When Up Is Down in 0g: How Gravity Sensing Affects the Timing of Interceptive Actions

Humans are known to regulate the timing of interceptive actions by modeling, in a simplified way, Newtonian mechanics. Specifically, when intercepting an approaching ball, humans trigger their movements a bit earlier when the target arrives from above than from below. This bias occurs regardless of the ball's true kinetics, and thus appears to reflect an a priori expectation that a downward moving object will accelerate. We postulate that gravito-inertial information is used to tune visuomotor responses to match the target's most likely acceleration. Here we used the peculiar conditions of parabolic flight—where gravity's effects change every 20 s—to test this hypothesis. We found a striking reversal in the timing of interceptive responses performed in weightlessness compared with trials performed on ground, indicating a role of gravity sensing in the tuning of this response. Parallels between these observations and the properties of otolith receptors suggest that vestibular signals themselves might plausibly provide the critical input. Thus, in addition to its acknowledged importance for postural control, gaze stabilization, and spatial navigation, we propose that detecting the direction of gravity's pull plays a role in coordinating quick reactions intended to intercept a fast-moving visual target.

[1]  A. Berthoz,et al.  Contribution of the otoliths to the calculation of linear displacement. , 1989, Journal of neurophysiology.

[2]  J. Goldberg,et al.  Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. I. Response to static tilts and to long-duration centrifugal force. , 1976, Journal of neurophysiology.

[3]  John Ignatius Griffin,et al.  Statistics; methods and applications , 1963 .

[4]  James F. Baker,et al.  The effect of gravity on the horizontal and vertical vestibulo-ocular reflex in the rat , 2000, Experimental Brain Research.

[5]  A Graybiel,et al.  Inversion illusion in parabolic flight: its probable dependence on otolith function. , 1966, Aerospace medicine.

[6]  F. O. Black,et al.  Vestibular perception and action employ qualitatively different mechanisms. I. Frequency response of VOR and perceptual responses during Translation and Tilt. , 2005, Journal of neurophysiology.

[7]  Francesco Lacquaniti,et al.  The role of vision in tuning anticipatory motor responses of the limbs , 1993 .

[8]  F. Lacquaniti,et al.  Does the brain model Newton's laws? , 2001, Nature Neuroscience.

[9]  Joseph McIntyre,et al.  Egocentric and allocentric reference frames for catching a falling object , 2010, Experimental Brain Research.

[10]  John C. Simons,et al.  WEIGHTLESS MAN: A SURVEY OF SENSATIONS AND PERFORMANCE WHILE FREE-FLOATING , 1963 .

[11]  F. Lacquaniti,et al.  Representation of Visual Gravitational Motion in the Human Vestibular Cortex , 2005, Science.

[12]  Vincenzo Maffei,et al.  Vestibular nuclei and cerebellum put visual gravitational motion in context. , 2008, Journal of neurophysiology.

[13]  J. Goldberg,et al.  Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. III. Response dynamics. , 1976, Journal of neurophysiology.

[14]  Maurizio Gentilucci,et al.  Visually guided pointing, the Müller-Lyer illusion, and the functional interpretation of the dorsal-ventral split: Conclusions from 33 independent studies , 2008, Neuroscience & Biobehavioral Reviews.

[15]  Brian L Day,et al.  Otolith and canal reflexes in human standing , 2005, The Journal of physiology.

[16]  F. Lacquaniti,et al.  Internal models and prediction of visual gravitational motion , 2008, Vision Research.

[17]  P. Werkhoven,et al.  Visual processing of optic acceleration , 1992, Vision Research.

[18]  J. Gibson The Ecological Approach to Visual Perception , 1979 .

[19]  J. Lackner,et al.  Sense of Body Position in Parabolic Flight a , 1992, Annals of the New York Academy of Sciences.

[20]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

[21]  Gilles Clément,et al.  Effects of static tilt about the roll axis on horizontal and vertical optokinetic nystagmus and optokinetic after-nystagmus in humans , 2004, Experimental Brain Research.

[22]  L. Harris,et al.  The subjective visual vertical and the perceptual upright , 2006, Experimental Brain Research.

[23]  H Mittelstaedt,et al.  The Role of the Otoliths in Perception of the Vertical and in Path Integration , 1999, Annals of the New York Academy of Sciences.

[24]  J. McIntyre,et al.  Kinematic and dynamic processes for the control of pointing movements in humans revealed by short-term exposure to microgravity , 2005, Neuroscience.

[25]  Francesco Lacquaniti,et al.  Anticipating the effects of gravity when intercepting moving objects: differentiating up and down based on nonvisual cues. , 2005, Journal of neurophysiology.

[26]  F Crevecoeur,et al.  Movement stability under uncertain internal models of dynamics. , 2010, Journal of neurophysiology.

[27]  Jean-Paul Gauthier,et al.  The Inactivation Principle: Mathematical Solutions Minimizing the Absolute Work and Biological Implications for the Planning of Arm Movements , 2008, PLoS Comput. Biol..

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

[29]  Vladimir Pletser,et al.  Short duration microgravity experiments in physical and life sciences during parabolic flights: the first 30 ESA campaigns. , 2004, Acta astronautica.

[30]  Dora E Angelaki,et al.  Resolution of Sensory Ambiguities for Gaze Stabilization Requires a Second Neural Integrator , 2003, The Journal of Neuroscience.

[31]  F. Lacquaniti,et al.  The weight of time: gravitational force enhances discrimination of visual motion duration. , 2011, Journal of vision.

[32]  Charalambos Papaxanthis,et al.  Sensorimotor adaptation of point-to-point arm movements after spaceflight: the role of internal representation of gravity force in trajectory planning. , 2011, Journal of neurophysiology.