Orbital spaceflight during pregnancy shapes function of mammalian vestibular system.

Abstract

Pregnant rats were flown on the NASA Space Shuttle during the early developmental period of their fetuses' vestibular apparatus and onset of vestibular function. The authors report that prenatal spaceflight exposure shapes vestibular-mediated behavior and central morphology. Postflight testing revealed (a) delayed onset of body righting responses, (b) cardiac deceleration (bradycardia) to 70°h ead-up roll, (c) decreased branching of gravistatic afferent axons, but (d) no change in branching of angular acceleration receptor projections with comparable synaptogenesis of the medial vestibular nucleus in flight relative to control fetuses. Kinematic analyses of the dams' on-orbit behavior suggest that, although the fetal otolith organs are unloaded in microgravity, the fetus' semicircular canals receive high levels of stimulation during longitudinal rotations of the mother's weightless body. Behaviorally derived stimulation from maternal movements may be a significant factor in studies of vestibular sensory development. Taken together, these studies provide evidence that gravity and angular acceleration shape prenatal organization and function within the mammalian vestibular system. Keywords microgravity; development; fetus; maternal; otoliths Sensory deprivation during ontogenesis has proven to be a highly effective tool for investigating sensory development. Studies employing dark-rearing (Hubel & Wiesel, 1982), plugging the ears (Batkin, Groth, Watson, & Ansberry, 1970), obstructing the nares (Kucharsky & Hall, 1987), or eliminating tactile input normally supplied by the vibrissae (Woolsey & Wann, 1976) have yielded important insights into how stimulation plays an active, formative role during sensory ontogenesis. Sensory deprivation during early life produces enduring deficits in sensory functions. For example, clinical observations (Peters, Litovsky, Parkinson, & Lake, 2007;Rubinstein & Miller, 1999) have shown that proper acoustic input is critical for the development of hearing; delayed provision of a cochlear implant in children can prevent acquisition of proper understanding of spoken words. Similarly, understanding the roles of early stimulation has augmented clinical approaches in the treatment of visual impairments (Maurer, Lewis, Brent, & Levin, 1999). In contrast to other sensory systems, our understanding of neurovestibular ontogeny has progressed slowly, due, in part, to the historic difficulty of depriving young organisms of the Earth-constant stimulus of gravity. A growing number of techniques are proving their utility for depriving the immature mammalian vestibular system of sensory input. For example, the semicircular canals (Geisler & Gramsbergen, 1998; Correspondence concerning this article should be addressed to April E. Ronca, Department of Obstetrics and Gynecology, Wake Forest University School of Medicine, Winston-Salem, NC 27157. E-mail: aronca@wfubmc.edu. Relatively little work has focused on the emergence of vestibular function. Yet within the sequentially fixed, highly conserve...

Move it or lose it—Is stimulation of the vestibular system necessary for normal spatial memory?

“…Later in evolution, the semicircular canals developed, enabling the detection of angular acceleration as well (Spoor et al, 1994(Spoor et al, , 2002. The vestibular system develops early in embryogenesis (Baker, 1998) so that it detects self-motion and gravitational vertical in the womb (Ronca et al, 2008); at the time of birth, it is almost fully functional, unlike the visual system, which undergoes a more substantial critical period after birth (Curthoys, 1983;Baker, 1998;Lai and Chan, 2001;Hooks and Chen, 2007). Because of its evolutionary significance, the vestibular system may provide the primary, baseline sensory information about self-motion against which all other sensory information is compared (Smith, 1997;Borel et al, 2008).…”

Development of Vestibular Systems in Altered Gravity

“…The numbers of synapses per 18.06 μm 2 were 39.6 ± 13.5 (mean ± SD) in the G1g and 43.5 ± 18.5 in the F0g embryos. The same DiI tracer technique applied to the posterior canal organ revealed no difference in the projection pattern of this organ between F0g and G1g embryos (Bruce and Fritzsch, 1997;Ronca et al, 2008). Neurons within the vestibular nuclei of rats FIGURE 16.10 Redistribution of synaptophysin in vestibular type I hair cells from the utriculus of 2g reared rats at day of birth (P0) and 6th post-natal day (P6) and from the crista lateralis from P6 rats compared to 1g reared rats.…”

“…Physiological activity of afferents matures during the first three postnatal weeks. Connections with the cerebellum, which is part of the control mechanisms of vestibulo-ocular and vestibulospinal reflexes, develop between the first and fourth post-natal week (Lannou et al, 1983;Ronca and Alberts, 2000;Ronca 2003;Raymond et al, 2003;Ronca et al, 2008).…”

“…Vestibular plasticity in response to labyrinthine lesions was intensively studied at the level of the vestibular nuclei (Dieringer, 1985) because throughout the vertebrate kingdom, these sites are integration centers for eye movements and postural reflexes. They are prime candidates for coordination centers for adaptation to altered gravity, as shown by adaptive modifications of afferent projections to the vestibular nuclei (Bruce and Fritzsch, 1997;Ronca et al, 2008) and the distribution of synaptic proteins in cells within the vestibular nuclei (Raymond et al, 2003). Furthermore, non-vestibular structures such as noradrenergic locus coeruleus neurons, which contribute to the control of vestibular responses (Pompeiano et al, 1991;Pompeiano, 2006), might be involved in the adaptation to altered gravity as shown in adult mammals (Pompeiano, 2006;Pompeiano et al, 2002).…”

Functional Development of the Vestibular System

“…Following 11 days in space during the prenatal period (μG, E9-E20), vestibular-specific tests performed on rats suggested they had a retarded ability to respond to gravistatic stimuli (Ronca and Alberts, 1997), abnormal water immersion responses , and increased bradycardia following roll stimulation (Ronca et al, 2008). The labeling of vestibular projections revealed that development in space might decrease the number of gravistatic-afferent synapses to the medial vestibular nucleus but would not change the overall amount of connections, suggesting a trade-off in favor of canal afferent synapses (Ronca et al, 2008). Current evidence suggests that in these animals, adaptation to normal gravity can occur in a few weeks after returning to earth.…”