Human manual control precision depends on vestibular sensory precision and gravitational magnitude.

Precise motion control is critical to human survival on Earth and in space. Motion sensation is inherently imprecise, and the functional implications of this imprecision are not well understood. We studied a "vestibular" manual control task in which subjects attempted to keep themselves upright with a rotational hand controller (i.e., joystick) to null out pseudorandom, roll-tilt motion disturbances of their chair in the dark. Our first objective was to study the relationship between intersubject differences in manual control performance and sensory precision, determined by measuring vestibular perceptual thresholds. Our second objective was to examine the influence of altered gravity on manual control performance. Subjects performed the manual control task while supine during short-radius centrifugation, with roll tilts occurring relative to centripetal accelerations of 0.5, 1.0, and 1.33 GC (1 GC = 9.81 m/s2). Roll-tilt vestibular precision was quantified with roll-tilt vestibular direction-recognition perceptual thresholds, the minimum movement that one can reliably distinguish as leftward vs. rightward. A significant intersubject correlation was found between manual control performance (defined as the standard deviation of chair tilt) and thresholds, consistent with sensory imprecision negatively affecting functional precision. Furthermore, compared with 1.0 GC manual control was more precise in 1.33 GC (-18.3%, P = 0.005) and less precise in 0.5 GC (+39.6%, P < 0.001). The decrement in manual control performance observed in 0.5 GC and in subjects with high thresholds suggests potential risk factors for piloting and locomotion, both on Earth and during human exploration missions to the moon (0.16 G) and Mars (0.38 G). NEW & NOTEWORTHY The functional implications of imprecise motion sensation are not well understood. We found a significant correlation between subjects' vestibular perceptual thresholds and performance in a manual control task (using a joystick to keep their chair upright), consistent with sensory imprecision negatively affecting functional precision. Furthermore, using an altered-gravity centrifuge configuration, we found that manual control precision was improved in "hypergravity" and degraded in "hypogravity." These results have potential relevance for postural control, aviation, and spaceflight.

[1]  Jean Laurens,et al.  Bayesian processing of vestibular information , 2007, Biological Cybernetics.

[2]  T. Brady,et al.  The challenge of safe lunar landing , 2010, 2010 IEEE Aerospace Conference.

[3]  A. J. Benson,et al.  Thresholds for the detection of the direction of whole-body, linear movement in the horizontal plane. , 1986, Aviation, space, and environmental medicine.

[4]  Frans C. T. van der Helm,et al.  An adaptive model of sensory integration in a dynamic environment applied to human stance control , 2001, Biological Cybernetics.

[5]  T. Mergner,et al.  Human postural responses to motion of real and virtual visual environments under different support base conditions , 2005, Experimental Brain Research.

[6]  R. Peterka,et al.  Sensory reweighting dynamics following removal and addition of visual and proprioceptive cues. , 2016, Journal of neurophysiology.

[7]  Jonathan B. Clark,et al.  Head-eye coordination during simulated orbiter landing. , 2008, Aviation, space, and environmental medicine.

[8]  M. De Vrijer,et al.  Accuracy-precision trade-off in visual orientation constancy. , 2009, Journal of vision.

[9]  Richard F. Lewis,et al.  Bayesian optimal adaptation explains age-related human sensorimotor changes. , 2018, Journal of neurophysiology.

[10]  Jennifer L. Campos,et al.  Bayesian integration of visual and vestibular signals for heading. , 2009, Journal of vision.

[11]  D M Merfeld,et al.  Effect of spaceflight on ability to sense and control roll tilt: human neurovestibular studies on SLS-2. , 1996, Journal of applied physiology.

[12]  J. R. Lackner,et al.  Mechanisms of human static spatial orientation , 2006, Experimental Brain Research.

[13]  Learning dynamic control of body roll orientation , 2016, Experimental Brain Research.

[14]  Dora E Angelaki,et al.  A unified internal model theory to resolve the paradox of active versus passive self-motion sensation , 2017, bioRxiv.

[15]  Laurence R. Young,et al.  Human manual control performance in hyper-gravity , 2015, Experimental Brain Research.

[16]  Richard J Krauzlis,et al.  Shared Response Preparation for Pursuit and Saccadic Eye Movements , 2003, The Journal of Neuroscience.

[17]  R. Strobl,et al.  Comparison of linear motion perception thresholds in vestibular migraine and Menière’s disease , 2016, European Archives of Oto-Rhino-Laryngology.

[18]  Daniel M Merfeld,et al.  A distributed, dynamic, parallel computational model: the role of noise in velocity storage. , 2012, Journal of neurophysiology.

[19]  W. Bialek,et al.  A sensory source for motor variation , 2005, Nature.

[20]  W. Pieter Medendorp,et al.  A Bayesian Account of Visual–Vestibular Interactions in the Rod-and-Frame Task , 2016, eNeuro.

[21]  Yue M. Lu,et al.  Dynamics of individual perceptual decisions. , 2016, Journal of neurophysiology.

[22]  H. Mittelstaedt,et al.  Somatic graviception , 1996, Biological Psychology.

[23]  Karl R. Gegenfurtner,et al.  Precision of speed discrimination and smooth pursuit eye movements , 2009, Vision Research.

[24]  Richard F. Lewis,et al.  Vestibular Labyrinth Contributions to Human Whole-Body Motion Discrimination , 2012, The Journal of Neuroscience.

[25]  Brian T. Peters,et al.  RISK OF SENSORY-MOTOR PERFORMANCE FAILURES AFFECTING VEHICLE CONTROL DURING SPACE MISSIONS: A REVIEW OF THE EVIDENCE , 2008 .

[26]  Mark Shelhamer,et al.  The dynamics of parabolic flight: flight characteristics and passenger percepts. , 2008, Acta astronautica.

[27]  L R Young,et al.  Spatial orientation in weightlessness and readaptation to earth's gravity. , 1984, Science.

[28]  H SCHOENE,et al.  ON THE ROLE OF GRAVITY IN HUMAN SPATIAL ORIENTATION. , 1964, Aerospace medicine.

[29]  Ola Eiken,et al.  Semicircular canal contribution to the perception of roll tilt during gondola centrifugation. , 2005, Aviation, space, and environmental medicine.

[30]  Herman van der Kooij,et al.  A multisensory integration model of human stance control , 1999, Biological Cybernetics.

[31]  Eric R. Ziegel,et al.  Generalized Linear Models , 2002, Technometrics.

[32]  J. Goldberg,et al.  Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. II. Response to sinusoidal stimulation and dynamics of peripheral vestibular system. , 1971, Journal of neurophysiology.

[33]  Alexander Sacha Panic,et al.  Direction of balance and perception of the upright are perceptually dissociable. , 2015, Journal of neurophysiology.

[34]  A. J. Benson,et al.  Thresholds for the perception of whole body angular movement about a vertical axis. , 1989, Aviation, space, and environmental medicine.

[35]  Yongwoo Yi,et al.  Determining thresholds using adaptive procedures and psychometric fits: evaluating efficiency using theory, simulations, and human experiments , 2015, Experimental Brain Research.

[36]  Lauren Scharff,et al.  Spatial disorientation: decades of pilot fatalities. , 2011, Aviation, space, and environmental medicine.

[37]  Jones Gm,et al.  Origin significance and amelioration of coriolis illusions from the semicircular canals: a non-mathematical appraisal. , 1970 .

[38]  D H Weir,et al.  Theory of manual vehicular control. , 1969, Ergonomics.

[39]  W. F. Rogers Apollo Lunar Module Landing Gear , 1972 .

[40]  Daniel M Merfeld,et al.  Perceptual precision of passive body tilt is consistent with statistically optimal cue integration. , 2017, Journal of neurophysiology.

[41]  Daniel M. Merfeld,et al.  Signal detection theory and vestibular thresholds: I. Basic theory and practical considerations , 2011, Experimental Brain Research.

[42]  Laurence R. Young,et al.  Optimal Estimator Model for Human Spatial Orientation a , 1988 .

[43]  Laurence R. Young,et al.  Modeling human perception of orientation in altered gravity , 2015, Front. Syst. Neurosci..

[44]  Fred W. Mast,et al.  Vestibular thresholds for yaw rotation about an earth-vertical axis as a function of frequency , 2008, Experimental Brain Research.

[45]  A. N. Exton-smith,et al.  Falls in the elderly related to postural imbalance. , 1977, British medical journal.

[46]  S Glasauer,et al.  Determinants of orientation in microgravity. , 1992, Acta astronautica.

[47]  Daniel M Merfeld,et al.  Human perceptual overestimation of whole body roll tilt in hypergravity. , 2015, Journal of neurophysiology.

[48]  R. Peterka Sensorimotor integration in human postural control. , 2002, Journal of neurophysiology.

[49]  G. DeAngelis,et al.  Vestibular Heading Discrimination and Sensitivity to Linear Acceleration in Head and World Coordinates , 2010, The Journal of Neuroscience.

[50]  Daniel M Merfeld,et al.  Abnormal motion perception in vestibular migraine , 2011, The Laryngoscope.

[51]  Mohsen Jamali,et al.  Response of vestibular nerve afferents innervating utricle and saccule during passive and active translations. , 2009, Journal of neurophysiology.

[52]  Torin K Clark,et al.  The Impact of Oral Promethazine on Human Whole-Body Motion Perceptual Thresholds , 2017, Journal of the Association for Research in Otolaryngology.

[53]  R. Krauzlis,et al.  Shared motion signals for human perceptual decisions and oculomotor actions. , 2003, Journal of vision.

[54]  H. Strasburger,et al.  Fitting the psychometric function , 1999, Perception & psychophysics.

[55]  Katherine I. Nagel,et al.  Cortical Mechanisms of Smooth Eye Movements Revealed by Dynamic Covariations of Neural and Behavioral Responses , 2008, Neuron.

[56]  Laurence R. Young,et al.  Perception of the Body in Space: Mechanisms , 2011 .

[57]  Michael G. Paulin,et al.  Dynamics of Compensatory Eye Movement Control: an Optimal Estimation Analysis of the Vestibulo-Ocular Reflex , 1989, Int. J. Neural Syst..

[58]  T E Hanna,et al.  Estimation of psychometric functions from adaptive tracking procedures , 1992, Perception & psychophysics.

[59]  M. Chacron,et al.  Neural Variability, Detection Thresholds, and Information Transmission in the Vestibular System , 2007, Journal of Neuroscience.

[60]  Mark Shelhamer,et al.  Neurovestibular considerations for sub-orbital space flight: A framework for future investigation. , 2010, Journal of vestibular research : equilibrium & orientation.

[61]  S. Lisberger,et al.  Variation, Signal, and Noise in Cerebellar Sensory–Motor Processing for Smooth-Pursuit Eye Movements , 2007, The Journal of Neuroscience.

[62]  Daniel M Merfeld,et al.  Whole body motion-detection tasks can yield much lower thresholds than direction-recognition tasks: implications for the role of vibration. , 2013, Journal of neurophysiology.

[63]  Adam D Goodworth,et al.  Sensorimotor control of the trunk in sitting sway referencing. , 2018, Journal of neurophysiology.

[64]  G. M. Jones,et al.  Origin significance and amelioration of coriolis illusions from the semicircular canals: a non-mathematical appraisal. , 1970, Aerospace medicine.

[65]  T A Stoffregen,et al.  The role of balance dynamics in the active perception of orientation. , 1992, Journal of experimental psychology. Human perception and performance.

[66]  A M Bronstein,et al.  Perceptual and nystagmic thresholds of vestibular function in yaw. , 2004, Journal of vestibular research : equilibrium & orientation.

[67]  Daniel M. Merfeld,et al.  Signal detection theory and vestibular perception: III. Estimating unbiased fit parameters for psychometric functions , 2012, Experimental Brain Research.

[68]  D Straumann,et al.  Gravity dependence of subjective visual vertical variability. , 2009, Journal of neurophysiology.

[69]  Daniel M. Merfeld,et al.  Multivariate Analyses of Balance Test Performance, Vestibular Thresholds, and Age , 2017, Front. Neurol..

[70]  A. Faisal,et al.  Noise in the nervous system , 2008, Nature Reviews Neuroscience.

[71]  F. Karmali,et al.  Variability in the Vestibulo-Ocular Reflex and Vestibular Perception , 2018, Neuroscience.

[72]  C Kaernbach,et al.  Slope bias of psychometric functions derived from adaptive data , 2001, Perception & psychophysics.

[73]  Dora E Angelaki,et al.  Computational approaches to spatial orientation: from transfer functions to dynamic Bayesian inference. , 2008, Journal of neurophysiology.

[74]  Daniel M Merfeld,et al.  Visual and vestibular perceptual thresholds each demonstrate better precision at specific frequencies and also exhibit optimal integration. , 2014, Journal of neurophysiology.

[75]  Benjamin T. Crane,et al.  Suprathreshold asymmetries in human motion perception , 2012, Experimental Brain Research.

[76]  M. Leek Adaptive procedures in psychophysical research , 2001, Perception & psychophysics.

[77]  María Carolina Bermúdez Rey,et al.  Vestibular Perceptual Thresholds Increase above the Age of 40 , 2016, Front. Neurol..

[78]  Herman van der Kooij,et al.  Non-linear stimulus-response behavior of the human stance control system is predicted by optimization of a system with sensory and motor noise , 2010, Journal of Computational Neuroscience.

[79]  Benjamin T. Crane,et al.  Direction Specific Biases in Human Visual and Vestibular Heading Perception , 2012, PloS one.

[80]  Paul A. Harris,et al.  Research Electronic Data Capture (REDCap) - planning, collecting and managing data for clinical and translational research , 2012, BMC Bioinformatics.

[81]  Daniel M Merfeld,et al.  Frequency dependence of vestibuloocular reflex thresholds. , 2012, Journal of neurophysiology.

[82]  M. M. Taylor,et al.  PEST: Efficient Estimates on Probability Functions , 1967 .