skip to main content
Explore Scholarly Publications and Datasets in the NSF-PAR

Title: Investigating the role of low level reinforcement reflex loops in insect locomotion
Abstract Insects are highly capable walkers, but many questions remain regarding how the insect nervous system controls locomotion. One particular question is how information is communicated between the ‘lower level’ ventral nerve cord (VNC) and the ‘higher level’ head ganglia to facilitate control. In this work, we seek to explore this question by investigating how systems traditionally described as ‘positive feedback’ may initiate and maintain stepping in the VNC with limited information exchanged between lower and higher level centers. We focus on the ‘reflex reversal’ of the stick insect femur-tibia joint between a resistance reflex (RR) and an active reaction in response to joint flexion, as well as the activation of populations of descending dorsal median unpaired (desDUM) neurons from limb strain as our primary reflex loops. We present the development of a neuromechanical model of the stick insect ( Carausius morosus ) femur-tibia (FTi) and coxa-trochanter joint control networks ‘in-the-loop’ with a physical robotic limb. The control network generates motor commands for the robotic limb, whose motion and forces generate sensory feedback for the network. We based our network architecture on the anatomy of the non-spiking interneuron joint control network that controls the FTi joint, extrapolated network connectivity based on known muscle responses, more » and previously developed mechanisms to produce ‘sideways stepping’. Previous studies hypothesized that RR is enacted by selective inhibition of sensory afferents from the femoral chordotonal organ, but no study has tested this hypothesis with a model of an intact limb. We found that inhibiting the network’s flexion position and velocity afferents generated a reflex reversal in the robot limb’s FTi joint. We also explored the intact network’s ability to sustain steady locomotion on our test limb. Our results suggested that the reflex reversal and limb strain reinforcement mechanisms are both necessary but individually insufficient to produce and maintain rhythmic stepping in the limb, which can be initiated or halted by brief, transient descending signals. Removing portions of this feedback loop or creating a large enough disruption can halt stepping independent of the higher-level centers. We conclude by discussing why the nervous system might control motor output in this manner, as well as how to apply these findings to generalized nervous system understanding and improved robotic control. « less
Authors:
; ;
Award ID(s):
2015317
Publication Date:
NSF-PAR ID:
10335092
Journal Name:
Bioinspiration & Biomimetics
Volume:
16
Issue:
6
Page Range or eLocation-ID:
065008
ISSN:
1748-3182
Sponsoring Org:
National Science Foundation
More Like this
  1. ; ; ; ; ( , Scientific Reports)
    Abstract

    Existing models of human walking use low-level reflexes or neural oscillators to generate movement. While appropriate to generate the stable, rhythmic movement patterns of steady-state walking, these models lack the ability to change their movement patterns or spontaneously generate new movements in the specific, goal-directed way characteristic of voluntary movements. Here we present a neuromuscular model of human locomotion that bridges this gap and combines the ability to execute goal directed movements with the generation of stable, rhythmic movement patterns that are required for robust locomotion. The model represents goals for voluntary movements of the swing leg on the task level of swing leg joint kinematics. Smooth movements plans towards the goal configuration are generated on the task level and transformed into descending motor commands that execute the planned movements, using internal models. The movement goals and plans are updated in real time based on sensory feedback and task constraints. On the spinal level, the descending commands during the swing phase are integrated with a generic stretch reflex for each muscle. Stance leg control solely relies on dedicated spinal reflex pathways. Spinal reflexes stimulate Hill-type muscles that actuate a biomechanical model with eight internal joints and six free-body degreesmore »of freedom. The model is able to generate voluntary, goal-directed reaching movements with the swing leg and combine multiple movements in a rhythmic sequence. During walking, the swing leg is moved in a goal-directed manner to a target that is updated in real-time based on sensory feedback to maintain upright balance, while the stance leg is stabilized by low-level reflexes and a behavioral organization switching between swing and stance control for each leg. With this combination of reflex-based stance leg and voluntary, goal-directed control of the swing leg, the model controller generates rhythmic, stable walking patterns in which the swing leg movement can be flexibly updated in real-time to step over or around obstacles.

    « less
  2. ; ; ; ( , Journal of Neurophysiology)
    Limb dominance is evident in many daily activities, leading to the prominent idea that each hemisphere of the brain specializes in controlling different aspects of movement. Past studies suggest that the dominant arm is primarily controlled via an internal model of limb dynamics that enables the nervous system to produce efficient movements. In contrast, the nondominant arm may be primarily controlled via impedance mechanisms that rely on the strong modulation of sensory feedback from individual joints to control limb posture. We tested whether such differences are evident in behavioral responses and stretch reflexes following sudden displacement of the arm during posture control. Experiment 1 applied specific combinations of elbow-shoulder torque perturbations (the same for all participants). Peak joint displacements, return times, end point accuracy, and the directional tuning and amplitude of stretch reflexes in nearly all muscles were not statistically different between the two arms. Experiment 2 induced specific combinations of joint motion (the same for all participants). Again, peak joint displacements, return times, end point accuracy, and the directional tuning and amplitude of stretch reflexes in nearly all muscles did not differ statistically when countering the imposed loads with each arm. Moderate to strong correlations were found between stretchmore »reflexes and behavioral responses to the perturbations with the two arms across both experiments. Collectively, the results do not support the idea that the dominant arm specializes in exploiting internal models and the nondominant arm in impedance control by increasing reflex gains to counter sudden loads imposed on the arms during posture control. NEW & NOTEWORTHY A prominent hypothesis is that the nervous system controls the dominant arm through predictive internal models and the nondominant arm through impedance mechanisms. We tested whether stretch reflexes of muscles in the two arms also display such specialization during posture control. Nearly all behavioral responses and stretch reflexes did not differ statistically but were strongly correlated between the arms. The results indicate individual signatures of feedback control that are common for the two arms.« less
  3. ( , Journal of neurophysiology)
    Capers, Miriam (Ed.)
    Supraspinal signals play a significant role in compensatory responses to postural perturbations after spinal cord injury (SCI). SCI disrupts descending motor control signals as well as ascending somatosensory information to and from below the lesion. In intact animals, While cortical signals are not necessary for basic postural tasks, but neurons in the motor cortex have been shown to respond to periodic postural perturbations in intact animals. However, the role of the cortex in postural control after spinal cord injury in response to unexpected postural perturbations has not been studied. To better understand how spinal lesions impact cortical encoding of information about unexpected postural perturbations, the activity of single neurons in the rat hindlimb sensorimotor cortex (HLSMC) were recorded during unexpected tilts before and after a complete midthoracic spinal transection. In a subset of animals, limb ground reaction forces were collected as well. Results show that responses in the HLSMC were modulated with changes in tilt severity (i.e. tilt velocity). As initial velocity of the tilt increased, more information was conveyed by the HLSMC neurons about the perturbation due to increases in both the number of recruited neurons and the magnitude of their response. After SCI hindlimb ground reaction forces weremore »both attenuated and delayed, and the neural responses were delayed and less likely to respond to slower tilts. This resulted in a moderate decrease inan attenuation of the information conveyed by cortical neurons about the tilts, requiring more cells to convey the same amount of information as before the transection. Given that reorganization of the hindlimb sensorimotor cortex in response to therapy after complete mid-thoracic SCI is necessary for behavioral recovery, this sustained encoding of information after SCI could be a substrate for the reorganization that uses sensory information from above the lesion to control trunk muscles that permit weight-supported stepping and postural control.« less
  4. ; ; ; ; ( , Journal of Neurophysiology)
    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 exhibitedmore »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.« less
  5. ( , Frontiers in Ecology and Evolution)
    The size and shape of articular cartilage in the limbs of extant vertebrates are highly variable, yet they are critical for understanding joint and limb function in an evolutionary context. For example, inferences about unpreserved articular cartilage in early tetrapods have implications for how limb length, joint range of motion, and muscle leverage changed over the tetrapod water-land transition. Extant salamanders, which are often used as functional models for early limbed vertebrates, have much thicker articular cartilage than most vertebrate groups, but the exact proportion of cartilage and how it varies across salamander species is unknown. I aimed to quantify this variation in a sample of 13 salamanders representing a broad range of sizes, modes of life, and genera. Using contrast-enhanced micro-CT, cartilage dimensions and bone length were measured non-destructively in the humerus, radius, ulna, femur, tibia, and fibula of each specimen. Cartilage correction factors were calculated as the combined thickness of the proximal and distal cartilages divided by the length of the bony shaft. Articular cartilage added about 30% to the length of the long bones on average. Cartilage was significantly thicker in aquatic salamanders (42 ± 14% in the humerus and 35 ± 8 in the femur) thanmore »in terrestrial salamanders (21 ± 7% in both humerus and femur). There was no consistent relationship between relative cartilage thickness and body size or phylogenetic relatedness. In addition to contributing to limb length, cartilage caps increased the width and breadth of the epiphyses by amounts that varied widely across taxa. To predict the effect of salamander-like cartilage correction factors on muscle leverage, a simplified model of the hindlimb of the Devonian stem tetrapod Acanthostega was built. In this model, the lever arms of muscles that cross the hip at an oblique angle to the femur was increased by up to six centimeters. Future reconstructions of osteological range of motion and muscle leverage in stem tetrapods and stem amphibians can be made more rigorous by explicitly considering the possible effects of unpreserved cartilage and justifying assumptions based on available data from extant taxa, including aquatic and terrestrial salamanders.« less
  • Citation Formats
  • MLA
  • APA
  • Chicago
  • BibTeX
  • Save / Share this Record
  • Send to Email