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Functional Responses in Otolith Structures from Micro- to Hyper-Gravity

Vertebrates and invertebrates sense gravito-inertial acceleration by mechanoreceptors in the otolith and statolith organs, respectively. These structures consist of ciliated sensory hair cells surmounted by biomineral grains of calcium carbonate (CaCO3) called oto-orstato-conia. The grains provide mechanical loading of hair cell cilia, and their high density increases sensitivity to acceleration. A widely considered mechanism by which the animal responds to a chronic change in amplitude of gravity is a change in weight lending otoconia. In G, it is argued, the organism counters the loss of gravity by increasing CaCO3 production, thereby increasing otolith mass, as a means to increase system gain. In hypergravity (HG), the converse is argued. Here, we present the results obtained in 3 species exposed both to G and HG. Adult toadfish, Opsanus tau, were exposed to G in 2 short-duration shuttle missions and to 1.24 1.73G centrifugation for 1-32 days; re-adaptation was studied following 1-8 days of 1G. Results show a biphasic pattern in response to 1.73G: initial hypersensitivity, similar to that observed after G exposure, followed by transition to a significant decrease at 16-32 days. Recovery from HG exposure is 4-8 days. Next, we examined directly the responses of statocyst receptors in the land snail after exposure to G on two unmanned Russian Orbital missions and at 1.24G. Similar to vertebrate afferents snail receptors increased their sensitivity to tilt after G exposure, and decrease it after 16-32 days of HG. Two major pieces of information are still needed: vertebrate hair cell response to altered gravity and impact of longer duration exposures on sensory plasticity. To address the latter, we applied electron microscopic techniques to image otoconia mass obtained from 1) mice subjected to 91-days of weightlessness in the Mouse Drawer System (MDS) flown on International Space Station, 2) mice subjected to 91-days of 1.24G centrifugation on ground, and 3) mice flown on 2 short-duration orbital missions. Images indicate a clear restructuring of individual otoconia, suggesting deposition to the outer shell. Images from their HG counterparts indicate the converse - an ablation of the otoconia mass. For shorter duration exposures to weightlessness on 13-day shuttle missions, mice otoconia appear normal. Despite the permanence of 1G in evolution, the animal senses exposure to a novel, non-1G, environment and adaptive mechanisms are initiated - in the short term, compensation is likely confined to the peripheral sensory receptors, the brain or both. For longer exposures structural modifications of the endorgan may also result. Support Contributed By: NASA 03-OBPR-04 and 11-11_Omni_2-0002

Vertebrates↗

Neural Mechanisms to the Space Environment

Highly conserved neural systems have evolved to sense the inertial forces due to head translation and head tilt relative to gravitational vertical. These structures consist of ciliated mechanosensitive receptor cells inserted into a neuroepithelium surmounted by biomineral grains of calcium carbonate (CaCO3) called oto- (vertebrates) or stato-conia (invertebrates). Detection of these forces by receptor cells relies on the CaCO3 mass being weighted in Earths 1G. A change in gravity or orientation with respect to gravity has a profound effect on how an organism interacts with its environment, and it is evident that the nervous system responds to the new gravity state. This response might involve the peripheral receptors, the CaCO3 mass, the brain or any combination of these mechanisms based on the intensity and duration of the gravity change. Here, we examine the arguments supporting the different mechanisms of adaptation to the space environment. First, a pre- or post-synaptic alteration in the strength of synaptic transmission between the receptor cell and nerve afferent can adjust the system output. The number of synaptic ribbons in certain type II hair cells in rodent is labile, increasing following exposure to microgravity. An increase in number of synaptic ribbons in toadfish otolith hair cells following exposure to microgravity could potentially explain the observed afferent hypersensitivity to acceleration postflight. The physiological findings in the isolated statocyst in snails are in line with the vertebrate data, and conform to the proposition that G exposure leads to changes in gravireceptor function. At the same time this similarity in neural response to G exposure between the vertebrates and invertebrates is intriguing: the increased neural sensitivity in the vertebrate was detected in the nerve afferents, one synapse away from the receptor cell, whereas the increased neural sensitivity observed in the snail was detected directly at the receptor level. Second, the CaCO3 mass provides mechanical loading of receptor cell cilia, and their density alters sensitivity. A widely considered mechanism by which the animal responds to a chronic change in amplitude of gravity is a change in weight-lending CaCO3 mass. In G, it is argued, the organism counters the loss of gravity by increasing CaCO3 production, thereby increasing its mass, as a means to increase system gain. In hypergravity, the converse is argued. Earlier evidence in mollusks and recent results in mice suggest a remodeling might occur, especially after long-term space exposure. Lastly, we have to distinguish at least two kinds of neural feedbacks. One is connected with local mechanisms of self-regulation and specific for initial period of organ development when the neural connections are still absent. And the other feedback is related to neural self-regulation and specific for later stages of the organ development, and includes an efferent vestibular feedback. Complexity of the problem is enhanced by incompleteness of experiments, and consequently the experimental results have not led to a clear interpretation despite the numerous studies.

Boyle, Richard D.↗