Data Sheet 4_Influence of semicircular canal morphology on the VOR and swimming activity in larval amphibians: a comparative study in Xenopus and axolotl.pdf

Gaze stabilization and locomotion rely often on an accurate sensory detection of head movements by the vestibular system. A functional relationship between vestibular sensitivity, locomotor skills and semicircular canal morphology has been suspected in vertebrates as an adaptation to eco-physiological and species-specific needs, but has only partially and indirectly documented. However, evaluating the vestibulo-ocular reflexive activity and the locomotor efficiency simultaneously with the rotational sensor geometry remains absent from the literature. From such a perspective, this study attempted to provide a simultaneous quantification of the vestibulo-ocular response, the swimming efficiency and the canal morphology in the salamander axolotl and the frog Xenopus laevis, two amphibian species with comparable lifestyle and identical locomotor and vestibular systems at larval stages. Animals were studied at an equivalent developmental period: the late pre-metamorphic stage where the hindlimbs start to differentiate. Larval axolotl demonstrated an angular vestibulo-ocular reflex (aVOR) with a gain ~83% lower than Xenopus. Like in Xenopus at earlier stages, the aVOR gain increased in axolotl indicating a later functional onset. The morphological comparison of the semicircular canals of both species revealed that the horizontal canal in axolotl was thinner, less curved and less coplanar to the horizontal plane compared to Xenopus. Additionally, the ampulla of Xenopus was rounder and less elongated than in axolotl. All these parameters are critical for endolymph flow and consequently for the capacity of semicircular canals to perceive head motion. Interestingly, axolotl demonstrated a reduced swimming activity, more episodic than Xenopus, resulting in less frequent exposure to important head accelerations. Altogether, our results provide correlative evidences for a clear functional link between semicircular canal morphology, vestibular sensitivity, influencing aVOR performance, but also locomotor capacity in two comparable species, representative of anuran and salamander amphibians. This study, even preliminary, should open the pathway for further and more complete demonstrations of this functional relationship, that seems to be commonly shared during the evolution.

凝视稳定与运动通常依赖前庭系统（vestibular system）对头部运动的精准感知。此前，脊椎动物的前庭敏感性、运动能力与半规管（semicircular canal）形态之间存在功能关联的假说，被认为是对生态生理需求及物种特异性需求的适应，但相关证据仅为部分间接佐证。然而，目前尚无文献能够同时评估前庭眼反射活动、运动效率与半规管作为旋转传感器的几何结构之间的关系。基于此视角，本研究尝试对美西钝口螈（axolotl）与非洲爪蟾（Xenopus laevis）这两种幼体阶段生活方式相似、运动与前庭系统高度相似的两栖动物，同时量化其前庭眼反射反应、游泳效率及半规管形态。实验选取了二者发育阶段一致的个体：即后肢开始分化的晚期前变态期。幼体美西钝口螈的角前庭眼反射（angular vestibulo-ocular reflex, aVOR）增益较非洲爪蟾低约83%。与非洲爪蟾幼体早期阶段类似，美西钝口螈的aVOR增益随发育提升，提示其功能激活时间较晚。对二者半规管的形态学对比显示，相较于非洲爪蟾，美西钝口螈的水平半规管更纤细、曲率更低，且与水平面共面性更差。此外，非洲爪蟾的壶腹（ampulla）相较美西钝口螈更圆润、长轴更短。上述所有参数均对内淋巴流动（endolymph flow）至关重要，进而影响半规管感知头部运动的能力。值得注意的是，美西钝口螈的游泳活动更少，且运动模式较非洲爪蟾更具间歇性，因此暴露于显著头部加速度的频率更低。综合来看，本研究结果为半规管形态、前庭敏感性与前庭眼反射性能及运动能力之间的明确功能关联提供了相关性证据，研究对象分别代表了有尾目（salamander）与无尾目（anuran）两栖动物。尽管本研究尚属初步，但它为进一步全面验证这一在演化中普遍存在的功能关联开辟了道路。