Vestibular perception and action employ qualitatively different mechanisms. I. Frequency response of VOR and perceptual responses during Translation and Tilt

Journal of Neurophysiology

Volumn 94, Issue 1, 2005, Pages 186-198

  Merfeld, Daniel M ^a,b   Park, Sukyung ^a,b   Gianna Poulin, Claire ^c   Black, F Owen ^c   Wood, Scott ^c  

^a MASSACHUSETTS EYE AND EAR INFIRMARY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c LEGACY RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BODY POSITION; CONTROLLED STUDY; EYE MOVEMENT; FEMALE; FREQUENCY MODULATION; HUMAN; HUMAN EXPERIMENT; MALE; MOVEMENT PERCEPTION; NERVE CELL NETWORK; NORMAL HUMAN; OTOLITH; PREDICTION; PRIORITY JOURNAL; PROCESS MODEL; QUALITATIVE ANALYSIS; SENSORY NERVE; TILT TABLE TEST; VESTIBULAR SYSTEM; VESTIBULOOCULAR REFLEX;

NASA DISCIPLINE NEUROSCIENCE; NON-NASA CENTER;

ADULT; EYE MOVEMENTS; FEMALE; GRAVITATION; GRAVITY PERCEPTION; HEAD MOVEMENTS; HUMANS; MALE; MIDDLE AGED; MODELS, BIOLOGICAL; MOTION; MOTION PERCEPTION; REFLEX, VESTIBULO-OCULAR; ROTATION; VESTIBULAR FUNCTION TESTS;

EID: 21544443133     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00904.2004     Document Type: Article

References (100)

1. Angelaki D. Three dimensional organization of otolith-ocular reflexes in rhesus monkeys. III. Responses to translation. J Neurophysiol 80: 680-695, 1998.
2. Angelaki D and Hess B. Inertial representation of angular motion in the vestibular system of rhesus monkeys. I. Vestibuloocular reflex. J Neurophysiol 71: 1222-1249, 1994.
3. Angelaki D, McHenry M, Dickman JD, Newlands S, and Hess B. Computation of inertial motion: neural strategies to resolve ambiguous otolith information. J Neurosci 19: 316-327, 1999.
4. Angelaki DE, McHenry MQ, and Hess BJ. Primate translational vestibuloocular reflexes. I. High-frequency dynamics and three-dimensional properties during lateral motion. J Neurophysiol 83: 1637-1647, 2000.
5. Angelaki DE, Shaikh AG, Green AM, and Dickman JD. Neurons compute internal models of the physical laws of motion. Nature 430: 560-564, 2004.
6. Angelaki DE, Wei M, and Merfeld DM. Vestibular discrimination of gravity and translational acceleration. Ann NY Acad Sci 942: 114-127, 2001.
7. Arrott AP, Young LR, and Merfeld DM. Perception of linear acceleration in weightlessness. Aviat Space Environ Med 61: 319-326, 1990.
8. Asch S and Witkin H. Studies in space orientation. I. Perception of the upright with displaced visual fields. J Exp Psychol 38: 325-337, 1948a.
9. Asch S and Witkin H. Studies in space orientation. II. Perception of the upright with displaced visual fields and with body tilted. J Exp Psychol 38: 455-477, 1948b.
10. Baloh R, Beykirch K, Honrubia V, and Yee R. Eye movements induced by linear acceleration on a parallel swing. J Neurophysiol 60: 2000-2013, 1988.
11. Becker W and Klein HM. Accuracy of saccadic eye movements and maintenance of eccentric eye positions in the dark. Vision Res 13: 1021-1034, 1973.
12. Benson AJ, Spencer MB, and Stott JR. Thresholds for the detection of the direction of whole-body, linear movement in the horizontal plane. Aviat Space Environ Med 57: 1088-1096, 1986.
13. Berthoz A, Israel I, Georges-Francois P, Grasso R, and Tsuzuku T. Spatial memory of body linear displacement: what is being stored? Science 269: 95-98, 1995.
14. Berthoz A, Israel I, Vieville T, and Zee D. Linear head displacement measured by the otoliths can be reproduced through the saccadic system. Neurosci Lett 82: 285-290, 1987.
15. Berthoz A, Israel I, Vitte E, and Zee D. Linear displacement can be derived from otolithic information and stored on spatial maps controlling the saccadic system. Adv Otorhinolaryngol 41: 76-81, 1988.
16. Boyle R, Belton T, and McCrea R. Responses of identified vestibulospinal neurons to voluntary and reflex eye and head movements in the alert squirrel monkey. Ann NY Acad Sci 781: 244-263, 1996.
17. Cannon SC and Robinson DA. An improved neural-network model for the neural integrator of the oculomotor system: more realistic neuron behavior. Biol Cybern 53: 93-108, 1985.
18. Cannon SC, Robinson DA, and Shamma S. A proposed neural network for the integrator of the oculomotor system. Biol Cybern 49: 127-136, 1983.
19. Carpenter-Smith TR, Futamura RG, and Parker DE. Inertial acceleration as a measure of linear vection: an alternative to magnitude estimation. Percept Psychophys 57: 35-42, 1995.
20. Clark B and Graybiel A. Contributing factors in the perception of the oculogravic illusion. Am J Psychol 76: 18-27, 1963.
21. Clark B and Graybiel A. Factors contributing to the delay in the perception of the oculogravic illusion. Am J Pyschol 79: 377-388, 1966.
22. Dichgans J, Diener HC, and Brandt T. Optokinetic-graviceptive interaction in different head positions. Acta Otolaryngol 78: 391-398, 1974.
23. Dichgans J, Held R, Young LR, and Brandt T. Moving visual scenes influence the apparent direction of gravity. Science 178: 1217-1219, 1972.
24. Dickman JD and Angelaki DE. Vestibular convergence patterns in vestibular nuclei neurons of alert primates. J Neurophysiol 88: 3518-3533, 2002.
25. Droulez J and Cornilleau-Peres V. Application of the coherence scheme to the multisensory fusion problem. In: Multisensory Control of Movement, edited by Berthoz A. Oxford, UK: Oxford Univ. Press, 1993, p. 485-501.
26. Droulez J and Darlot C. The geometric and dynamic implications of the coherence constraints in three-dimensional sensorimotor interactions. In: Attention and Performance XIII, edited by Jeannerod M. New York: Erlbaum, 1989, p. 495-526.
27. Fetter M, Tweed D, Hermann W, Wohland-Braun B, and Koenig E. The influence of head position and head reorientation on the axis of eye rotation and the vestibular time constant during postrotatory nystagmus. Exp Brain Res 91: 121-128, 1992.
28. Gianna C, Heimbrand S, and Gresty M. Thresholds for detection of motion direction during passive lateral whole-body acceleration in normal subjects and patients with bilateral loss of labyrinthine function. Brain Res Bull 40: 443-447; discussion 448-449, 1996.
29. Glasauer S. Interaction of semicircular canals and otoliths in the processing structure of the subjective zenith. Ann NY Acad Sci 656: 847-849, 1992.
30. Glasauer S. Linear acceleration perception: frequency dependence of the hilltop illusion. Acta Otolaryngol Suppl 520: 37-40, 1995.
31. Glasauer S and Merfeld D. Modelling three dimensional vestibular responses during complex motion stimulation. In: Three-Dimensional Kinematics of Eye, Head, and Limb Movements, edited by Fetter M, Misslisch H, Tweed D, and Halswanter T. Amsterdam: Harwood Academic Publishers, 1997, p. 389-400.
32. Graybiel A and Brown R. 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, 1951.
33. Green AM and Angelaki DE. Resolution of sensory ambiguities for gaze stabilization requires a second neural integrator. J Neurosci 23: 9265-9275, 2003.
34. Haslwanter T and Moore S. A theoretical analysis of three dimensional eye position measurement using polar cross correlation. IEEE Trans Biomed Eng 42: 1053-1061, 1995.
35. Henn V, Young L, and Finley C. Vestibular nucleus units in alert monkeys are also influenced by moving visual fields. Brain Res 71: 144-149, 1974.
36. Hess B, Van Opstal A, Staumann D, Hepp K, and Henn V. Calibration of three-dimensional eye position using search coil signals in the rhesus monkey. Vision Res 32: 1647-1654, 1992.
37. Howard IP and Childerson L. The contribution of motion, the visual frame, and visual polarity to sensations of body tilt. Perception 23: 753-762, 1994.
38. Howard I and Templeton W. Orientation to gravity. In: Human Spatial Orientation. New York: Wiley, 1966, p. 175-212.
39. Huang JK and Young LR. Influence of visual and motion cues on manual lateral stabilization. Aviat Space Environ Med 58: 1197-1204, 1987.
40. Israel I and Berthoz A. Contribution of the otoliths to the calculation of linear displacement. J Neurophysiol 62: 247-263, 1989.
41. Israel I, Chapuis N, Glasauer S, Charade O, and Berthoz A. Estimation of passive horizontal linear whole-body displacement in humans. J Neurophysiol 70: 1270-1273, 1993.
42. Israel I, Grasso R, Georges-Francois P, Tsuzuku T, and Berthoz A. Spatial memory and path integration studied by self-driven passive linear displacement. I. Basic properties. J Neurophysiol 77: 3180-3192, 1997.
43. Jaschinski-Kruza W. Effects of stimulus distance on measurements of dark convergence. Ophthal Physiol Opt 10: 243-251, 1990.
44. Johnson RA and Wichern DW. Applied Multivariate Statistical Analysis. Englewood Cliffs, NJ: Prentice-Hall, 1982.
45. Lichtenberg BK, Young LR, and Arrott AP. Human ocular counterrolling induced by varying linear accelerations. Exp Brain Res 48: 127-136, 1982.
46. Mayne R. A systems concept of the vestibular organs. In: Handbook of Sensory Physiology. Vestibular System. Psychophysics, Applied Aspects and General Interpretations, edited by Kornhuber H. Berlin: Springer-Verlag, 1974, vol. VI, part 2, p. 493-580.
47. McCabe B. Nystagmus response of the otolith organs. Laryngoscope 74: 372-381, 1964.
48. McCrea RA, Chen-Huang C, Belton T, and Gdowski GT. Behavior contingent processing of vestibular sensory signals in the vestibular nuclei. Ann NY Acad Sci 781: 292-303, 1996.
49. McCrea RA, Gdowski GT, Boyle R, and Belton T. Firing behavior of vestibular neurons during active and passive head movements: vestibulospinal and other non-eye-movement related neurons. J Neurophysiol 82: 416-428, 1999.
50. Melvill Jones G and Young LR. Subjective detection of vertical acceleration: a velocity dependent response? Acta Otolaryngol 85: 45-53, 1978.
51. Merfeld DM. Modeling human vestibular responses during eccentric rotation and off vertical axis rotation. Acta Oto-Laryngol Suppl 520: 354-359, 1995a.
52. Merfeld DM. Modeling the vestibulo-ocular reflex of the squirrel monkey during eccentric rotation and roll tilt. Exp Res 106: 123-134, 1995b.
53. Merfeld DM. Spatial Orientation in the Squirrel Monkey: An Experimental and Theoretical Investigation (PhD thesis). Cambridge, MA: MIT, 1990.
54. Merfeld DM, Christie JRI, and Young LR. Perceptual and eye movement responses elicited by linear acceleration following spaceflight. Aviat Space Environ Med 65: 1015-1024, 1994.
55. Merfeld D, Park S, Gianna-Poulin C, Black FO, and Wood S. Vestibular perception and action employ qualitatively different mechanisms. II. VOR and perceptual responses during combined Tilt&Translation. J Neurophysiol 94: 199-205, 2005.
56. Merfeld D, Polutchko K, and Schultz K. Perceptual responses to linear acceleration after spaceflight: human neurovestibular studies on SLS-2. J Appl Physiol 81: 58-68, 1996a.
57. Merfeld D, Teiwes W, Clarke A, Scherer H, and Young L. The dynamic contributions of the otolith organs to human ocular torsion. Exp Brain Res 110: 315-321, 1996b.
58. Merfeld D and Young L. Three dimensional eye velocity measurement following postrotational tilts in monkeys. Ann NY Acad Sci 656: 783-794, 1992.
59. Merfeld DM and Young LR. The vestibulo-ocular reflex of the squirrel monkey during eccentric rotation and roll tilt. Exp Brain Res 106: 111-122, 1995.
60. Merfeld DM, Young L, Oman C, and Shelhamer M. A multi-dimensional model of the effect of gravity on the spatial orientation of the monkey. J Vestib Res 3: 141-161, 1993a.
61. Merfeld DM, Young L, Paige G, and Tomko D. Spatial orientation of VOR to combined vestibular stimuli in squirrel monkeys. Acta Oto-Laryngol Suppl 481: 287-292, 1991.
62. Merfeld DM, Young L, Paige G, and Tomko D. Three dimensional eye movements of squirrel monkeys following post-rotatory tilt. J Vestib Res 3: 123-139, 1993b.
63. Merfeld D and Zupan L. Influence of rotational cues on the neural processing of gravito-inertial force. In: Levels of Perception, edited by Harris L and Jenkin L. New York: Springer-Verlag, 2003, p. 341-373.
64. Merfeld DM and Zupan LH. Neural processing of gravitoinertial cues in humans. III. Modeling tilt and translation responses. J Neurophysiol 87: 819-833, 2002.
65. Merfeld DM, Zupan LH, and Gifford CA. Neural processing of gravitoinertial cues in humans. II. Influence of the semicircular canals during eccentric rotation. J Neurophysiol 85: 1648-1660, 2001.
66. Merfeld D, Zupan L, and Peterka R. Humans use internal models to estimate gravity and linear acceleration. Nature 398: 615-618, 1999.
67. Mergner T, Schweigart G, Botti F, and Lehmann A. Eye movements evoked by proprioceptive stimulation along the body axis in humans. Exp Brain Res 120: 450-460, 1998.
68. Mittelstaedt H. Somatic graviception. Biol Psychol 42: 53-74, 1996.
69. Moore S, Haslwanter T, Curthoys I, and Smith S. A geometric basis for measurement of three dimensional eye position using image processing. Vision Res 36: 445-459, 1996.
70. Niven J, Hixson W, and Correia M. Elicitation of horizontal nystagmus by periodic linear acceleration. Acta Otolaryngol 62: 429-441, 1966.
71. Paige G. The influence of target distance on eye movement responses during vertical linear motion. Exp Brain Res 77: 585-593, 1989.
72. Paige GD and Seidman SH. Characteristics of the VOR in response to linear acceleration. Ann NY Acad Sci 871: 123-135, 1999.
73. Paige GD and Seidman SH. Tilt-translation ambiguity in the linear vestibuloocular reflex (LVOR). Society for Neuroscience Annual Meeting, San Diego, 2001.
74. Paige GD, Telford L, Seidman SH, and Barnes GR. Human vestibuloocular reflex and its interactions with vision and fixation distance during linear and angular head movement. J Neurophysiol 80: 2391-2404, 1998.
75. Paige G and Tomko D. Eye movement responses to linear head motion in the squirrel monkey. I. Basic characteristics. J Neurophysiol 65: 1170-1182, 1991.
76. Peterka RJ, Gianna-Poulin CC, Zupan LH, and Merfeld DM. Origin of orientation-dependent asymmetries in vestibulo-ocular reflexes evoked by caloric stimulation. J Neurophysiol 92: 2333-2345, 2004.
77. Peterson BW and Chen-Huang C. Otolith neurons distinguish between translation and tilts. J Vestib Res 11: 255, 2002.
78. Raphan T, Matsuo V, and Cohen B. Velocity storage in the vestibulo-ocular reflex arc (VOR). Exp Brain Res 35: 229-248, 1979.
79. Raphan T, Matsuo V, and Cohen B. A velocity storage mechanism responsible for optokinetic nystagmus (OKN), optokinetic after-nystagmus (OKAN) and vestibular nystagmus. In: Control of Gaze by Brain Stem Neurons, Developments in Neuroscience, edited by Baker R and Berthoz A. Amsterdam: Elsevier/North Holland Biomedical Press, 1977, p. 37-47.
80. Robinson D. Vestibular and optokinetic symbiosis: an example of explaining by modelling. In: Control of Gaze by Brain Stem Neurons, Developments in Neuroscience, edited by Baker R and Berthoz A. Amsterdam: Elsevier/North-Holland Biomedical Press, 1977, p. 49-58.
81. Roy JE and Cullen KE. Selective processing of vestibular reafference during self-generated head motion. J Neurosci 21: 2131-2142, 2001.
82. Schor CM, Alexander J, Cormack L, and Stevenson S. Negative feedback control model of proximal convergence and accommodation. Ophthal Physiol Opt 12: 307-318, 1992.
83. Schwarz C, Busettini C, and Miles F. Ocular responses to linear motion are inversely proportional to viewing distance. Science 245: 1394-1396, 1989.
84. Schwarz C and Miles F. Ocular responses to translation and their dependence on viewing distance. I. Motion of the Observer. J Neurophysiol 66: 851-864, 1991.
85. Seidman SH and Paige GD. Perception and eye movement during low-frequency centripetal acceleration. Ann N Y Acad Sci 781: 693-695, 1996.
86. Seidman SH, Telford L, and Paige GD. Vertical, horizontal, and torsional eye movement responses to head roll in the squirrel monkey. Exp Brain Res 104: 218-226, 1995.
87. Seidman S, Telford L, and Paige G. Tilt perception during dynamic linear acceleration. Exp Brain Res 119: 307-314, 1998.
88. Stockwell C and Guedry F. The effect of semicircular canal stimulation during tilting on the subsequent perception of the visual vertical. Acta Oto-Laryngol 70: 170-175, 1970.
89. Telford L, Seidman S, and Paige G. Dynamics of squirrel monkey linear vestibuloocular reflex and interactions with fixation distance. J Neurophysiol 78: 1775-1790, 1997.
90. Tweed D, Cadera W, and Vilis T. Computing three-dimensional eye position quaternions and eye velocity from search coil signals. Vision Res 30: 97-110, 1990.
91. Tweed D, Sievering D, Misslisch H, Fetter M, Zee D, and Koenig E. Rotational kinematics of the human vestibuloocular reflex. I. Gain matrices. J Neurophysiol 72: 2467-2479, 1994.
92. von Holst E, and Grisebach E. Einfluβ des Bogengangssystems auf die "subjektive" Lotrechte beim Menschen. Naturwissenschaften 38: 67-68, 1951.
93. Wearne S, Raphan T, and Cohen B. Effects of tilt of the gravito-inertial acceleration vector on the angular vestibuloocular reflex during centrifugation. J Neurophysiol 81: 2175-2190, 1999.
94. Wick B and Bedell HE. Magnitude and velocity of proximal vergence. Invest Ophthalmol Vis Sci 30: 755-760, 1989.
95. Wood SJ. Human otolith-ocular reflexes during off-vertical axis rotation: effect of frequency on tilt-translation ambiguity and motion sickness. Neurosci Lett 323: 41-44, 2002.
96. Young L. Perception of the body in space: mechanisms. In: Handbook of Physiology. The Nervous System. Motor Control, edited by Darian-Smith I. Bethesda, MD: Am. Physiol. Soc., 1984, sect. 1, vol. I, p. 1023-1066.
97. Zhou W, Tang B, and King WM. Vestibular neurons encode linear translation and head tilt with respect to gravity. Society for Neuroscience Annual Meeting, New Orleans, 2000.
98. Zupan LH and Merfeld DM. Neural processing of gravito-inertial cues in humans. IV. Influence of visual rotational cues during roll optokinetic stimuli. J Neurophysiol 89: 390-400, 2003.
99. Zupan L, Merfeld D, and Darlot C. Using sensory weighting to model the influence of canal, otolith and visual cues on spatial orientation and eye movements. Biol Cybern 86: 209-230, 2002.
100. Zupan L, Peterka R, and Merfeld D. Neural processing of gravito-inertial cues in humans. I. Influence of the semicircular canals following post-rotatory tilt. J Neurophysiol 84: 2001-2015, 2000.