Representation of Visual Gravitational Motion in the Human Vestibular Cortex

How do we perceive the visual motion of objects that are accelerated by gravity? We propose that, because vision is poorly sensitive to accelerations, an internal model that calculates the effects of gravity is derived from graviceptive information, is stored in the vestibular cortex, and is activated by visual motion that appears to be coherent with natural gravity. The acceleration of visual targets was manipulated while brain activity was measured using functional magnetic resonance imaging. In agreement with the internal model hypothesis, we found that the vestibular network was selectively engaged when acceleration was consistent with natural gravity. These findings demonstrate that predictive mechanisms of physical laws of motion are represented in the human brain.

[1]  J T Todd,et al.  Visual information about moving objects. , 1981, Journal of experimental psychology. Human perception and performance.

[2]  David N. Lee,et al.  Plummeting gannets: a paradigm of ecological optics , 1981, Nature.

[3]  R. Shepard.  Ecological constraints on internal representation: resonant kinematics of perceiving, imagining, thinking, and dreaming. , 1984, Psychological review.

[4]  F. Lacquaniti,et al.  The role of preparation in tuning anticipatory and reflex responses during catching , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  O J Grüsser,et al.  Localization and responses of neurones in the parieto‐insular vestibular cortex of awake monkeys (Macaca fascicularis). , 1990, The Journal of physiology.

[6]  Martin S Banks,et al.  Gravity as a Monocular Cue for Perception of Absolute Distance and/or Absolute Size , 1992 .

[7]  E S Spelke,et al.  Infants' sensitivity to effects of gravity on visible object motion. , 1992, Journal of experimental psychology. Human perception and performance.

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

[9]  A. Berthoz.  Multisensory control of movement , 1993 .

[10]  M Dieterich,et al.  Vestibular cortex lesions affect the perception of verticality , 1994, Annals of neurology.

[11]  M K Kaiser,et al.  How baseball outfielders determine where to run to catch fly balls. , 1995, Science.

[12]  Daeyeol Lee,et al.  Manual interception of moving targets I. Performance and movement initiation , 1997, Experimental Brain Research.

[13]  Guldin Wo,et al.  Is there a vestibular cortex , 1998 .

[14]  D M Merfeld,et al.  Humans use internal models to estimate gravity and linear acceleration , 1999, Nature.

[15]  Maninder K. Kahlon,et al.  Visual Motion Analysis for Pursuit Eye Movements in Area MT of Macaque Monkeys , 1999, The Journal of Neuroscience.

[16]  Karl J. Friston,et al.  A direct quantitative relationship between the functional properties of human and macaque V5 , 2000, Nature Neuroscience.

[17]  Hiroshi Imamizu,et al.  Human cerebellar activity reflecting an acquired internal model of a new tool , 2000, Nature.

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

[19]  T. Brandt,et al.  Multisensory cortical signal increases and decreases during vestibular galvanic stimulation (fMRI). , 2001, Journal of neurophysiology.

[20]  O. Blanke,et al.  Neuropsychology: Stimulating illusory own-body perceptions , 2002, Nature.

[21]  Geoffrey P Bingham,et al.  Causation, causal perception, and conservation laws , 2002, Perception & psychophysics.

[22]  V. Smetácek.  Balance: Mind-grasping gravity , 2002, Nature.

[23]  Christian Darlot,et al.  Using sensory weighting to model the influence of canal, otolith and visual cues on spatial orientation and eye movements , 2002, Biological Cybernetics.

[24]  Anne-Marie Brouwer,et al.  Perception of acceleration with short presentation times: Can acceleration be used in interception? , 2001, Perception & psychophysics.

[25]  Guy A. Orban,et al.  Similarities and differences in motion processing between the human and macaque brain: evidence from fMRI , 2003, Neuropsychologia.

[26]  F. Lacquaniti,et al.  Internal models of target motion: expected dynamics overrides measured kinematics in timing manual interceptions. , 2004, Journal of neurophysiology.

[27]  R. Peterka,et al.  Origin of orientation-dependent asymmetries in vestibulo-ocular reflexes evoked by caloric stimulation. , 2004, Journal of neurophysiology.

[28]  Dora E. Angelaki,et al.  Neurons compute internal models of the physical laws of motion , 2004, Nature.

[29]  A. Georgopoulos,et al.  Neural responses during interception of real and apparent circularly moving stimuli in motor cortex and area 7a. , 2004, Cerebral cortex.

[30]  Richard S. J. Frackowiak,et al.  Identification of the central vestibular projections in man: a positron emission tomography activation study , 2004, Experimental Brain Research.