Static Vestibulo-ocular Reflex Research Articles

Altered gravity affects ventral root activity during fictive swimming and the static vestibuloocular reflex in young tadpoles (Xenopus laevis).

During early periods of life, modifications of the gravitational environment affect the development of sensory, neuronal and motor systems. The vestibular system exerts significant effects on motor networks that control eye and body posture as well as swimming. The objective of the present study was to study whether altered gravity (AG) affects vestibuloocular and spinal motor systems in a correlated manner. During the French Soyuz taxi flight Andromède to the International Space Station ISS (launch: October 21, 2001; landing: October 31, 2001) Xenopus laevis embryos were exposed for 10 days to microgravity (microg). In addition, a similar experiment with 3g-hypergravity (3g) was performed in the laboratory. At onset of AG, embryos had reached developmental stages 24 to 27. After exposure to AG, each tadpole was tested for its roll-induced vestibuloocular reflex (rVOR) and 3 hours later it was tested for the neuronal activity recorded from the ventral roots (VR) during fictive swimming. During the post-AG recording periods tadpoles had reached developmental stages 45 to 47. It was observed that microgravity affected VR activity during fictive swimming and rVOR. In particular, VR activity changes included a significant decrease of the rostrocaudal delay and a significant increase of episode duration. The rVOR-amplitude was transiently depressed. Hypergravity was less effective on the locomotor pattern; occurring effects on fictive swimming were the opposite of microg effects. As after microgravity, the rVOR was depressed after 3g-exposure. All modifications of the rVOR and VR-activity recovered to normal levels within 4 to 7 days after termination of AG. Significant correlations between the rVOR amplitude and VR activity of respective tadpoles during the recording period have been observed in both tadpoles with or without AG experience. The data are consistent with the assumptions that during this period of life which is characterized by a progressive development of vestibuloocular and vestibulospinal projections (i) microgravity retards the development of VR activity while hypergravity weakly accelerates it; (ii) that microgravity retards the rVOR development while hypergravity caused a sensitization, and that (iii) AG-induced changes of VR activity during fictive swimming have a vestibular origin.

"Critical periods" in vestibular development or adaptation of gravity sensory systems to altered gravitational conditions?

1. A feature of sensory, neuronal and motor systems is the existence of a critical period during their development. Modification of environmental conditions during this specific period of life affects development in a long-term manner, or even irreversibly. Deprivation is the prefered approach to study the existence and duration of critical periods. For gravity sensory systems, space flights offer the only opportunity for deprivation conditions. 2. Studies in a fish (Oreochromis mossambicus) and an amphibian (Xenopus laevis) revealed a significant sensitivity of their roll-induced static vestibuloocular reflex (rVOR) to a 9- to 10-day gravity deprivation (microgravity) during a spaceflight. In some instances, the rVOR was augmented after the flight as demonstrated in young Oreochromis which were launched when their rVOR had not been developed, and in Xenopus tadpoles launched after their rVOR had developed. Fish which could perform the rVOR at launch were insensitive to microgravity exposure. A similar insensitivity to microgravity was observed in Xenopus tadpoles with normal body shape which had not yet developed their rVOR at launch. Some tadpoles, however, developed an upward bended tail during their space flight; their rVOR was significantly depressed after termination of microgravity independent of the age at onset of the flight. Hypergravity depressed the rVOR for all so far tested developmental stages in both Oreochromis and Xenopus. 3. Both adaptive processes during exposure to altered gravity as well as the existence of a critical period in vestibular development might be responsible for the modulation of the rVOR recorded after exposure to altered gravity. Deprivation studies have to be extended to older developmental stages to test the possibility of a critical period; however, this approach is limited due to the low number of space flights.

Adaptation of the macular vestibuloocular reflex to altered gravitational conditions in a fish ( Oreochromis mossambicus)

Young fish ( Oreochromis mossambicus) were exposed to microgravity (μg) for 9 to 10 days, or to hypergravity (hg) for 9 days. For several weeks after termination of μg and hg, the roll-induced static vestibuloocular reflex (rVOR) was recorded. In stage 11 12 -fish, the rVOR amplitude (angle between the maximal up and down movement of an eye during a complete 360° lateral roll) of μg-animals increased significantly by 25% compared to 1g-controls during the first post-flight week but decreased to the control level during the second post-flight week. Microgravity had no effect in stage 14 16 fish on the rVOR amplitude. After 3g-exposure, the rVOR amplitude was significantly reduced for both groups compared to their 1g-controls. Readaptation to 1g-condition was completed during the second post-3g week. We postulate a critical period during which the development of the macular vestibuloocular reflex depends on gravitational input, and which is limited by the first appearence of the rVOR. At this period of early development, exposure to microgravity sensitizes the vestibular system while hypergravity desensitizes it.

Altered gravitational forces affect the development of the static vestibuloocular reflex in fish (Oreochromis mossambicus).

Young fish (Oreochromis mossambicus) were exposed to microgravity (micro g) for 9 to 10 days during space missions STS-55 and STS-84, or to hypergravity (hg) for 9 days. Young animals (stages 11-12), which had not yet developed the roll-induced static vestibuloocular reflex (rVOR) at micro g- and hg-onset, and older ones (stages 14-16), which had already developed the rVOR, were used. For several weeks afterwards, the rVOR was recorded after termination of mug and hg. Here are the main results: (1) In the stage 11-12 fish, the rVOR gain (response angle/roll angle) measured for roll angles 15 degrees, 30 degrees, and 45 degrees was not affected by microgravity if animals were rolled from the horizontal to the inclined posture, but was increased significantly if animals were rolled in the opposite manner. The rVOR amplitude (maximal eye movement during a complete 360 degrees roll) of micro g animals increased significantly by 25% compared to 1g controls during the first postflight week, but decreased to the control level during the second postflight week. Microgravity had no effect in stage 14-16 fish on either rVOR gain or amplitude. (2) After 3g exposure, both rVOR gain and amplitude were significantly reduced for both stage 11-12 and stage 15 fish. One g readaptation was completed during the second post-3g week. Hypergravity at 2 or 2.5 g had no effect. (3) Hypergravity at all three levels tested (2g, 2.5g, and 3g) accelerated the morphological development as assessed by external morphological markers. Exposure to micro g- or 3g-periods during an early developmental period modifies the physiological properties of the neuronal network underlying the static rVOR; in susceptible developmental stages, these modifications include sensitization by microgravity and desensitization by hypergravity.

An age-dependent sensitivity of the roll-induced vestibuloocular reflex to hypergravity exposure of several days in an amphibian ( Xenopus laevis)

In tadpoles of the Southern Clawed Toad ( Xenopus laevis), the effects of an exposure to hypergravity of several days duration on the development of the roll-induced static vestibuloocular reflex (rVOR) were investigated. Special attention was given to the onset of the 9 or 12 days lasting 3G-period during early life. First recordings of the rVOR characteristics for complete 360 ° rolls of the tadpoles were performed 24 hrs after the end of the 3G-period. The rVOR peak-to-peak amplitudes as well as the VOR-gain for a roll angle of 15 ° from 3G-and 1G-samples recorded at the 2nd and 3rd day after 3G-termination agreed for the youngest group, but were reduced by approx. 30% in the older tadpoles. Long-term observations lasting up to 8 weeks after termination of the 3G-period, demonstrated (i) an early retardation of the development, and (ii) a developmental acceleration in all groups so that after 2 weeks in the stage 6/9- and 33/36-samples and after 8 weeks in the stage 45-tadpoles, the rVOR-amplitude as well as the rVOR-gain for a 15 ° roll were at the same level in both the 3G- and the 1G-samples. The results support the existence of a sensitive period for the rVOR development, and additionally demonstrate the importance of the period of the first appearance of the rVOR for the development of adaptive properties of the underlying neuronal network. They also demonstrate the dominant efficiency of genetic programs in the functional development of the vestibular system. Methodological approaches are discussed which will be useful in the further description of the critical period. They include studies on the neuronogenesis and synaptic maturation within the vestibular pathways as well as on the fundamentals of buoyancy control during swimming. A modular but closed mini-system for experimental use is described which allows survival periods lasting many weeks and multiple types of treatments of developing aquatic animals in orbit, controlled automatically.

Clinical testing of the statolith-ocular reflex.

Quantification of eye torsion induced by stimulation of the statolith organ has recently become available (in the clinic) thanks to the development of video nystagmography. A major step forward has been the development of real-time measurement of eye torsion which enables interactive testing of the statolith-ocular reflex. The function of the statolith organs can be evaluated by the study of the impact of statolith stimulation upon the canal-mediated dynamic vestibulo-ocular reflex (VOR) or by measurement of the static VOR. The latter is more appropriate because instruction or alertness seems not to affect the reflex substantially. Four ways of inducing the static reflex are discussed and related experiments are described. In normal subjects, the gain of eye torsion upon lateroflexion (up to 45 degrees) and whole-body roll (up to 90 degrees) ranges from 0.13 to 0.22; eye torsion is 10.3 degrees maximal. Eccentric rotation inducing a maximal centrifugal force of 1 g results in a gain of eye torsion ranging from 0.15 to 0.23 with a maximal eye torsion of 7.8 degrees in normals. Sinusoidal sideward translation at accelerations of about 0.5 g at 0.3 Hz, which can be considered as specific dynamic statolith stimulation, induces a small but substantial eye torsion of maximally 4.1 degrees and with an eye torsion gain ranging from 0.10 to 0.15. Lateroflexion and body flexion do not require sophisticated stimulation equipment and therefore are attractive for implementation in the out-patient department. In patients, impairment of the statolith-ocular reflex is frequently found both in patients with normal as well as in those with defective dynamic VORs (caloric asymmetries). A qualitative concept is presented to describe the deflection pattern of the cilia upon lateroflexion, eccentric rotation and sidewards translational acceleration. According to this theoretical concept, a reduced static eye torsion might point to both a saccular and/or an utricular lesion. An asymmetry of ocular torsion is only expected upon eccentric rotation or sidewards translation in case of a unilateral saccular lesion.

A hypergravity related sensitive period during the development of the roll induced vestibuloocular reflex in an amphibian (Xenopus laevis)

In tadpoles of Xenopus laevis , the effects of an exposure to hypergravity on the development of the roll-induced static vestibuloocular reflex (rVOR) were investigated. Special attention was given to the onset of the 9 or 12 days lasting 3 g period during early life. Recordings of rVOR characteristics for complete 360° rolls of the tadpoles started 24 h after the end of the 3 g period. The rVOR peak-to-peak amplitudes from the 3 g samples recorded at the 2nd and 3rd day after termination of the 3 g exposure agreed with that recorded from the 1 g reared tadpoles for the youngest group, but were reduced by 30% in the older tadpoles. During further development under 1 g condition, the NOR amplitude of tadpoles with 3 g experience did not change if the 3 g exposure started before the first appearance of the rVOR, but increased if it had started thereafter, albeit on a lower level than that of the 1 g reared siblings. The results support the existence of a sensitive period for the rVOR development, and additionally demonstrate that the period during which the rVOR appeared for the first time is an important milestone for the development of adaptive properties of the underlying neuronal network.

A hypergravity related sensitive period during the development of the roll induced vestibuloocular reflex in an amphibian ( Xenopus laevis)

In tadpoles of Xenopus laevis, the effects of an exposure to hypergravity on the development of the roll-induced static vestibuloocular reflex (rVOR) were investigated. Special attention was given to the onset of the 9 or 12 days lasting 3 g period during early life. Recordings of rVOR characteristics for complete 360° rolls of the tadpoles started 24 h after the end of the 3 g period. The rVOR peak-to-peak amplitudes from the 3 g samples recorded at the 2nd and 3rd day after termination of the 3 g exposure agreed with that recorded from the 1 g reared tadpoles for the youngest group, but were reduced by 30% in the older tadpoles. During further development under 1 g condition, the NOR amplitude of tadpoles with 3 g experience did not change if the 3 g exposure started before the first appearance of the rVOR, but increased if it had started thereafter, albeit on a lower level than that of the 1 g reared siblings. The results support the existence of a sensitive period for the rVOR development, and additionally demonstrate that the period during which the rVOR appeared for the first time is an important milestone for the development of adaptive properties of the underlying neuronal network.

Readaptation of the vestibuloocular reflex to 1g-Condition in immature lower vertebrates ( Xenopus laevis) after micro- or hypergravity exposure

The effects of altered gravitational conditions (AGC) on the development of the static vestibulo-ocular reflex (VOR) and readaptation to 1g were investigated in the amphibian Xenopus laevis. Tadpoles were exposed to microgravity (μg) during the German Space Mission D-2 for 10 days, using the STATEX closed survival system, or to 3g for 9 days during earth-bound experiments. At the beginning of AGC, the tadpoles had not yet developed the static VOR. The main results were: (i) Tadpoles with ug- or 3g-experience had a lower gain of the static VOR than the 1g-controls during the 2nd and 5th post-AGC days, (ii) Readaptation to response levels of 1g-reared controls usually occurred during the following weeks, except in slowly developing tadpoles with 3g-experience. Readaptation was less pronounced if, during the acute VOR test, tadpoles were rolled from the inclined to the normal posture than in the opposite test situation. It is postulated that (i) gravity is necessarily involved in the development of the static VOR, but only during a period including the time before onset of the first behavioural response; and (ii) readaptation which is superimposed by the processes of VOR development depends on many factors including the velocity of development, the actual excitation level of the vestibular systems and the neuroplastic properties of its specific pathways.

The Static Vestibuloocular Reflex in Lower Vertebrates After a Transient Gravity Deprivation During an Early Period of Life

The Static Vestibuloocular Reflex in Lower Vertebrates After a Transient Gravity Deprivation During an Early Period of Life

The development of the static vestibulo-ocular reflex in the southern clawed toad, Xenopus laevis. II. Animals with acute vestibular lesions.

Acute hemilabyrinthectomized tadpoles of the Southern Clawed Toad (Xenopus laevis), younger than stage 47 (about 6 days old), perform no static vestibulo-ocular reflex (Fig. 1). Older acute lesioned animals respond with compensatory movements of both eyes during static roll. Their threshold roll angle, however, depends on the developmental stage. For lesioned stages 60 to 64, it is 75 degrees while stage 52 to 56 tadpoles respond even during a lateral roll of 15 degrees (Figs. 1 and 2). Selective destruction of single macula and crista organs revealed that the static vestibulo-ocular reflex is evoked by excitation of the macula utriculi (Figs. 3 and 4) even in young tadpoles. The results demonstrate that bilateral projections of the vestibular apparatus must have developed at the time of occurrence of the static VOR, that during the first week of life the excitation of a single labyrinth is subthreshold (Fig. 1). We discuss the possibility whether the loss of the static VOR during the prometamorphic period of life (Fig. 2) is caused by increasing formation of multimodal connections in the vestibular pathway.

The development of the static vestibulo-ocular reflex in the southern clawed toad, Xenopus laevis. III. Chronic hemilabyrinthectomized tadpoles.

The static vestibulo-ocular reflex was investigated in tadpoles at different times following unilateral destruction of the labyrinth during the period of early organogenesis and premetamorphosis. Balance compensation is completed after a few weeks, while gain compensation only occurs partially (Figs. 2-4). Tadpoles hemilabyrinthectomized in the age of 2.5 days (stage 38) develop no vestibular nuclei on their lesioned side, while tadpoles operated later in their life, possess these nuclei (Figs. 5, 6) even if they were not detectable at the operation day (Fig. 7). For their dorsal vestibular nucleus (DVN), the number of neurons is usually larger on the intact than on the lesioned side; while for the ventral vestibular nucleus (VVN), there is either numerical symmetry or a transient decrease of cell number on the intact side (Fig. 5). The results demonstrate that vestibular compensation occurs even if vestibular nuclei have developed only on one side, i.e. the vestibular commissure is not a prerequisite for a successful compensation process. It is discussed whether the use of extra-vestibular error signals for balance but not for gain compensation may cause the differences in time courses of both compensation processes.

The development of the static vestibulo-ocular reflex in the southern clawed toad, Xenopus laevis. I. Intact animals.

In the clawed toad, Xenopus laevis, the static vestibulo-ocular reflex appears in 3 days old tadpoles (developmental stage 42) (Fig. 2). The amplitude and gain of this reflex increase up to stage 52, and then decrease to an almost constant value at stage 60 and older tadpoles (Fig. 3). The most effective roll angle gradually increases during development (Fig. 4). The size of the sensory epithelia reaches the final value at the end of the premetamorphic period (stage 56) (Fig. 5). The small-cellular medial ventral vestibular nucleus (VVN) reaches its maximal number of neurons before the large-cellular lateral VVN. Cell death is more pronounced in the medial than in the lateral part of the VVN. In the dorsal vestibular nucleus (DVN), the numerical development of the small and large neurons is similar to that in the small-cellular medial and large-cellular lateral portion of the VVN (Fig. 7). The results demonstrate that labyrinth and oculomotor centres are anatomically connected before the labyrinth and the vestibular nuclei are fully developed. We discuss the possibility that the ciliary polarity pattern of the sensory epithelium is radial during the first period of life, and changes to the vertebrate fan-type pattern during the second week of life. According to the increase of gain during the first three weeks of life, an increase of the spontaneous activity of vestibular neurons may occur during this period.

The Development of the Static Vestibulo-Ocular Reflex in Xenopus

Abstract The relation between the amount of the static vestibulo-ocular reflex arc and the developmental stage is characterized by an optimum function. The reflexes occur before the labyrinth is completely developed, but at this time, bilateral connections of the labyrinth with the oculomotor centers are efficient.