Evaluation of force feedback in walking using joint torques as “naturalistic” stimuli

Abstract

Control of adaptive walking requires the integration of sensory signals of muscle force and load. We have studied how mechanoreceptors (tibial campaniform sensilla) encode 'naturalistic' stimuli derived from joint torques of stick insects walking on a horizontal substrate. Previous studies showed that forces applied to the legs using the mean torque profiles of a proximal joint were highly effective in eliciting motor activities. However, substantial variations in torque direction and magnitude occurred at the more distal femoro-tibial joint, which can generate braking or propulsive forces and provide lateral stability. To determine how these forces are encoded, we utilized torque waveforms of individual steps that had maximum values in stance in the directions of flexion or extension. Analysis of kinematic data showed that the torques in different directions tended to occur in different ranges of joint angles. Variations within stance were not accompanied by comparable changes in joint angle but often reflected vertical ground reaction forces and leg support of body load. Application of torque waveforms elicited sensory discharges with variations in firing frequency similar to those seen in freely walking insects. All sensilla directionally encoded the dynamics of force increases and showed hysteresis to transient force decreases. Smaller receptors exhibited more tonic firing. Our findings suggest that dynamic sensitivity in force feedback can modulate ongoing muscle activities to stabilize distal joints when large forces are generated at proximal joints. Further, use of 'naturalistic' stimuli can reproduce characteristics seen in freely moving animals that are absent in conventional restrained preparations.

Sensory signals of unloading in insects are tuned to distinguish leg slipping from load variations in gait: experimental and modeling studies

“…1 C , right ). As in our previous studies ( 27 , 28 ), we selected and analyzed recordings in which sensory responses remained mechanically stable through lengthy sequences of stimulus repetitions at comparable force levels. Data on firing rates and forces were calculated using custom Spike 2 scripts.…”

Adaptive load feedback robustly signals force dynamics in robotic model of Carausius morosus stepping

“…For biological experiments, “sensory discharge” is the resulting activity of the sensory neurons measured in action potentials per second. Such data has been collected by extracellular recordings of leg nerves while controlled forces are applied to insect legs (for example, Ridgel et al, 2000 ; Noah et al, 2001 , 2004 ; Keller et al, 2007 ; Zill et al, 2009 , 2021 ; Harris et al, 2022 ). Action potentials are identified in the recordings and then “binned” over time to approximate the discharge in action potentials per second.…”

“…In the same way as insects’ CS discharge ( Ridgel et al, 1999 ; Harris et al, 2022 ), the CS model discharge emphasizes the dynamic changes in force that occur at the beginning and end of stance phase. This is because the model discharge, like the sensilla discharge, is highly sensitive to the rate of change of force ( Zill et al, 2021 ). Detecting the initiation and end of stance phase is critical to the coordination of walking in insects ( Cruse, 1990 ; Duysens et al, 2000 ; Zill et al, 2004 ; Dallmann et al, 2017 ), underlining the importance of CS and their sensory discharge dynamics.…”

“…Insects appear to utilize CS sensory feedback in a number of ways. All leg CS are sensitive to force dynamics and tests using joint torques derived from freely walking animals ( Dallmann et al, 2016 ) indicate that the discharges of the receptors reflect variations in the rate of change of forces rather than simply encoding the force level ( Zill et al, 2021 ). These signals could be used to adjust muscle activities to compensate for force variations to ensure smooth movements in walking.…”

“…Many groups of CS are located on the exoskeleton close to the insertions of leg muscles. In these locations, the strains in the exoskeleton can be calculated as functions of the joint torques, the net rotational forces that occur about the joint (independent of the joint angles) due to muscle contractions and loads ( Zill et al, 2021 ). Recent studies have examined the signals produced by the tibial group of CS to joint torques calculated by inverse dynamics.…”