Effects of aging on behavior and leg kinematics during locomotion in two species of cockroach.

Aging is often associated with locomotor deficits. Behavior in aged Blaberus discoidalis cockroaches was analyzed during horizontal walking, climbing, righting and inclined walking. Adult animals showed a decrease in spontaneous locomotion with increasing age. Tarsal abnormalities, termed 'tarsus catch', were often present in aged individuals. In 'tarsus catch', the prothoracic leg catches on the mesothoracic leg during the swing phase. This deficit causes alterations of the gait, but animals are able to regain a tripod gait after the perturbation. The tibio-tarsal joint angle in individuals with 'tarsus catch' was significantly less than in intact animals. Structural defects were consistently associated with 'tarsus catch'. The tracheal tubes in the tarsus and around the tibio-tarsal joint were often discolored and the tarsal pads were hardened in aged cockroaches. All aged individuals were able to climb. However, prior to climbing, some animals with 'tarsus catch' failed to show postural changes that are normally seen in young animals. Aged individuals can right as rapidly as 1-week-old adults. However, animals with 'tarsus catch' take longer to right than aged intact individuals. Old cockroaches have difficulty climbing an incline of 45 degrees, and leg slipping is extensive. Slipping may be caused by tarsal degeneration, but animals that are unsuccessful in inclined walking often show uncoordinated gaits during the attempt. Escape behavior was examined in aged American cockroaches (Periplaneta americana). They do not show normal escape. However, after decapitation, escape movements return, suggesting that degeneration in head ganglia may actually interfere with escape. These findings provide evidence for age-related changes both in the periphery and in the central nervous system of cockroaches and stress the importance of multi-level approaches to the study of locomotion.

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.

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.