Dataset Information

Fast tuning of posture control by visual feedback underlies gaze stabilization in walking Drosophila.

ABSTRACT: Locomotion requires a balance between mechanical stability and movement flexibility to achieve behavioral goals despite noisy neuromuscular systems, but rarely is it considered how this balance is orchestrated. We combined virtual reality tools with quantitative analysis of behavior to examine how Drosophila uses self-generated visual information (reafferent visual feedback) to control gaze during exploratory walking. We found that flies execute distinct motor programs coordinated across the body to maximize gaze stability. However, the presence of inherent variability in leg placement relative to the body jeopardizes fine control of gaze due to posture-stabilizing adjustments that lead to unintended changes in course direction. Surprisingly, whereas visual feedback is dispensable for head-body coordination, we found that self-generated visual signals tune postural reflexes to rapidly prevent turns rather than to promote compensatory rotations, a long-standing idea for visually guided course control. Together, these findings support a model in which visual feedback orchestrates the interplay between posture and gaze stability in a manner that is both goal dependent and motor-context specific.

SUBMITTER: Cruz TL

PROVIDER: S-EPMC8556163 | biostudies-literature | 2021 Oct

REPOSITORIES: biostudies-literature

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Fast tuning of posture control by visual feedback underlies gaze stabilization in walking Drosophila.

Cruz Tomás L TL Pérez Sebastián Malagón SM Chiappe M Eugenia ME

Current biology : CB 20210908 20

Locomotion requires a balance between mechanical stability and movement flexibility to achieve behavioral goals despite noisy neuromuscular systems, but rarely is it considered how this balance is orchestrated. We combined virtual reality tools with quantitative analysis of behavior to examine how Drosophila uses self-generated visual information (reafferent visual feedback) to control gaze during exploratory walking. We found that flies execute distinct motor programs coordinated across the bod ...[more]

PMID: 34499851

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Project description:Gait rehabilitation following incomplete spinal cord injury (iSCI) often aims to enhance speed and stability. Concurrently increasing both may be difficult though as certain stabilization strategies will be compromised at faster speeds. To evaluate the interaction between speed and lateral stability, we examined individuals with (n = 12) and without (n = 12) iSCI as they performed straight walking and lateral maneuvers at Preferred and Fast treadmill speeds. To better detect the effects of speed on stability, we challenged lateral stability with a movement amplification force field. The Amplification field, created by a cable-driven robot, applied lateral forces to the pelvis that were proportional to the real-time lateral center of mass (COM) velocity. While we expected individuals to maintain stability during straight walking at the Fast speed in normal conditions, we hypothesized that both groups would be less stable in the Amplification field at the Fast speed compared to the Preferred. However, we found no effects of speed or the interaction between speed and field on straight-walking stability [Lyapunov exponent or lateral margin of stability (MOS)]. Across all trials at the Fast speed compared to the Preferred, there was greater step width variability (p = 0.031) and a stronger correlation between lateral COM state at midstance and the subsequent lateral foot placement. These observations suggest that increased stepping variability at faster speeds may be beneficial for COM control. We hypothesized that during lateral maneuvers in the Amplification field, MOS on the Initiation and Termination steps would be smaller at the Fast speed than at the Preferred. We found no effect of speed on the Initiation step MOS within either field (p > 0.350) or group (p > 0.200). The Termination step MOS decreased at the Fast speed within the group without iSCI (p < 0.001), indicating a trade-off between lateral stability and forward walking speed. Unexpectedly, participants took more steps and time to complete maneuvers at the Fast treadmill speed in the Amplification field. This strategy prioritizing stability over speed was especially evident in the group with iSCI. Overall, individuals with iSCI were able to maintain lateral stability when walking fast in balance-challenging conditions but may have employed more cautious maneuver strategies.

Project description:PurposePost-concussion syndrome (PCS) is commonly associated with dizziness and visual motion sensitivity. This case-control study set out to explore altered motion processing in PCS by measuring gaze stabilization as a reflection of the capacity of the brain to integrate motion, and it aimed to uncover mechanisms of injury where invasive subcortical recordings are not feasible.MethodsA total of 554 eye movements were analyzed in 10 PCS patients and nine healthy controls across 171 trials. Optokinetic and vestibulo-ocular reflexes were recorded using a head-mounted eye tracker while participants were exposed to visual, vestibular, and visuo-vestibular motion stimulations in the roll plane. Torsional and vergence eye movements were analyzed in terms of slow-phase velocities, gain, nystagmus frequency, and sensory-specific contributions toward gaze stabilization.ResultsParticipants expressed eye-movement responses consistent with expected gaze stabilization; slow phases were fastest for visuo-vestibular trials and slowest for visual stimulations (P < 0.001) and increased with stimulus acceleration (P < 0.001). Concussed patients demonstrated increased gain from visual input to gaze stabilization (P = 0.005), faster slow phases (P = 0.013), earlier nystagmus beats (P = 0.003), and higher relative visual influence over the gaze-stabilizing response (P = 0.001), presenting robust effect sizes despite the limited population size.ConclusionsThe enhanced neural responsiveness to visual motion in PCS, combined with semi-intact visuo-vestibular integration, presented a subcortical hierarchy for altered gaze stabilization. Drawing on comparable animal trials, findings suggest that concussed patients may suffer from diffuse injuries to inhibiting pathways for optokinetic information, likely early in the visuo-vestibular hierarchy of sensorimotor integration. These findings offer context for common but elusive symptoms, presenting a neurological explanation for motion sensitivity and visual vertigo in PCS.

Dataset Information

Fast tuning of posture control by visual feedback underlies gaze stabilization in walking Drosophila.

Publications

Fast tuning of posture control by visual feedback underlies gaze stabilization in walking Drosophila.

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