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 receptor's 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.

Walking on a 'peg leg': extensor muscle activities and sensory feedback after distal leg denervation in cockroaches.

Previous studies in insects demonstrated that leg coordination changes following complete ablation of distal limb segments. However, normal coordination was restored when small 'peg leg' prostheses were attached to leg stumps to permit substrate contact. We have adapted this paradigm to preserve appropriate leg mass and inertia by severing all nerves and muscle tendons in the femur of the cockroach hind leg and converting the animal's own limb into a peg leg. Recordings of muscle activities and leg movements before and after denervation showed that: (1) the 'peg leg' is actively used in walking and regular bursts occur in motoneurons to leg extensor muscles; (2) driving of motoneuron activity is sufficient to produce 'fictive' bursting in a muscle whose tendon (apodeme) is cut in the ablation; and (3) similar motoneuron activities are found in walking on an oiled glass surface, when the effects of body weight and mechanical coupling are minimized. When distal segments were completely severed in these preparations, leg use and muscle bursting were disrupted but could be restored if the stumps were pressed against the substrate. These results support the hypothesis that feedback from receptors in proximal leg segments indicating forces allows for active leg use in walking.

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.

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.

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.

Active signaling of leg loading and unloading in the cockroach.

The ability to detect changes in load is important for effective use of a leg in posture and locomotion. While a number of limb receptors have been shown to encode increases in load, few afferents have been demonstrated to signal leg unloading, which occurs cyclically during walking and is indicative of slipping or perturbations. We applied mechanical forces to the cockroach leg at controlled rates and recorded activities of the tibial group of campaniform sensilla, mechanoreceptors that encode forces through the strains they produce in the exoskeleton. Discrete responses were elicited from the group to decreasing as well as increasing levels of leg loading. Discharges of individual afferents depended on the direction of force application, and unit responses were correlated morphologically with the orientation of the receptor's cuticular cap. No units responded bidirectionally. Although discharges to decreasing levels of load were phasic, we found that these bursts could effectively encode the rate of force decreases. These discharges may be important in indicating leg unloading in the step cycle during walking and could rapidly signal force decreases during perturbations or loss of ground support.

Load signalling by cockroach trochanteral campaniform sensilla.

A major problem in sensory motor integration is to delineate how forces acting upon a leg are encoded and regulated in the control of posture and locomotion. We have studied responses of the trochanteral campaniform sensilla, the largest array of force detecting mechanoreceptors in the cockroach leg. Afferents from two groups of sensilla (Groups 3 and 4) encode forces applied to the leg in the plane of joint movement of the coxo-trochanteral joint. The receptors within Group 3 exhibit fixed patterns of recruitment that could differentially indicate when force levels are adequate to provide support and propulsion during walking.

Effects of load inversion in cockroach walking.

To examine how walking patterns are adapted to changes in load, we recorded leg movements and muscle activities when cockroaches (Periplaneta americana) walked upright and on an inverted surface. Animals were videotaped to measure the hindleg femoro-tibial joint angle while myograms were taken from the tibial extensor and flexor muscles. The joint is rapidly flexed during swing and extended in stance in upright and inverted walking. When inverted, however, swing is shorter in duration and the joint traverses a range of angles further in extension. In slow upright walking, slow flexor motoneurons fire during swing and the slow extensor in stance, although a period of co-contraction occurs early in stance. In inverted walking, patterns of muscle activities are altered. Fast flexor motoneurons fire both in the swing phase and early in stance to support the body by pulling the animal toward the substrate. Extensor firing occurs late in stance to propel the animal forward. These findings are discussed within the context of a model in which stance is divided into an early support and subsequent propulsion phase. We also discuss how these changes in use of the hindleg may represent adaptations to the reversal of the effects of gravity.

Characteristics of dynamic postural reactions in the locust hindleg.

The use of the locust (Schistocerca americana) hindleg in postural control was examined in animals that stood on a repeatedly swayed vertical substrate. Myograms were recorded from leg muscles and the angle of the femoro-tibial joint was monitored photographically. Two discrete strategies were observed; in compensatory reactions the hindleg was held in place, while in "flexion" reactions, the leg was moved, most often to complete flexion of the femoro-tibial joint. Tightly coupled, rhythmic bursting occurred in the flexor and levator muscles of the leg during compensatory reactions. Bursting was initiated repeatedly when the substrate was being pulled away from the animal. Bursting was correlated with subsequent decreases in the rate of change of the femoro-tibial joint angle. Compensatory and "flexion" reactions occurred preferentially in different ranges of joint angles: most often, compensatory reactions occurred in the mid-range, while "flexion" reactions were elicited in the extremes of joint angle. These differences may be due to the mechanical advantages of the tibial muscles and the leg may be moved to full flexion because of a locking mechanism of the flexor muscle tendon. These reactions are compared with known reflexes of hindleg proprioceptors and contrasted with similar responses of vertebrates.

Responses of locusts in a paradigm which tests postural load compensatory reactions.

The abilities of locusts to generate postural load compensatory reactions were tested by placing them in a chamber that was mounted on a swivel joint and repetitively swayed (an adaptation of the paradigm of Nashner). Tests were performed when animals stood upon a screen on the wall of the cage and sinusoidal displacements were imposed that repeatedly forced the animal away from and toward the side of the chamber upon which it was standing. Myographic activities of muscles of the middle legs and the angle of the chamber relative to the horizontal plane were recorded during these tests. Locusts were readily able to maintain postures during these tests. Myographic recordings of activities of muscles of the mesothoracic legs showed repetitive bursting in the trochanteral levator, tibial flexor and tarsal levator muscles that was coupled to the cycles of movement of the chamber. Similar bursts were not regularly recorded in antagonist muscles. Comparison of the phase of onset of bursting among different muscles demonstrated that the levator and flexor muscles are activated nearly synchronously during the phase of movement when the surface upon which the animal was standing was being moved away from it. Measurements of the forces developed by all the legs during similar reactions in semi-restrained preparations showed that these bursts can regularly generate force levels in excess of 3 times the animal's weight. We conclude that the patterns of muscle activity seen during tests in which animals were swayed could effectively function in postural load compensation. These patterns of activity are compared with similar responses of vertebrates.

Functions of a proprioceptive sense organ in freely moving insects: characteristics of reflexes elicited by stimulation of the locust metathoracic femoral chordotonal organ.

(1) The metathoracic femoral chordotonal organ is an identified joint angle receptor of the locust hindleg. In order to assess and quantify the functions of this sense organ in the control of posture, mechanical stimuli were applied to the main ligament of the receptor in freely standing locusts. These stimuli produced an afferent discharge that mimicked a sudden small (10-15 degree) change in the angle of the femoro-tibial joint of the hindleg. The reflex effects that resulted from afferent stimulation were monitored myographically in the tibial extensor and flexor muscles. The angle of the femoro-tibial joint at the onset of sensory stimulation was also recorded by still photography. (2) As previously reported, stimulation of the chordotonal organ in freely standing animals produced resistance reflexes in tibial muscles that opposed the apparent joint movement. However, we also found that, at certain joint angles, a different mode of reflex response was elicited in which motoneurons to the tibial flexor muscle fired in response to apparent movements in any direction. (3) In this study, characteristics of resistance reflexes in the tibial extensor muscle were analyzed quantitatively, as that muscle is innervated by only one slow excitatory motoneuron. The gain of the resistance reflex (ratio of the firing frequency during afferent stimulation versus the rate of activity prior to the stimulus) was quite high in all preparations, and represent a greater than two-fold increase in motoneuron frequency (mean 2.11 +/- 0.54 S.D.). The reflex gain was also highest at the lowest initial rates of motoneuron activity (circa 5 Hz) and declined for higher firing frequencies (maximum 35 Hz).(ABSTRACT TRUNCATED AT 250 WORDS)

Evolutionary adaptation of a reflex system: sensory hysteresis counters muscle 'catch' tension.

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.

Selective mechanical stimulation of an identified proprioceptor in freely moving locusts: role of resistance reflexes in active posture.

Direct mechanical stimulation of an identified proprioceptive sense organ, the femoral chordotonal organ of the locust hindleg, has been applied in freely moving animals to evaluate its function in maintenance of posture. A piezo-electric crystal mounted on the leg produced displacements of the main ligament of the organ mimicking 10-15 degree changes in joint angle. These stimuli produced consistent responses that (1) occurred as resistance reflexes to oppose the apparent joint movement and (2) demonstrated strong, tonic coupling of motoneuron activity to afferent input. These experiments have, therefore, directly demonstrated that the chordotonal organ functions in posture to aid in load compensation and to set the level of tonic motoneuron activity.

A model of pattern generation of cockroach walking reconsidered.

Cockroaches that have been decapitated or that have cut thoracic connectives can show rhythmic bursting in motoneurons to intrinsic leg muscles. These preparations have been studied as models for walking and to evaluate the functions of leg proprioceptors. The present study demonstrates that headless cockroaches walk extremely poorly and slowly with considerable discoordination of motoneuronal activity, these preparations show rhythmic motoneuron bursting that is similar to righting responses (attempts to turn upright) of intact animals when placed on their backs, and bursting is inhibited when a headless animal is turned or turns itself upright. Thus, rhythmic motoneuron activity of these preparations is most probably attempted righting rather than walking. It is concluded that the headless cockroach is useful for understanding the motor mechanisms underlying righting and walking but is not of value in assessing the functions of proprioceptive feedback.

Single unit sensory activity in free walking crabs: force sensitive mechanoreceptors of the dactyl.

Activities of individual, force-sensitive mechanoreceptors (funnel canal organs) of the terminal segment (dactyl) of the crab leg have been recorded in freely moving animals. During the stance phase of walking receptors discharge in regular bursts that are closely correlated with activity of the opener muscle of the propodite when the leg is used on the trailing side in lateral locomotion. Individual funnel canal organs also show sustained discharges to imposed cuticular strains and strains resulting from resisted muscle contractions. These receptors thus can monitor both internal and external forces that are applied to the leg in locomotion.

Plasticity and proprioception in insects. I. Responses and cellular properties of individual receptors of the locust metathoracic femoral chordotonal organ.

The metathoracic femoral chordotonal organ is a joint angle receptor of the locust hindleg. It consists of 45-55 bipolar sensory neurones located distally in the femur and mechanically coupled to the tibia. Responses of receptors of the organ were examined by extracellular and intracellular recording. The organ as a whole encodes the angle of the femorotibial joint but shows substantial hysteresis. Tonic activity is greatest at the extremes of joint position. The organ possesses no direct linkage to tibial muscle fibres and shows no response to resisted muscle contractions in most ranges of joint angle. However, responses to extensor muscle contractions are obtained when the tibia is held in full flexion due to specializations of the femoro-tibial joint. These responses could be of importance in signalling preparedness for a jump. Intracellular soma recordings of activity in individual receptors indicate that the organ contains two types of receptors: phasic units that respond to joint movement and tonic units that encode joint position and also show some response to movement. All units are directionally sensitive and respond only in limited ranges of joint angle. Some phasic units increase firing frequency with increasing rate of movement and thus encode joint velocity. Other phasic units fire only single action potentials and can encode only the occurrence and direction of joint movement. All tonic units increase activity in the extremes of joint position and show substantial hysteresis upon return to more median positions. Direct soma depolarization produces different responses in different types of units: phasic receptors show only transient discharges to current injection; tonic receptors exhibit sustained increases in activity that are followed by periods of inhibition of background firing upon cessation of current injection. Receptors of the chordotonal organ are separable into two major groups, based upon their response characteristics, soma location and dendritic orientation: a dorsal group of receptors contains tonic units that respond in ranges of joint flexion (joint angle 0-80 degrees) and phasic units that respond to flexion movements; a ventral group of sensilla contains tonic units active in ranges of joint extension (joint angle 80-170 degrees) and phasic receptors that respond to extension movements. The response properties of these receptors are discussed with reference to the potential functions of the chordotonal organ in the locust's behavioural repertoire.

Plasticity and proprioception in insects. II. Modes of reflex action of the locust metathoracic femoral chordotonal organ.

Reflex responses of tibial motoneurones were examined during mechanical stimulation of the femoral chordotonal organ, a joint angle receptor of the locust hindleg. Step displacements of the main ligament of the organ, mimicking 10-15 degree changes in joint angle, produced different patterns of discharge in motoneurones (1) when the leg was resting against a support and (2) when the support was removed to induce active searching movements. Tibial motoneurones showed resistance reflex responses to oppose the apparent joint movement when the leg rested against a support. Resistance reflexes consisted of constant, short latency excitatory responses followed by discharges that varied in intensity (gain) and degree of tonic coupling. These variations were not due to simple summation with other inputs to motoneurones. Responses changed during periods of active searching movements. Tibial flexor motoneurones fired phasically in response to apparent joint movement in any direction. Tibial extensor motoneurones were generally inhibited by chordotonal inputs. These reflex changes are not simple reflex 'reversals', but represent more complex changes in reflex mode. Potential functions of each of these reflex modes and the need for plasticity in reflexes of the chordotonal organ are discussed.

Leg position learning by an insect: II. Motor strategies underlying learned leg extension.

The patterns of myographic activity in the flexor and extensor tibiae muscles of the locust which accompany learned tibial extension were examined. Three distinct motor strategies were identified: (1) repeated flexion-extension movements, each of which resulted in a momentary excursion beyond the required, pre-set joint angle (demand angle) and in sum met the criterion for learning; (2) changes in basic muscle tonus, which resulted in maintained shifts in tibial position without discernible myographic activity; (3) tonic activity in the single slow excitatory motoneuron of the extensor tibiae ( SETi ) which produced maintained tibial extension. These strategies were selectively employed depending on the particular range of joint angle required. These strategies were compared and their effectiveness evaluated using a variety of behavioral criteria. Neuronal mechanisms which might underlie each of these strategies are discussed.

Suppression of reflex postural tonus: a role of peripheral inhibition in insects.

Postural reflexes act through a single excitatory motoneuron of the several that innervate a flexor muscle of the cockroach leg. A peripheral inhibitory neuron whose axon accompanies this excitatory motoneuron is able to suppress muscle tensions developed from postural reflexes without affecting centrally generated muscle tensions. The inhibitory neuron could thus serve to rapidly suppress postural tensions at the initiation of escape.

A somatotopic organization of groups of afferents in insect peripheral nerves.

Sensory axon projections in the main leg nerves of two orthopteran insects, the cockroach Periplaneta americana and the grasshopper Melanoplus bivittatus, were studied by observing patterns of axonal degeneration after ablation of different leg segments. The patterns of degeneration seen in transverse sections of the leg nerves, close to their entrance to the central nervous system (thoracic ganglion) show that sensory axons occur in constant positions in the leg nerves. When distal leg segments are removed, a discrete area of degeneration is found in the leg nerve along its posterior edge. More proximal ablations produce larger areas of degeneration that progressively extend into the anterior half of the nerve. A comparison of the patterns of degeneration produced by different leg ablations shows a posterior to anterior laminar arrangement of groups of sensory axons that corresponds to a distal to proximal map of the leg. This mapping has been confirmed by localized ablations of small groups of leg sensory receptors.