An integrative neural network for detecting inertial motion and head orientation

Journal of Neurophysiology

Volumn 92, Issue 2, 2004, Pages 905-925

  Green, Andrea M ^a   Angelaki, Dora E ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACCELERATION; ARTICLE; BEHAVIOR; GRAVITY; HEAD MOVEMENT; MOVEMENT PERCEPTION; NERVE CELL NETWORK; OTOLITH; PRIORITY JOURNAL; SEMICIRCULAR CANAL; SPATIAL ORIENTATION; VESTIBULAR SYSTEM; VESTIBULOOCULAR REFLEX;

NASA DISCIPLINE NEUROSCIENCE; NON-NASA CENTER;

ACCELERATION; ANIMALS; BEHAVIOR, ANIMAL; COMPUTER SIMULATION; DISCRIMINATION (PSYCHOLOGY); HEAD; HUMANS; MATHEMATICS; MODELS, NEUROLOGICAL; MOTION PERCEPTION; NEURAL NETWORKS (COMPUTER); NONLINEAR DYNAMICS; ORIENTATION; OTOLITHIC MEMBRANE; SEMICIRCULAR CANALS; SPACE PERCEPTION;

EID: 3142711489     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.01234.2003     Document Type: Article

References (103)

1. Angelaki DE. Two-dimensional coding of linear acceleration and the angular velocity sensitivity of the otolith system. Biol Cybern 67: 511-521, 1992a.
2. Angelaki DE. Detection of rotating gravity signals. Biol Cybern 67: 523-533, 1992b.
3. Angelaki DE. Three-dimensional organization of otolith-ocular reflexes in rhesus monkeys. III. Responses to translation. J Neurophysiol 80: 680-695, 1998.
4. Angelaki DE, Bush GA, and Perachio AA. Two-dimensional spatiotemporal coding of linear acceleration in vestibular nuclei neurons. J Neurosci 13: 1403-1417, 1993.
5. Angelaki DE and Dickman JD. Spatiotemporal processing of linear acceleration: primary afferent and central vestibular neuron responses. J Neurophysiol 84: 2113-2132, 2000.
6. Angelaki DE, Green AM, and Dickman JD. Differential sensorimotor processing of vestibulo-ocular signals during rotation and translation. J Neurosci 21: 3968-3985, 2001a.
7. Angelaki DE and Hess BJM. Inertial representation of angular motion in the vestibular system of rhesus monkeys. I. Vestibuloocular reflex. J Neurophysiol 71: 1222-1249, 1994.
8. Angelaki DE and Hess BJM. Inertial representation of angular motion in the vestibular system of rhesus monkeys. II. Otolith-controlled transformation that depends on an intact cerebellar nodulus. J Neurophysiol 73: 1729-1751, 1995.
9. Angelaki DE and Hess BJM. Three-dimensional organization of otolithocular reflexes in rhesus monkeys. II. Inertial detection of angular velocity. J Neurophysiol 75: 2425-2440, 1996.
10. Angelaki DE, Hess BJM, and Suzuki J-I. Differential processing of semicircular canal signals in the vestibulo-ocular reflex. J Neurosci 15: 7201-7216, 1995.
11. Angelaki DE, McHenry MQ, Dickman JD, Newlands SD, and Hess BJM. Computation of inertial motion: neural strategies to resolve ambiguous otolith information. J Neurosci 19: 316-327, 1999.
12. Angelaki DE, Shaikh A, and Dickman JD. Responses of vestibular nuclei neurons during combinations of tilt and translation. Program No. 593.8 2003 Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience, 2003. Online.
13. Angelaki DE, Wei M, and Merfeld DM. Vestibular discrimination of gravity and translational acceleration. Ann NY Acad Sci 942: 114-127, 2001b.
14. Baker J, Goldberg J, Hermann G, and Peterson B. Optimal response planes and canal convergence in secondary neurons in vestibular nuclei of alert cats. Brain Res 294: 133-137, 1984a.
15. Baker J, Goldberg J, Hermann G, and Peterson B. Spatial and temporal response properties of secondary neurons that receive convergent input in vestibular nuclei of alert cats. Brain Res 294: 138-143, 1984b.
16. Bos JE and Bles W. Theoretical considerations on canal-otolith interaction and an observer model. Biol Cybern 86: 191-207, 2002.
17. Brettler SC and Baker JF. Directional sensitivity of anterior, posterior, and horizontal canal vestibulo-ocular neurons in the cat. Exp Brain Res 140: 432-442, 2001.
18. Buettner UW, Büttner U, and Henn V. Transfer characteristics of neurons in vestibular nuclei of the alert monkey. J Neurophysiol 41: 1614-1628, 1978.
19. Busettini C, Miles FA, Schwarz U, and Carl JR. Human ocular responses to translation of the observer and of the scene: dependence on viewing distance. Exp Brain Res 100: 484-494, 1994.
20. Bush GA, Perachio AA, and Angelaki DE. Encoding of head acceleration in vestibular neurons. I. Spatiotemporal response properties to linear acceleration. J Neurophysiol 69: 2039-2055, 1993.
21. Cannon SC and Robinson DA. Loss of the neural integrator of the oculomotor system from brain stem lesions in monkey. J Neurophysiol 57: 1383-1409, 1987.
22. Chen-Huang C and Peterson BW. Three-dimensional rotational and translational responses of vestibular neurons in squirrel monkeys. Program No. 168.11 2002 Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience, 2002. Online.
23. Correia MJ and Money KE. The effect of blockage of all six semicircular canal ducts on nystagmus produced by dynamic linear acceleration in the cat. Acta Otolaryngol 69: 7-16, 1970.
24. Crawford JD and Vilis T. Axes of eye rotation and Listing's law during rotations of the head. J Neurophysiol 65: 407-423, 1991.
25. Dai MJ, Raphan T, and Cohen B. Spatial orientation of the vestibular system: dependence of optokinetic after-nystagmus on gravity. J Neurophysiol 66: 1422-1439, 1991.
26. Dickman JD and Angelaki DE. Vestibular convergence patterns in vestibular nuclei neurons of alert primates. J Neurophysiol 88: 3518-3533, 2002.
27. Dickman JD and Angelaki DE. Dynamics of vestibular neurons during rotational motion in alert rhesus monkeys. Exp Brain Res (Epub ahead of print), 2003
28. Einstein A. Uber das Relativitätsprinzip und die aus demselben gezogenen Folgerungen. Jahrb Radioakt 4: 411-462, 1908.
29. Endo K, Thomson DB, Wilson VJ, Yamaguchi T, and Yates BJ. Vertical vestibular input to and projections from the caudal parts of the vestibular nuclei of the decerebrate cat. J Neurophysiol 74: 428-436, 1995.
30. Fernandez C and Goldberg JM. 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, 1971.
31. Fernandez C and Goldberg JM. Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. I. Response to static tilts and to long-duration centrifugal force. J Neurophysiol 39: 970-984, 1976a.
32. Fernandez C and Goldberg JM. Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. III. Response dynamics. J Neurophysiol 39: 996-1008, 1976b.
33. Fukushima K, Perlmutter SI, Baker JF, and Peterson BW. Spatial properties of second-order vestibulo-ocular relay neurons in the alert cat. Exp Brain Res 81: 462-478, 1990.
34. Galiana HL and Outerbridge JS. A bilateral model for central neural pathways in the vestibuloocular reflex. J Neurophysiol 51: 210-241, 1984.
35. Glasauer S and Merfeld DM. Modelling three-dimensional vestibular responses during complex motion stimulation. In: Three-Dimensional Kinematics of Eye, Head and Limb Movements, edited by Fetter M, Haslwanter T, Misslisch H, and Tweed D. Amsterdam: Harwood Academic, 1997, p. 387-398.
36. Goldstein H. Classical Mechanics. Reading, MA: Addison-Wesley, 1980.
37. Graf W, Baker J, and Peterson BW. Sensorimotor transformation in the cat's vestibuloocular reflex system. I. Neuronal signals coding spatial coordination of compensatory eye movements. J Neurophysiol 70: 2425-2441, 1993.
38. Green AM. Visual-Vestibulaar Interaction in a Bilateral Model of the Rotational and Translational Vestibulo-Ocular Reflexes: An Investigation of Viewing-Context-Dependent Reflex Performance (PhD thesis). Montreal, Canada: McGill University, 2000.
39. Green AM and Angelaki DE. A model to explore the relationship between tilt/translation discrimination and velocity storage. Vestibular Influences on Movement satellite of the 22nd Meeting of the Barany Society, Orcas Island, Sep. 22-26, 2002.
40. Green AM and Angelaki DE. Resolution of sensory ambiguities for gaze stabilization requires a second neural integrator. J Neurosci 23: 9265-9275, 2003.
41. Green AM, Dickman JD, and Angelaki DE. Investigation of the relationship between tilt/translation discrimination and velocity storage. Program No. 565.8. 2002 Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience, 2002. Online.
42. Green AM and Galiana HL. Hypothesis for shared central processing of canal and otolith signals. J Neurophysiol 80: 2222-2228, 1998.
43. Guedry FE. Psychophysics of vestibular sensation. In: Handbook of Sensory Physiology: The Vestibular System, Pt 2, Psychophysics, Applied Aspects and General Interpretations, edited by Guedry FE Jr. Berlin: Springer-Verlag, 1974.
44. Hain TC. A model of the nystagmus induced by off vertical axis rotation. Biol Cybern 54: 337-350, 1986.
45. Harris LR. Vestibular and optokinetic eye movements evoked in the cat by rotation about a tilted axis. Exp Brain Res 66: 522-532, 1987.
46. Haslwanter T, Straumann D, Hess BJM, and Henn V. Static roll and pitch in the monkey: shift and rotation of Listing's plane. Vision Res 32: 1341-1348, 1992.
47. Hess BJ and Angelaki DE. Inertial vestibular coding of motion: concepts and evidence. Clin Opin Neurobiol 7: 860-866, 1997.
48. Iwamoto Y, Perlmutter SI, Baker JF, and Peterson BW. Spatial coordination by descending vestibular signals, II. Response properties of medial and lateral vestibulospinal tract neurons in alert and decerebrate cats. Exp Brain Res 108: 85-100, 1996,
49. Kasper J, Schor RH, and Wilson VJ. Response of vestibular neurons to head rotations in vertical planes. I. Response to vestibular stimulation. J Neurophysiol 60: 1753-1764, 1988.
50. Katz E, Vianney de Jong JM, Buettner-Ennever JA, and Cohen B. Effects of midline medullary lesions on velocity storage and the vestibulo-ocular reflex. Exp Brain Res 87: 505-520, 1991.
51. Kushiro K, Dai M, Kunin M, Yakushin SB, Cohen B, and Raphan T. Compensatory and orienting eye movements induced by off-vertical axis rotation (OVAR) in monkeys. J Neurophysiol 88: 2445-2462, 2002.
52. Mayne RA. A systems concept of the vestibular organs. In: Handbook of Sensory Physiology: The Vestibular System, edited by Kornhuber HH. New York: Springer-Verlag, 1974, p. 493-580.
53. Merfeld DM. Modeling the vestibulo-ocular reflex of the squirrel monkey during eccentric rotation and roll tilt. Exp Brain Res 106: 123-134, 1995.
54. Merfeld DM, Park S, Gianna-Poulin C, Black F, and Wood S. Neural strategies to resolve ambiguous otolith cues: influence of rotational cues on human perception of tilt and translation. Program No. 268.18. 2003 Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience, 2003. Online.
55. 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.
56. Merfeld DM, Young LR, Oman CM, and Shelhamer MJ. A multidimensional model of the effect of gravity on the spatial orientation of the monkey. J Vest Res 3: 141-161, 1993b.
57. Merfeld DM, Young LR, Paige GD, and Tomko DL. Three dimensional eye movements of squirrel monkeys following postrotatory tilt. J Vest Res 3: 123-139, 1993a.
58. Merfeld DM and Zupan LH. Neural processing of gravitoinertial cues in humans. III. Modeling tilt and translation responses. J Neurophysiol 87: 819-833, 2002.
59. Merfeld DM, Zupan LH, and Peterka RJ. Humans use internal models to estimate gravity and linear acceleration. Nature 398: 615-618, 1999.
60. Mergner T and Glasauer S. A simple model of vestibular canal-otolith signal fusion. Ann NY Acad Sci 871: 430-434, 1999.
61. Musallam S and Tomlinson RD. Asymmetric integration recorded from vestbular-only cells in response to position transients. J Neurophysiol 88: 2104-2113, 2002.
62. Musallam WS and Tomlinson RD. Model for the translational vestibuloocular reflex (VOR). J Neurophysiol 82: 2010-2014, 1999.
63. 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.
64. Paige GD and Tomko DL. Eye movement responses to linear head motion in the squirrel monkey. I. Basic characteristics. J Neurophysiol 65: 1170-1182, 1991a.
65. Paige GD and Tomko DL. Eye movement responses to linear head motion in the squirrel monkey. II. Visual-vestibular interactions and kinematic considerations. J Neurophysiol 65: 1183-1196, 1991b.
66. Perlmutter SI, Iwamoto Y, Baker JF, and Peterson BW. Interdependence of spatial properties and projection patterns of medial vestibulospinal tract neurons in the cat. J Neurophysiol 79: 270-284, 1998.
67. Perlmutter SI, Iwamoto Y, Baker JF, and Peterson BW. Spatial alignment of rotational and static tilt responses of vestibulospinal neurons in the cat. J Neurophysiol 82: 855-862, 1999.
68. Raphan T, Dai M, and Cohen B. Spatial orientation of the vestibular system. Ann NY Acad Sci 656: 140-157, 1992.
69. 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, edited by Baker R and Berthoz A. Amsterdam: Elsevier, 1977, p. 37-47.
70. Raphan T, Matsuo V, and Cohen B. Velocity storage in the velocity-ocular reflex arc (VOR). Exp Brain Res 35: 229-248, 1979.
71. Raphan T and Schnabolk C. Modeling slow phase velocity generation during off-vertical axis rotation. Ann NY Acad Sci 545: 29-50, 1988.
72. Raphan T and Sturm D. Modeling the spatiotemporal organization of velocity storage in the vestibuloocular reflex by optokinetic studies. J Neurophysiol 66: 1410-1421, 1991.
73. Reisine H and Raphan T. Neural basis for eye velocity generation in the vestibular nuclei of alert monkeys during off-vertical axis rotation. Exp Brain Res 92: 209-226, 1992.
74. Robinson DA. Linear addition of optokinetic and vestibular signals in the vestibular nucleus. Exp Brain Res 30: 447-450, 1977.
75. Robinson DA. The use of control systems analysis in the neurophysiology of eye movements. Annu Rev Neurosci 4: 463-503, 1981.
76. Schor RH, Miller AD, Timerick SBJ, and Tomko DL. Responses to head tilt in cat central vestibular neurons. II. Frequency dependence of neural response vectors. J Neurophysiol 53: 1444-1452, 1985.
77. Schor RH, Miller AD, and Tomko DL. Responses to head tilt in cat central vestibular neurons. I. Direction of maximum sensitivity. J Neurophysiol 51: 136-146, 1984.
78. Schwarz U, Busettini C, and Miles FA. Ocular responses to linear motion are inversely proportional to viewing distance. Science 245: 1394-1396, 1989.
79. Schwarz U and Miles FA. Ocular responses to translation and their dependence on viewing distance. I. Motion of the observer. J Neurophysiol 66: 851-864, 1991.
80. 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.
81. Siebold C, Anagnostou E, Glasauer S, Gionti L, Kleine JF, Tchelidze T, and Büttner U. Canal-otolith interaction in the fastigial nucleus of the alert monkey. Exp Brain Res 136: 169-178, 2001.
82. Siebold C, Glonti L, Glasauer S, and Büttner U. Rostral fastigial nucleus activity in the alert monkey during three-dimensional passive head movements. J Neurophysiol 77: 1432-1446, 1997.
83. Siebold C, Kleine JF, Glonti L, Tchelidze T, and Büttner U. Fastigial nucleus activity during different frequencies and orientations of vertical vestibular stimulation in the monkey. J Neurophysiol 82: 34-41, 1999.
84. Skavenski AA and Robinson DA. Role of abducens neurons in vestibuloocular reflex. J Neurophysiol 36: 724-738, 1973.
85. Telford L, Seidman SH, and Paige GD. Dynamics of squirrel monkey linear vestibuloocular reflex and interactions with fixation distance. J Neurophysiol 78: 1775-1790, 1997.
86. Tomlinson RD, McConville KMV, and Na E-Q. Behavior of cells without eye movement sensitivity in the vestibular nuclei during combined rotational and translational stimuli. J Vest Res 6: 145-158, 1996.
87. Uchino Y, Ikegami H, Sasaki M, Endo K, Imagawa M, and Isu N. Monosynaptic and disynaptic connections in the utriculo-ocular reflex arc of the cat. J Neurophysiol 71: 950-958, 1994.
88. Viéville T and Faugeras OD. Cooperation of the inertial and visual systems. In: Traditional and Non-Traditional Robotic Sensors, edited by Henderson TC. Berlin: Springer-Verlag, 1990.
89. Waespe W, Cohen B, and Raphan T. Dynamic modification of the vestibuloocular reflex by the nodulus and uvula. Science 228: 199-202, 1985.
90. Waespe W and Henn V. Neuronal activity in the vestibular nuclei of the alert monkey during vestibular and optokinetic stimulation. Exp Brain Res 27: 523-538, 1977.
91. Waespe W and Henn V. Conflicting visual-vestibular stimulation and vestibular nucleus activity in alert monkeys. Exp Brain Res 33: 203-211, 1978.
92. Waespe W and Henn V. The velocity response of vestibular nucleus neurons during vestibular, visual, and combined angular acceleration. Exp Brain Res 37: 337-347, 1979.
93. Wearne S, Raphan T, and Cohen B. Contribution of vestibular commissural pathways to spatial orientation of the angular vestibuloocular reflex. J Neurophysiol 78: 1193-1197, 1997.
94. Wearne S, Raphan T, and Cohen B. Control of spatial orientation of the angular vestibuloocular reflex by the nodulus and uvula. J Neurophysiol 79: 2690-2715, 1998.
95. 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.
96. Wei M and Angelaki DE. Cross-axis adaptation of the translational vestibuloocular reflex. Exp Brain Res 138: 304-312, 2001.
97. Wilson VJ, Ikegami H, Schor RH, and Thomson DB. Tilt responses of neurons in the caudal descending nucleus of the decerebrate cat: influence of the caudal cerebellar vermis and of neck receptors. J Neurophysiol 75: 1242-1249, 1996.
98. Wilson VJ, Yamagata Y, Yates BJ, Schor RH, and Nonaka S. Response of vestibular neurons to head rotations in vertical planes. III. Response of vestibulocollic neurons to vestibular and neck stimulation. J Neurophysiol 64: 1695-1703, 1990.
99. Yakushin SB, Raphan T, and Cohen B. Spatial properties of otolith units recorded in the vestibular nuclei. Ann NY Acad Sci 871: 458-462, 1999.
100. Young LR. Perceptions of the body in space: mechanisms. In: Handbook of Physiology. The Nervous System. Sensory Processes. Bethesda, MD: Am. Physiol. Soc., 1984, sect. 1, vol. III, pt. 2, p. 1023-1066.
101. Zhou W, Tang B-F, and King WM. Vestibular neurons encode linear translation and head tilt with respect to gravity. Soc Neurosci Abstr 26: 1491, 2000.
102. Zhou W, Tang B-F, and King WM. Responses of rostral fastigial neurons to linear acceleration in an alert monkey. Exp Brain Res 139: 111-115, 2001.
103. Zupan LH, Merfeld DM, 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.