Microgravity-induced modifications of the vestibuloocular reflex inXenopus laevistadpoles are related to development and the occurrence of tail lordosis

Abstract

SUMMARY During space flights, tadpoles of the clawed toad Xenopus laevisoccasionally develop upward bended tails (tail lordosis). The tail lordosis disappears after re-entry to 1g within a couple of days. The mechanisms responsible for the induction of the tail lordosis are unknown;physical conditions such as weight de-loading or physiological factors such as decreased vestibular activity in microgravity might contribute. Microgravity(μg) also exerts significant effects on the roll-induced vestibuloocular reflex (rVOR). The rVOR was used to clarify whether tail lordosis is caused by physiological factors, by correlating the occurrence ofμ g-induced tail lordosis with the extent of μg-induced rVOR modifications. Post-flight recordings from three space flights (D-2 Spacelab mission,STS-55 in 1993; Shuttle-to-Mir mission SMM-06, STS-84 in 1997; French Soyuz taxi flight Andromède to ISS in 2001) were analyzed in these experiments. At onset of microgravity, tadpoles were at stages 25-28, 33-36 or 45. Parameters tested were rVOR gain (ratio between the angular eye movement and the lateral 30° roll) and rVOR amplitude (maximal angular postural change of the eyes during a 360° lateral roll). A ratio of 22-84% of tadpoles developed lordotic tails, depending on the space flight. The overall observation was that the rVOR of tadpoles with normal tails was either not affected by microgravity, or it was enhanced. In contrast, the rVOR of lordotic animals always revealed a depression. In particular, during post-flight days 1-11, tadpoles with lordotic tails from all three groups (25-28, 33-36 and 45) showed a lower rVOR gain and amplitude than the 1g-controls. The rVOR gain and amplitude of tadpoles from the groups 25-28 and 33-36 that developed normal tails was not affected by microgravity while the rVOR of μg-tadpoles from the stage-45 group with normal tails revealed a significant rVOR augmentation. In conclusion: (1)the vestibular system of tadpoles with lordotic tails is developmentally retarded by microgravity; (2) after a critical status of vestibular maturation obtained during the appearance of first swimming, microgravity activates an adaptation mechanism that causes a sensitization of the vestibular system.

Xenopus development from late gastrulation to feeding tadpole in simulated microgravity

“…The tadpoles, launched at the early tailbud stage (approximately one day old), exhibited caudal lordosis (also noted in a study by Horn, 2006), disproportionately long tails and short bodies, a failure to inflate their lungs, and a reduced, misshapen branchial apparatus (Snetkova et al, 1995). The acceleration and vibration of the launch and the sudden onset of μG may have caused or contributed to these irregularities.…”

“…Both swimming behavior and optomotor response were sometimes altered in the tadpoles raised in μG, but tadpoles would normalize upon return to normal gravity (Souza et al, 1995;Fejtek et al, 1998). Other studies involving exposure to spaceflight μG during development in Xenopus have found alterations in the development of the vestibular apparatus (Souza et al, 1994;Pronych et al, 1996) and vestibuloocular reflex (Sebastian and Horn, 2001;Horn, 2006).…”

The vestibuloocular reflex of tadpoles (Xenopus laevis) after knock-down of the isthmus related transcription factor XTcf-4

“…Immediately before the rVOR recording, we documented tail morphology. Previous studies of the relationship between tail shape and vestibuloocular reflex after spaceflights revealed that the rVOR in tadpoles with abnormal tails differs from those with normal tails in an age-related manner (Horn, 2006;Horn and Gabriel, 2011).…”

“…This curve was used to calculate the rVOR amplitude, which is the maximal peak-to-peak movement of the eyes during a 360deg lateral roll. Previous studies in Xenopus laevis, young fish (Oreochromis mossambicus) and salamander larvae (Pleurodeles waltl) have shown that the rVOR amplitude is a sensitive indicator to describe (1) modifications of the rVOR during development (Horn et al, 1986a;Sebastian and Horn, 1999;Gabriel et al, 2012), (2) the susceptibility to changes within the vestibuloocular system induced by vestibular lesions (Horn et al, 1986b), (3) the extent of vestibular plasticity after such lesions (Rayer and Horn, 1986) and (4) the impact of altered gravitational conditions on vestibular function (Horn 2006;Sebastian et al, 2001;Horn and Gabriel, 2011;Gabriel et al, 2012). The rVOR amplitude was determined by the angular difference between the mean of eye angles recorded for roll angles between 60deg to 120deg and 240deg to 300deg, respectively (cf.…”

“…To test this hypothesis, we selected the roll-induced vestibuloocular reflex (rVOR). Its development and adaptation to surgical lesions and modifications of the gravitational environment have been extensively studied in Xenopus (Horn et al, 1986a;Horn et al, 1986b;Rayer and Horn, 1986;Sebastian et al, 1996;Horn, 2006;Horn and Gabriel, 2011).…”