Directional specificity and encoding of muscle forces and loads by stick insect tibial campaniform sensilla,including receptors with round cuticular caps

In many systems, loads are detected as the resistance to muscle contractions. We studied responses to loads and muscle forces in stick insect tibial campaniform sensilla, including a subgroup of receptors (Group 6B) with unusual round cuticular caps in oval-shaped collars. Loads were applied in different directions and muscle contractions were emulated by applying forces to the tibial flexor muscle tendon (apodeme). All sensilla 1) were maximally sensitive to loads applied in the plane of joint movement and 2) encoded muscle forces but did not discharge to unresisted movements. Identification of 6B sensilla by stimulation of cuticular caps demonstrated that receptor responses were correlated with their morphology. Sensilla with small cuticular collars produced small extracellular potentials, had low thresholds and strong tonic sensitivities that saturated at moderate levels. These receptors could effectively signal sustained loads. The largest spikes, derived from sensilla with large cuticular collars, had strong dynamic sensitivities and signaled a wide range of muscle forces and loads. Tibial sensilla are apparently tuned to produce no responses to inertial forces, as occur in the swing phase of walking. This conclusion is supported by tests in which animals 'stepped' on a compliant surface and sensory discharges only occurred in stance.     

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.     

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.     

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.     

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.     

Load sensing and control of posture and locomotion

This article reviews recent findings on how forces are detected by sense organs of insect legs and how this information is integrated in control of posture and walking. These experiments have focused upon campaniform sensilla, receptors that detect forces as strains in the exoskeleton, and include studies of sensory discharges in freely moving animals and intracellular characterization of connectivity of afferent inputs in the central nervous system. These findings provide insights into how campaniform sensilla can contribute to the adjustment of motor outputs to changes in load. In this review we discuss (1) anatomy of the receptors and their activities in freely moving insects, (2) mechanisms by which inputs are incorporated into motor outputs and (3) the integration of sensory signals of diverse modalities. The discharges of some groups of receptors can encode body load when standing. Responses are also correlated with muscle-generated forces during specific times in walking. These activities can enhance motor outputs through reflexes and can affect the timing of motoneuron firing through inputs to pattern generating interneurons. Flexibility in the system is also provided by interactions of afferent inputs at several levels. These mechanisms can contribute to the adaptability of insect locomotion to diverse terrains and environments.     

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.     

Force detection in cockroach walking reconsidered: discharges of proximal tibial campaniform sensilla when body load is altered

We examined the mechanisms underlying force feedback in cockroach walking by recording sensory and motor activities in freely moving animals under varied load conditions. Tibial campaniform sensilla monitor forces in the leg via strains in the exoskeleton. A subgroup (proximal receptors) discharge in the stance phase of walking. This activity has been thought to result from leg loading derived from body mass. We compared sensory activities when animals walked freely in an arena or on an oiled glass plate with their body weight supported. The plate was oriented either horizontally (70-75% of body weight supported) or vertically (with the gravitational vector parallel to the substrate). Proximal sensilla discharged following the onset of stance in all load conditions. In addition, activity was decreased in the middle third of the stance phase when the effect of body weight was reduced. Our results suggest that sensory discharges early in stance result from forces generated by contractions of muscles that press the leg as a lever against the substrate. These forces can unload legs already in stance and assure the smooth transition of support among the limbs. Force feedback later in stance may adjust motor output to changes in leg loading.     

Tuning posture to body load: decreases in load produce discrete sensory signals in the legs of freely standing cockroaches

Decreases in load are important cues in the control of posture and walking. We recorded activities of the tibial campaniform sensilla, receptors that monitor forces as strains in the exoskeleton, in the middle legs of freely moving cockroaches. Small magnets were attached to the thorax and body load was changed by applying currents to a coil below the substrate. Body position was monitored by video recording. The tibial sensilla are organized into proximal and distal subgroups that have different response properties and reflex effects: proximal sensilla excite extensor motoneurons while distal receptors inhibit extensor firing. Sudden load decreases elicited bursts from distal sensilla, while increased load excited proximal receptors. The onset of sensory discharges closely approximated the time of peak velocity of body movement in both load decreases and increases. Firing of distal sensilla rapidly adapted to sustained unloading, while proximal sensilla discharged tonically to load increases. Load decreases of small amplitude or at low rates produced only inhibition of proximal activity while decrements of larger size or rate elicited distal firing. These response properties may provide discrete signals that either modulate excitatory extensor drive during small load variations or inhibit support prior to compensatory stepping or initiation of swing.     

Detecting substrate engagement: responses of tarsal campaniform sensilla in cockroaches

Sensory signals of contact and engagement with the substrate are important in the control and adaptation of posture and locomotion. We characterized responses of campaniform sensilla, receptors that encode forces as cuticular strains, in the tarsi (feet) of cockroaches using neurophysiological techniques and digital imaging. A campaniform sensillum on the fourth tarsal segment was readily identified by its large action potential in nerve recordings. The receptor discharged to contractions of the retractor unguis muscle, which engages the pretarsus (claws and arolium) with the substrate. We mimicked the effects of muscle contractions by applying displacements to the retractor apodeme (tendon). Sensillum firing did not occur to unopposed movements, but followed engagement of the claws with an object. Vector analysis of forces suggested that resisted muscle contractions produce counterforces that axially compress the tarsal segments. Close joint packing of tarsal segments was clearly observed following claw engagement. Physiological experiments showed that the sensillum responded vigorously to axial forces applied directly to the distal tarsus. Discharges of tarsal campaniform sensilla could effectively signal active substrate engagement when the pretarsal claws and arolium are used to grip the substrate in climbing, traversing irregular terrains or walking on inverted surfaces.     

An instrumented shoe—A portable force measuring device

Effective protection from fracture for diseased or partially healed bones can be quantitatively developed only with a knowledge of the external forces applied to the bone. While force studies using force plates have documented the forces for certain activities, a more portable force measuring device is required to determine forces during most daily activities. The authors have developed an instrumented shoe with load cells attached directly to the shoe which measured orthogonal components of foot-to-ground forces and moments. Goniometers simultaneously monitor the position of the lower leg. The signals are transported to a system of loads acting at the lower leg. Typical load curves are presented.     

Tonic and modulatory subsystems of the complex gravity receptor system in crickets, Gryllus bimaculatus

The gravity receptor system of crickets Gryllus bimaculatus is composed of antennal, cercal and leg subsystems. The cercal gravity receptors are the club-shaped sensilla. Each of these subsystems elicits compensatory head movements during passive roll.The extent of compensatory head movements depends on the strength of the gravitational stimulus applied to the leg subsystem. Amputation of 2 legs never causes a decrease in reflex amplitude. Unilateral amputation of 1 to 3 legs always induces a roll movement of the head to the intact body side. Therefore, the leg gravity receptor system exerts a modulatory and tonic effect on the neck muscles.The gravity receptors of 1 cercus or 1 antenna only elicit compensatory head movements. They exert no tonic effect on the neck muscles.The results are discussed with respect to (i) the proposed connectivity of the cercus-neck muscle pathway, (ii) mutual inhibitory interactions between the sensory pathways originating in the leg gravity receptors, and (iii) the influence of non-gravitationally induced excitation on the occurrence of compensatory head movements during passive roll of the crickets.     

Modifications of dynamic and static behavior by small-length perturbations in crayfish stretch receptor organs

To investigate whether static and dynamic sensitivities of slowly and rapidly adapting stretch receptor organs (SAO and RAO, respectively) or crayfish are different when perturbed compared with those in conventional laboratory experiments, receptors were submitted to ramplike length changes of different velocities separated by long-duration, constant lengths of different values. They were perturbed at random by fast, small-amplitude length variations called "jitter." First-order afferent discharges were recorded extracellularly. Quantifications involved the separate estimation of static and dynamic response components. In the SAO, jitter (1) augmented the static sensitivity, (2) decreased the dynamic sensitivity, (3) simplified response profiles by decreasing nonlinearities and increasing transduction fidelity in terms of coding length. In the RAO, jitter (1) changed the behavior from phasic to tonic with length sensitivity, (2) decreased the dynamic sensitivity to values close to those of the unperturbed SAO, (3) increased transduction fidelity for stimulus length and decreased nonlinearities. Perturbation effects suggest that differences between SAO and RAO are more quantitative than qualitative. Moreover, they have general implications and are relevant to other mechanoreceptors at other levels in the CNS.     

Carrying loads with springy poles.

People throughout Asia use springy bamboo poles to carry the loads of everyday life. These poles are a very compliant suspension system that allows the load to move along a nearly horizontal path while the person bounces up and down with each step. Could this be an economical way to carry loads inasmuch as no gravitational work has to be done to lift the load repeatedly? To find out, an experiment was conducted in which four male subjects ran at 3.0 m/s on a motorized treadmill with no load and while carrying a load equal to 19% body wt with compliant poles. Oxygen consumption rate, vertical ground reaction force, and the force exerted by the load on the shoulders were measured. Oxygen consumption rate increased by 22%. The same increase has previously been observed when loads are carried with a backpack. Thus compliant poles are not a particularly economical method of load carriage. However, pole suspension systems offer important advantages: they minimize peak shoulder forces and loading rates. In addition, the peak vertical ground reaction force is only slightly increased above unloaded levels when loads are carried with poles.     

Altered control of submaximal bite force during bruxism in humans

The control of bite force during varying submaximal loads was examined in patients suffering from bruxism compared to healthy humans not showing these symptoms. The subjects raised a bar (preload) with their incisor teeth and held it between their upper and lower incisors using the minimal bite force required to keep the bar in a horizontal position. Further loading was added during the preload phase. A sham load was also used. Depending on the session, the teeth were loaded by the experimenter or the subject and in one session the subject did not see the load (no visual feedback). The bite force was measured continuously using a calibrated force transducer. In all the subjects, the bite force increased with increasing load. Following the addition of the load, the level of the tonic bite force was reached rapidly with no marked overshoot. The patients with bruxism used significantly higher bite forces to hold the submaximal loads compared to the control subjects. In the control subjects, the holding forces for each submaximal load were identical in the men and the women and were independent of subject maximal bite force. Sham loading evoked no marked responses in biting force. Whether the subject or the experimenter added the load or whether the subject had visual feedback or not were not significant factors in determining the level of bite force. The results indicated that the patients with bruxism used excessively large biting forces for each given submaximal load. This study showed no evidence that the inappropriate control of bite force by patients with bruxism was due to an abnormality in the higher cortical circuits that regulates the function of trigeminal motoneurons in the brainstem. This was shown by a lack of abnormality in coordination of voluntary hand movement with biting force, a lack of abnormal anticipation response to a sham load and a lack of any effect of visual feedback. The results were in line with the hypothesis that afferent input from oral (periodontal or masticatory muscle) tissues does not provide an appropriate control of motor command in bruxism.     

Neurophysiology of the vibration sense in locusts and bushcrickets: Response characteristics of single receptor units

The response characteristics of the vibration receptors in the legs of the migratory locust, Locusta migratoria, and the tettigoniid Decticus verrucivorus were investigated electro-physiologically by single cell recordings. The legs were stimulated by sinusoidal vibrations. There are four types of vibration receptor in each leg of Locusta and Decticus, which can be classified physiologically. One type—most probably campaniform sensilla—shows a phase-locked response to vibrations from 30 to 200 Hz, its threshold reflecting the displacement. A second type shows similar responses in the same frequency range, but its reactions depend on the stimulus acceleration. The receptor cells of the subgenual organ are very sensitive to vibration from 30 to at least 5000 Hz, and their responses depend on acceleration. There are two types of subgenual receptors, one of which shows a clear maximum of sensitivity between 200 and 1000 Hz, with a threshold below 0.01 m/sec^?2 acceleration. Subgenual receptors with different thresholds and different characteristic frequencies occur in each leg. The receptors of each leg pair have quite similar mean sensitivities and characteristic frequencies. However, in the front legs of tettigoniids the more sensitive subgenual receptors and an additional receptor type also respond to low-frequency airborne sound up to 10 kHz.     

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.     

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.     

Predicted and observed shapes of human mandibular condyles.

A mathematical model based on linear programming was used to study the directions of the joint forces used to maintain the human jaw in three-dimensional static equilibrium when producing bite forces of 100 N to a maximum of 1000 N down the long axis of a central incisor, first premolar, first molar and third molar. Seven different versions of the model were studied. The two simplest versions minimized the total muscle tension and the total joint load, respectively. Assuming that the joint force direction must be normal to some part of the articular surface of the condyle, neither version produced directions consistent with the observed shapes of human condyles. The other five versions minimized different combinations of muscle tensions and joint loads. Two of these versions produced joint force directions compatible with the shapes of condyles. Both minimized total muscle tension plus the (vertical) joint load on the back of the condyle. The results suggest that joint mechanoreceptors (probably non-directional) as well as muscle receptors contribute to the neuromuscular control of bite forces. Our results are consistent with some recent observations [Marshall and Tatton, Exp. Brain Res. 83, 137-150 (1990)] of the cat knee joint.     

Physiological tremor and control of limb position in 1 and 0 G

Muscle and skeletal mechanoreceptors play an important role for the regulation of muscular tone and the genesis of normal Physiological Tremor (PT). For example if a big limb as the arm or leg is kept against the gravity vector, the la afferent spindle discharges continuously control the load bearing flexor in a negative feedback manner in order to compensate the gravity vector and to the stabilize arm position. This servo-like action, denoted as 'stretch reflex', not only increases static postural stability (tonic stretch reflex) but also counteracts against external disturbances by dynamically increasing the muscle tone. Muscle spindles are very sophisticated sensory organs. They have an own innervation and the endings of the nuclear bag fibres are highly sensitive for small microstretches. EMG and microneurografic studies showed their importance in the mechanism of the 8-12 Hz component for PT. In a 0 G a limb becomes position controlled. In contrast to 1g, where control of limb position is a subordinated function of force compensation in the load bearing muscle, an antagonistic control scheme is necessary in 0 G to compensate the arm against positional drifts. As a consequence there is a shift from load dependent (muscular) to position dependent (skeletal) mechanoreceptors that become involved in the neural control process. As the control process is reflected in the tremor pattern, we investigated arm tremor in a constant limb position in 1 and 0 G.