of force application. Our studies show that: (1) tonic discharges of sensilla can signal the level of force, but accurate encoding of static loads may be affected by substantial receptor adaptation and hysteresis; (2) the absolute tonic sensitivities of receptors decrease when incremental forces are applied at different initial load levels; (3) phasic discharges of sensilla accurately encode the rate of force application; and (4) sensitivities to changing rates of force are strictly preserved in the presence of static loads. These findings imply that discharges of the sensilla are particularly tuned to the rate of change of force at all levels of leg loading. This information could be utilized to adapt posture and walking to varying terrains and unexpected perturbations. Accepted: 8 January 2000