Abstract
Model simulations of the squirrel monkey vestibulo-ocular reflex (VOR) are presented for two motion paradigms: constant velocity eccentric rotation and roll tilt about a naso-occipital axis. The model represents the implementation of three hypotheses: the “internal model” hypothesis, the “gravito-inertial force (GIF) resolution” hypothesis, and the “compensatory VOR” hypothesis. The internal model hypothesis is based on the idea that the nervous system knows the dynamics of the sensory systems and implements this knowledge as an internal dynamic model. The GIF resolution hypothesis is based on the idea that the nervous system knows that gravity minus linear acceleration equals GIF and implements this knowledge by resolving the otolith measurement of GIF into central estimates of gravity and linear acceleration, such that the central estimate of gravity minus the central estimate of acceleration equals the otolith measurement of GIF. The compensatory VOR hypothesis is based on the idea that the VOR compensates for the central estimates of angular velocity and linear velocity, which sum in a near-linear manner. During constant velocity eccentric rotation, the model correctly predicts that: (1) the peak horizontal response is greater while “facing-motion” than with “back-to-motion”; (2) the axis of eye rotation shifts toward alignment with GIF; and (3) a continuous vertical response, slow phase downward, exists prior to deceleration. The model also correctly predicts that a torsional response during the roll rotation is the only velocity response observed during roll rotations about a nasooccipital axis. The success of this model in predicting the observed experimental responses suggests that the model captures the essence of the complex sensory interactions engendered by eccentric rotation and roll tilt.
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References
Borah J, Young L, Curry R (1988) Optimal estimator model for human spatial orientation. Ann N Y Acad Sci 545:51–73
Clark B, Graybiel A (1963) Contributing factors in the perception of the oculogravic illusion. Am J Psychol 76:18–27
Clark B, Graybiel A (1966) Factors contributing to the delay in the perception of the oculogravic illusion. Am J Psychol 79:377–388
Fernandez C, Goldberg J (1976) Physiology of peripheral neurons innervating the otolith organs of the squirrel monkey. I. Response to static tilts and to long-duration centrifugal force. J Neurophysiol 39:970–984
Galiana H, Outerbridge J (1984) A bilateral model for central neural pathways in the vestibulo-ocular reflex. J Neurophysiol 51:210–241
Glasauer S (1992) Interaction of semicircular canals and otoliths in the processing structure of the subjective zenith. Ann N Y Acad Sci 656:847–849
Goldberg J, Fernandez C (1971a) Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. I. Resting discharge and response to constant angular accelerations. J Neurophysiol 34:635–660
Goldberg J, Fernandez C (1971b) Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. II. Response to sinusoidal stimulation and dynamics of peripheral vestibular system. J Neurophysiol 34:661–675
Goldberg J, Fernandez C (1982) Eye movements and vestibular-nerve responses produced in the squirrel monkey by rotations about an Earth-horizontal axis. Exp Brain Res 46:393–402
Graybiel A, Brown R (1951) The delay in visual reorientation following exposure to a change in direction of resultant force on a human centrifuge. J Gen Psychol 45:143–150
Guitton D, Munoz D, Galiana H (1990) Gaze control in the cat: studies and modeling of the coupling between orienting eye and head movement in different behavioral tasks. J Neurophysiol 64(2):509–531
Held R (1961) Exposure history as a factor in maintaining stability of perception and coordination. J Nerv Ment Dis 132:26–32
Luenberger D (1971) An introduction to observers. IEEE Trans Autom Control 36(5):456–460
Merfeld D (1990) Spatial orientation in the squirrel monkey: an experimental and theoretical investigation. PhD thesis, MIT, Cambridge, Mass
Merfeld D, Young L (1995) The vestibulo-ocular reflex of the squirrel monkey during eccentric rotation and roll tilt. Exp Brain Res 106:111–122
Merfeld D, Young L, Paige G, Tomko D (1991) Spatial orientation of VOR to combined vestibular stimuli in squirrel monkeys. Acta Oto Laryngol Suppl (Stockh) 481:287–292
Merfeld D, Wearne S, Curthoys I, Halmagyi G (1992) Perceptual tilt responses in humans during eccentric rotation. Abstract presented at the Barany Society Meeting, Prague, Czech Republic, pp 73–74
Merfeld D, Young L, Paige G, Tomko D (1993a) Three dimensional eye movements of squirrel monkeys following post-rotatory tilt. J Vestib Res 3:123–139
Merfeld D, Young L, Oman C, Shelhamer M (1993b) A multi-dimensional model of the effect of gravity on the spatial orientation of the monkey. J Vestib Res 3:141–161
Oman C (1982) A heuristic model mathematical model for the dynamics of sensory conflict and motion sickness. Acta Oto Laryngol Suppl (Stockh) 392:1–44
Paige G (1989) The influence of target distance on eye movement responses during vertical linear motion. Exp Brain Res 77:585–593
Paige G, Tomko D (1991a) Eye movement responses to linear head motion in the squirrel monkey. I. Basic characteristics. J Neurophysiol 65(5): 1170–1182
Paige G, Tomko D (1991b) Eye movement responses to linear head motion in the squirrel monkey. II. Visual-vestibular interactions and kinematic considerations. J Neurophysiol 65(5):1183–1196
Raphan T, Matsuo V, Cohen B (1977) A velocity storage mechanism responsible for optokinetic nystagmus (OKN), optokinetic after-nystagmus (OKAN) and vestibular nystagmus. In: Baker R, Berthoz A (eds) Control of gaze by brain stem neurons. Developments in neuroscience. Elsevier North Holland, pp 37–47
Robinson D (1977) Vestibular and optokinetic symbiosis: an example of explaining by modelling. In: Baker R, Berthoz A (eds) Control of Gaze by brain-stem neurons. Developments in neuroscience. Elsevier North-Holland, pp 49–58
Robinson D (1989) Integrating with neurons. Ann Rev Neurosci 12:33–45
Robinson D, Gordon J, Gordon S (1986) A model of the smooth pursuit eye movement system. Biol Cybern 55:43–57
Rolfe J, Staples K (1977) Flight simulation. Cambridge University Press, Cambridge, UK
Sargent E, Paige G (1991) The primate vestibulo-ocular reflex during combined linear and angular head motion. Exp Brain Res 87:75–84
Schwarz C, Miles F (1991) Ocular responses to translation and their dependence on viewing distance. I. Motion of the observer. J Neurophysiol 66(3):851–864
Schwarz C, Busettini C, Miles F (1989) Ocular responses to linear motion are inversely proportional to viewing distance. Science 245:1394–1396
Shelhamer MJ, Merfeld DM, Mendoza J-C (1994) Vergence can be controlled by audio feedback, and induces downward ocular deviation. Exp Brain Res 101:169–172
Shelhamer MJ, Merfeld DM, Mendoza J-C (1995) Effect of vergence on the gain of the linear vestibulo-ocular reflex. Acta Otolaryngol Suppl (Stockh) (in press)
Tomko D, Paige G (1992) Linear vestibuloocular reflex during motion along axes between nasooccipital and interaural. Ann N Y Acad Sci 656:233–241
Tweed D, Vilis T (1987) Implications of rotational kinematics for the oculomotor system in three dimensions. J Neurophysiol 58:832–849
Yasui S, Young L (1975) Perceived visual motion as effective stimulus to pursuit eye movement system. Science 190:906–908
Young, L, and Oman, D (1970) Modeling adaptation in human semicircular canal response to rotation. Trans N Y Acad Sci 32(4):489–494
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This research was supported by NASA contracts NASW-3651, NAG2-445, NAS9-16523, the NASA Graduate Student Researchers Program, and the GE Forgivable Loan Fund. Preliminary findings were presented in a PhD thesis (Merfeld 1990) and at the Sixteenth Barany Society Meeting in Tokyo in 1990 (Merfeld et al. 1991).
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Merfeld, D.M. Modeling the vestibulo-ocular reflex of the squirrel monkey during eccentric rotation and roll tilt. Exp Brain Res 106, 123–134 (1995). https://doi.org/10.1007/BF00241362
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DOI: https://doi.org/10.1007/BF00241362