Visuo-vestibular sensorimotor plasticity in Xenopus and Axolotl larvae

Schneider-Soupiadis, Parthena (2024): Visuo-vestibular sensorimotor plasticity in Xenopus and Axolotl larvae. Dissertation, LMU München: Graduate School of Systemic Neurosciences (GSN)

Abstract

Locomotion causes disrupting consequences for sensory perception, which requires concurrent gaze stabilization to maintain visual acuity. Visuo-vestibular reflexes along with spinal efference copy signalling generate motor commands that enable the eyes to perceive a stable image during body/head movement. In vertebrates, these short-latency motor behaviors work synergistically and are evolutionarily well conserved. However, the underlying neural and circuit components must remain plastic and adapt to accommodate the eco-physiological requirements and locomotor characteristics of each species. This dissertation aimed to explore such adaptations of the oculomotor system ensuring gaze stabilization during self-motion. The following chapters focused on understanding how motor performances may be altered or improved in phylogenetically related species that share many similarities but also clear differences. This exploration got extended to pathological conditions, acutely after a severe loss of vestibular sensory input. For this, I profiled and compared the locomotion pattern of two amphibian species, the salamander Axolotl, and the frog Xenopus laevis. To ensure that potential differences were biologically meaningful I used similarly aged and sized animals of both species, at comparable developmental stages which were validated by comparing external morphological features. While Xenopus move more or less continuously, Axolotls exhibit interspersed, short bouts of locomotion followed by a passive glide. Moreover, Xenopus have longer bouts, while Axolotls display higher velocity bouts. In vitro whole-head recordings of the angular vestibulo-ocular reflex (VOR) in Axolotl were significantly lower in gain compared to Xenopus at identical stimulus conditions. Older staged Axolotls show an increase in gain but did only reach the level of stage 49 Xenopus hinting at a delayed developmental onset of angular gaze compensation. Further experiments on fictive locomotion revealed no compensation through efference copy derived eye motions. In addition, the capacity to stabilize gaze is critically dependent on the morphological parameters of inner ear structures. A comparative investigation of the horizontal canals revealed distinct differences in various parameters between Xenopus and Axolotl. These differences favor the dynamic of endolymph flow and, consequently, the capacity of semicircular canals to detect angular head accelerations in Xenopus. In an additional set of experiments, I investigated the plasticity potential during pathological conditions, after the complete loss of unilateral vestibular input in Xenopus. Such a loss generates severe symptoms related to posture, eye movements, and higher- order perceptual deficits. While compensation of such injuries has been explored already extensively in various species, the novelty of my experiments involved in vitro whole head preparations. Such an approach enables a targeted nerve transection with a direct evaluation of its impact within minutes after the surgery, without the influence of anesthesia. Indeed, a severe impairment of the VOR could be observed after the lesion. However, a delayed further decline of both visual and vestibular reflexes persisted and did not show any signs of compensation. This led to the conclusion that the sensory loss was intensified by secondary neuronal effects that likely involve plasticity mechanisms evoked by the ongoing asymmetric activity in the shared visuo-vestibular circuits.

• Dokumententyp: Dissertationen (Dissertation, LMU München)
• Keywords: vestibulo-ocular reflex (VOR), optokinetic reflex (OKR), semicircular canals, eye movements, locomotion, xenopus, axolotl, unilateral labyrinthectomy, homeostatic plasticity
• Themengebiete: 500 Naturwissenschaften und Mathematik ; 500 Naturwissenschaften und Mathematik > 570 Biowissenschaften, Biologie
• Fakultäten: Graduate School of Systemic Neurosciences (GSN)
• Sprache der Hochschulschrift: Englisch
• Datum der mündlichen Prüfung: 2. Juli 2024
• 1. Bericht­erstatter:in: Zwergal, Andreas