An experimentally informed computational model of neurovestibular adaptation to altered gravity.
Bayesian inference
astronaut
centrifugation
hypergravity
sensorimotor
spaceflight
Journal
Experimental physiology
ISSN: 1469-445X
Titre abrégé: Exp Physiol
Pays: England
ID NLM: 9002940
Informations de publication
Date de publication:
16 Apr 2024
16 Apr 2024
Historique:
received:
09
02
2024
accepted:
27
03
2024
medline:
16
4
2024
pubmed:
16
4
2024
entrez:
16
4
2024
Statut:
aheadofprint
Résumé
Transitions to altered gravity environments result in acute sensorimotor impairment for astronauts, leading to serious mission and safety risks in the crucial first moments in a new setting. Our understanding of the time course and severity of impairment in the early stages of adaptation remains limited and confounded by unmonitored head movements, which are likely to impact the rate of adaptation. Here, we aimed to address this gap by using a human centrifuge to simulate the first hour of hypergravity (1.5g) exposure and the subsequent 1g readaptation period, with precisely controlled head tilt activity. We quantified head tilt overestimation via subjective visual vertical and found ∼30% tilt overestimation that did not decrease over the course of 1 h of exposure to the simulated gravity environment. These findings extended the floor of the vestibular adaptation window (with controlled vestibular cueing) to 1 h of exposure to altered gravity. We then used the empirical data to inform a computational model of neurovestibular adaptation to changes in the magnitude of gravity, which can offer insight into the adaptation process and, with further tuning, can be used to predict the temporal dynamics of vestibular-mediated misperceptions in altered gravity.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NASA
ID : 80NSSC21K1271
Pays : United States
Informations de copyright
© 2024 The Authors. Experimental Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society.
Références
Aitchison, L., Jegminat, J., Menendez, J. A., Pfister, J.‐P., Pouget, A., & Latham, P. E. (2021). Synaptic plasticity as Bayesian inference. Nature Neuroscience, 24, 565–571.
Allred, A. R., & Clark, T. K. (2023). Vestibular perceptual thresholds for rotation about the yaw, roll, and pitch axes. Experimental Brain Research, 241(4), 1101–1115.
Allred, A. R., Kravets, V. G., Ahmed, N., & Clark, T. K. (2023). Modeling orientation perception adaptation to altered gravity environments with memory of past sensorimotor states. Frontiers in Neural Circuits, 17, 1190582.
Bloomberg, J. J., Peters, B. T., Cohen, H. S., & Mulavara, A. P. (2015). Enhancing astronaut performance using sensorimotor adaptability training. Frontiers in Systems Neuroscience, 9, 129.
Bos, J., & Bles, W. (1998). Modelling motion sickness and subjective vertical mismatch detailed for vertical motions. Brain Research Bulletin, 47(5), 537–542.
Bos, J. E., MacKinnon, S. N., & Patterson, A. (2005). Motion sickness symptoms in a ship motion simulator: Effects of inside, outside, and no view. Aviation, Space, and Environmental Medicine, 76(12), 1111–1118.
Braithwaite, M., Groh, S., & Alvarez, E. (1997). Spatial Disorientation in U.S. Army Helicopter Accidents: An Update of the 1987–92 Survey to Include 1993–95 (pp. 97‐13). Army Aeromedical Research Lab.
Bretl, K. N., & Clark, T. K. (2020). Improved feasibility of astronaut short‐radius artificial gravity through a 50‐day incremental, personalized, vestibular acclimation protocol. NPJ Microgravity, 6(1), 22.
Brooks, J. X., Carriot, J., & Cullen, K. E. (2015). Learning to expect the unexpected: Rapid updating in primate cerebellum during voluntary self‐motion. Nature Neuroscience, 18(9), 1310–1317.
Carriot, J., Cullen, K. E., & Chacron, M. J. (2021). The neural basis for violations of Weber's law in self‐motion perception. Proceedings of the National Academy of Sciences, 118(36), e2025061118.
Clark, T. K. (2019). Effects of spaceflight on the vestibular system. In Y. Pathak, M. Araújo dos Santos, & L. Zea (Eds.), Handbook of space pharmaceuticals (pp. 1–39). Springer International Publishing.
Clark, T. K., Newman, M. C., Oman, C. M., Merfeld, D. M., & Young, L. R. (2015). Human perceptual overestimation of whole body roll tilt in hypergravity. Journal of Neurophysiology, 113(7), 2062–2077.
Clark, T. K., & Young, L. R. (2017). A case study of human roll tilt perception in hypogravity. Aerospace Medicine and Human Performance, 88(7), 682–687.
Clément, G., & Wood, S. J. (2014). Rocking or rolling—perception of ambiguous motion after returning from space. PLoS ONE, 9(10), e111107.
Darlington, T. R., Beck, J. M., & Lisberger, S. G. (2018). Neural implementation of Bayesian inference in a sensorimotor behavior. Nature Neuroscience, 21(10), 1442–1451.
Diaz‐Artiles, A., & Karmali, F. (2021). Vestibular precision at the level of perception, eye movements, posture, and neurons. Neuroscience, 468, 282–320.
Fetsch, C. R., Pouget, A., DeAngelis, G. C., & Angelaki, D. E. (2012). Neural correlates of reliability‐based cue weighting during multisensory integration. Nature Neuroscience, 15(1), 146–U185.
Fetsch, C. R., Turner, A. H., DeAngelis, G. C., & Angelaki, D. E. (2009). Dynamic reweighting of visual and vestibular cues during self‐motion perception. The Journal of Neuroscience, 29(49), 15601–15612.
Galvan‐Garza, R. C., Clark, T. K., Sherwood, D., Diaz‐Artiles, A., Rosenberg, M., Natapoff, A., Karmali, F., Oman, C. M., & Young, L. R. (2018). Human perception of whole body roll‐tilt orientation in a hypogravity analog: Underestimation and adaptation. Journal of Neurophysiology, 120(6), 3110–3121.
Goldberg, J., & Fernandez, C. (1971). Physiology of peripheral neurons innervating semicircular canals of squirrel monkey. I. Resting discharge and response to constant angular accelerations. Journal of Neurophysiology, 34(4), 635–660.
Golding, J. F. (1998). Motion sickness susceptibility questionnaire revised and its relationship to other forms of sickness. Brain Research Bulletin, 47(5), 507–516.
Golding, J. F. (2006). Predicting individual differences in motion sickness susceptibility by questionnaire. Personality and Individual Differences, 41(2), 237–248.
Groen, E., Clark, T. K., Houben, M., Bos, J., & Mumaw, R. (2022). Objective evaluation of the somatogravic illusion from flight data of an airplane accident. Safety, 8(4), 4.
Haque, A., Angelaki, D. E., & Dickman, J. D. (2004). Spatial tuning and dynamics of vestibular semicircular canal afferents in rhesus monkeys. Experimental Brain Research, 155(1), 81–90.
Howard, I. P. (1982). Human visual orientation. J. Wiley.
Hupfeld, K. E., McGregor, H. R., Koppelmans, V., Beltran, N. E., Kofman, I. S., De Dios, Y. E., Riascos, R. F., Reuter‐Lorenz, P. A., Wood, S. J., Bloomberg, J. J., Mulavara, A. P., & Seidler, R. D. (2022). Brain and behavioral evidence for reweighting of vestibular inputs with long‐duration spaceflight. Cerebral Cortex, 32(4), 755–769.
Jamali, M., Carriot, J., Chacron, M. J., & Cullen, K. E. (2019). Coding strategies in the otolith system differ for translational head motion vs. Static orientation relative to gravity. eLife, 8, e45573.
Kobel, M. J., Wagner, A. R., Merfeld, D. M., & Mattingly, J. K. (2021). Vestibular thresholds: A review of advances and challenges in clinical applications. Frontiers in Neurology, 12, 643634.
Körding, K. P., & Wolpert, D. M. (2004). Bayesian integration in sensorimotor learning. Nature, 427(6971), 244–247.
Kravets, V. G., Ahmed, N., & Clark, T. (2022). A rao‐blackwellized particle filter for modeling neurovestibular adaptation to altered gravity. 2022 International Conference on Environmental Systems.
Kravets, V. G., Dixon, J. B., Ahmed, N. R., & Clark, T. K. (2021). COMPASS: Computations for orientation and motion perception in altered sensorimotor states. Frontiers in Neural Circuits, 15, 757817.
Lackner, J. R., & DiZio, P. (2006). Space motion sickness. Experimental Brain Research, 175(3), 377–399.
Laurens, J., & Droulez, J. (2007). Bayesian processing of vestibular information. Biological Cybernetics, 96(4), 389–404.
Mackrous, I., Carriot, J., Jamali, M., & Cullen, K. E. (2019). Cerebellar prediction of the dynamic sensory consequences of gravity. Current Biology, 29(16), 2698–2710.e4.
Merfeld, D. M. (2003). Rotation otolith tilt‐translation reinterpretation (ROTTR) hypothesis: A new hypothesis to explain neurovestibular spaceflight adaptation. Journal of Vestibular Research, 13(4–6), 309–320.
Merfeld, D. M., Young, L. R., Oman, C. M., & Shelhamer, M. J. (1993). A multidimensional model of the effect of gravity on the spatial orientation of the monkey. Journal of Vestibular Research: Equilibrium & Orientation, 3(2), 141–161.
Merfeld, D. M., Young, L. R., Paige, G. D., & Tomko, D. L. (1993). Three dimensional eye movements of squirrel monkeys following postrotatory tilt. Journal of Vestibular Research: Equilibrium & Orientation, 3(2), 123–139.
Merfeld, D. M., & Zupan, L. (2002). Neural processing of gravitoinertial cues in humans. III. Modeling tilt and translation responses. Journal of Neurophysiology, 87(2), 819–833.
Merfeld, D. M., Zupan, L., & Peterka, R. J. (1999). Humans use internal models to estimate gravity and linear acceleration. Nature, 398(6728), 615–618.
Meskers, A. J. H., Houben, M. M. J., Pennings, H. J. M., Clément, G., & Groen, E. L. (2021). Underestimation of self‐tilt increases in reduced gravity conditions. Journal of Vestibular Research, 31(5), 345–352.
Miller, E. F., & Graybiel, A. (1966). Magnitude of gravitoinertial force, an independent variable in egocentric visual localization of the horizontal. Journal of Experimental Psychology, 71(3), 452–460.
Mulavara, A. P., Peters, B. T., Miller, C. A., Kofman, I. S., Reschke, M. F., Taylor, L. C., Lawrence, E. L., Wood, S. J., Laurie, S. S., Lee, S. M. C., Buxton, R. E., May‐Phillips, T. R., Stenger, M. B., Ploutz‐Snyder, L. L., Ryder, J. W., Feiveson, A. H., & Bloomberg, J. J. (2018). Physiological and functional alterations after spaceflight and bed rest. Medicine & Science in Sports & Exercise, 50(9), 1961–1980.
Newman, M. C. (2009). A multisensory observer model for human spatial orientation perception. MIT.
Paloski, W. H., Oman, C. M., Bloomberg, J. J., Reschke, M. F., Wood, S. J., Harm, D. L., Peters, B. T., Mulavara, A. P., Locke, J. P., & Stone, L. S. (2008). Risk of sensory‐motor performance failures affecting vehicle control during space missions: A review of the evidence. Journal of Gravitational Physiology, 15, 29.
Paloski, W., Reschke, M., Black, F., & Dow, R. (1999). Recovery of postural equilibrium control following space flight. Extended Duration Orbiter Medical Project Final Report 1989–1995. NASA SP‐1999‐534. https://www.researchgate.net/publication/24328542_Recovery_of_postural_equilibrium_control_following_space_flight
Poisson, R. J., & Miller, M. E. (2014). Spatial disorientation mishap trends in the U.S. Air Force 1993–2013. Aviation, Space, and Environmental Medicine, 85(9), 919–924.
Quenouille, M. H. (1956). Notes on bias in estimation. Biometrika, 43(3–4), 353–360.
Reschke, M. F., Bloomberg, J. J., Harm, D. L., Paloski, W. H., Layne, C., & McDonald, V. (1998). Posture, locomotion, spatial orientation, and motion sickness as a function of space flight. Brain Research Reviews, 28(1–2), 102–117.
Roy, J. E., & Cullen, K. E. (2004). Dissociating self‐generated from passively applied head motion: Neural mechanisms in the vestibular Nuclei. Journal of Neuroscience, 24(9), 2102–2111.
Schoenmaekers, C., De Laet, C., Kornilova, L., Glukhikh, D., Moore, S., MacDougall, H., Naumov, I., Fransen, E., Wille, L., Jillings, S., & Wuyts, F. L. (2022). Ocular counter‐roll is less affected in experienced versus novice space crew after long‐duration spaceflight. NPJ Microgravity, 8(1), 27.
Schöne, H. (1964). On the role of gravity in human spatial orientation. Aerospace Medicine, 35, 764–772.
Shelhamer, M. (2015). Trends in sensorimotor research and countermeasures for exploration‐class space flights. Frontiers in Systems Neuroscience, 9, 115.
Suri, K., & Clark, T. K. (2020). Human vestibular perceptual thresholds for pitch tilt are slightly worse than for roll tilt across a range of frequencies. Experimental Brain Research, 238(6), 1499–1509.
Tarnutzer, A. A., Bockisch, C., Straumann, D., & Olasagasti, I. (2009). Gravity dependence of subjective visual vertical variability. Journal of Neurophysiology, 102(3), 1657–1671.
Tin, C., & Poon, C.‐S. (2005). Internal models in sensorimotor integration: Perspectives from adaptive control theory. Journal of Neural Engineering, 2(3), S147–S163.
Tjernström, F., Fransson, P.‐A., Hafström, A., & Magnusson, M. (2002). Adaptation of postural control to perturbations—A process that initiates long‐term motor memory. Gait & Posture, 15(1), 75–82.
Vingerhoets, R., Medendorp, W., & Van Gisbergen, J. (2006). Time course and magnitude of illusory translation perception during off‐vertical axis rotation. Journal of Neurophysiology, 95(3), 1571–1587.
Vingerhoets, R., Van Gisbergen, J., & Medendorp, W. (2007). Verticality perception during off‐vertical axis rotation. Journal of Neurophysiology, 97(5), 3256–3268.
Wood, S. J., Paloski, W. H., & Clark, J. B. (2015). Assessing sensorimotor function following ISS with computerized dynamic posturography. Aerospace Medicine and Human Performance, 86(12), 45–53.