Visual-vestibular interaction hypothesis for the control of orienting gaze shifts by brain stem omnipause neurons

Journal of Neurophysiology

Volumn 97, Issue 2, 2007, Pages 1149-1162

  Prsa, Mario ^a   Galiana, Henrietta L ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BEHAVIOR; BRAIN NERVE CELL; BRAIN STEM; GAZE; HEAD MOVEMENT; HUMAN; HYPOTHESIS; NEUROANATOMY; PRIORITY JOURNAL; SACCADIC EYE MOVEMENT; SIMULATION; VELOCITY; VESTIBULAR FUNCTION; VESTIBULOOCULAR REFLEX;

BRAIN MAPPING; BRAIN STEM; COMPUTER SIMULATION; FIXATION, OCULAR; FUNCTIONAL LATERALITY; HEAD MOVEMENTS; HUMANS; MODELS, NEUROLOGICAL; NEURONS; NYSTAGMUS, OPTOKINETIC; ORIENTATION; ROTATION; SACCADES; VESTIBULE; VISION;

EID: 33846903777     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00856.2006     Document Type: Article

References (80)

1. Baker R, Mano N, Shimazu H. Postsynaptic potentials in abducens motoneurons induced by vestibular stimulation. Brain Res 15: 577-580, 1969.
2. Barnes GR. Vestibulo-ocular function during coordinated head and eye movements to acquire visual targets. J Physiol 287: 127-147, 1979.
3. Belton T, McCrea RA. Role of the cerebellar flocculus region in cancellation of the VOR during passive whole body rotation. J Neurophysiol 84: 1599-1613, 2000.
4. Bergeron A, Guitton D. In multiple-step gaze shifts: omnipause (OPNs) and collicular fixation neurons encode gaze position error; OPNs gate saccades. J Neurophysiol 88: 1726-1742, 2002.
5. Bergeron A, Matsuo S, Guitton D. Superior colliculus encodes distance to target, not saccade amplitude, in multiple-step gaze shifts. Nat Neurosci 6: 404-413, 2003.
6. Büttner-Ennever JA, Horn AKE, Henn V, Cohen B. Projections from the superior colliculus motor map to omnipause neurons in monkey. J Comp Neurol 413: 55-67, 1999.
7. Choi WY, Guitton D. Responses of collicular fixation neurons to gaze shift perturbations in head-unrestrained monkey reveal gaze feedback control. Neuron 50: 491-505, 2006.
8. Chubb MC, Fuchs AF, Scudder CA. Neuron activity in monkey vestibular nuclei during vertical vestibular stimulation and eye movements. J Neurophysiol 52: 724-742, 1984.
9. Chun KS, Robinson DA. A model for quick phase generation in the vestibuloocular reflex. Biol Cybern 28: 209-221, 1978.
10. Chimoto S, Iwamoto Y, Shimazu H, Yoshida K. Monosynaptic activation of medium-lead burst neurons from the superior colliculus in the alert cat. J Neurophysiol 75: 2658-2661, 1996.
11. Cohen B, Henn V. Unit activity in the pontine reticular formation associated with eye movements. Brain Res 46: 403-410, 1972.
12. Cohen B, Komatsuzaki A. Eye movements induced by stimulation of the pontine reticular formation: evidence for integration in oculomotor pathways. Exp Neurol 36: 101-107, 1972.
13. Cullen KE, Belton T, McCrea RA. A non-visual mechanism for voluntary cancellation of the vestibuloocular reflex. Exp Brain Res 83: 237-252, 1991.
14. Cullen KE, Guitton D. Analysis of primate IBN spike trains using system identification techniques. I. Relationship to eye-movement dynamics during head-fixed saccades. J Neurophysiol 78: 3259-3282, 1997a.
15. Cullen KE, Guitton D. Analysis of primate IBN spike trains using system identification techniques. II. Relationship to gaze, eye and head movement dynamics during head-free gaze shifts. J Neurophysiol 78: 3283-3306, 1997b.
16. Cullen KE, Guitton D, Rey CG, Jiang W. Gaze-related activity of putative inhibitory burst neurons in the head-free cat. J Neurophysiol 70: 2678-2683, 1993.
17. Cullen KE, Huterer M, Braidwood DA, Sylvestre PA. Time course of vestibuloocular reflex suppression during gaze shifts. J Neurophysio, 92: 3408-3422, 2004.
18. Curthoys IS, Markham CH, Furuya N. Direct projection of pause neurons to nystagmus-related excitatory burst neurons in the cat pontine reticular formation. Exp Neurol 83: 414-422, 1984.
19. Freedman EG. Interactions between eye and head control signals can account for movement kinematics. Biol Cybern 84: 453-462, 2001.
20. Freedman EG, Sparks DL. Eye-head coordination during head-unrestrained gaze shifts in rhesus monkeys. J Neurophysiol 77: 2328-2348, 1997.
21. Fuchs AF, Kimm J. Unit activity in vestibular nucleus of the alert monkey during horizontal angular acceleration and eye movement. J Neurophysiol 38: 1140-1161, 1975.
22. Galiana HL. A nystagmus strategy to linearize the vestibulo-ocular reflex. IEEE Trans Biomed Eng. 38: 243-254, 1991.
23. Galiana HL, Guitton D. Central organization and modeling of eye-head coordination during orienting gaze shifts. Ann NY Acad Sci 656: 452-471, 1992.
24. Galiana HL, Outerbridge JS. A bilateral model for central neural pathways in the vestibuloocular reflex. J Neurophysiol 51: 210-241, 1984.
25. Goossens HHLM, Van Opstal AJ. Human eye-head coordination in two dimensions under different sensorimotor conditions. Exp Brain Res 114: 542-560, 1997.
26. Guitton D, Choi WY. Discharge characteristics of fixation neurons in primate superior colliculus during head-perturbed gaze shifts. Soc Neurosci Abstr 28: 11.8, 2002.
27. Guitton D, Douglas RM, Volle M. Eye-head coordination in cats. J Neurophysiol 52: 1030-1049, 1984.
28. Guitton D, Mandl G. A comparison between saccades and quick phases of vestibular nystagmus in the cat. Vis Res 20: 865-873, 1980.
29. Guitton D, Volle M. Gaze control in humans: eye-head coordination during orienting movements to targets within and beyond the oculomotor range. J Neurophysiol 58: 427-458, 1987.
30. Hepp K, Van Opstal AJ, Straumann D, Hess BJM, Henn V. Monkey superior colliculus represents rapid eye movements in a two-dimensional motor map. J Neurophysiol 69: 965-979, 1993.
31. Ito J, Markham CH, Curthoys IS. Direct projection of type II vestibular neurons to eye movement-related pause neurons in the cat pontine reticular formation. Exp Neurol 91: 331-342, 1986.
32. Ito J, Markham CH, Curthoys IS. Modification of vestibular-induced pause neuron firing during anesthesia and light sleep. Exp Neurol 95: 571-586, 1987.
33. Kamogawa H, Ohki Y, Shimazu H, Suzuki I, Yamashita M. Inhibitory input to pause neurons from pontine burst neuron area in the cat. Neurosci Lett 203: 163-166, 1996.
34. Kaneko CRS, Fuchs AF. Connections of cat omnipause neurons. Brain Res 241: 166-170, 1982.
35. Kaneko CRS. Saccade-related long-lead burst neurons in the monkey rostral pons. J Neurophysiol 95: 979-994, 2006.
36. King WM, Precht W, Dieringer N. Connections of behaviorally identified cat omnipause neurons. Exp Brain Res 32: 435-438, 1978.
37. King WM, Precht W, Dieringer N. Afferent and efferent connections of cat omnipause neurons. Exp Brain Res 38: 395-409. 1980.
38. Kitama T, Ohki Y, Shimazu H, Tanaka M, Yoshida K. Site of interaction between saccade signals and vestibular signals induced by head rotation in the alert cat: functional properties and afferent organization of burster-driving neurons. J Neurophysiol 74: 273-287, 1995.
39. Keller EL. Participation of medial pontine reticular formation in eye movement generation in monkey. J Neurophysiol 37: 316-332, 1974.
40. Keller EL. Brain stem mechanisms in saccadic control. In: Progress in Oculomotor Research, Developments in Neuroscience, edited by Fuchs AF, Becker W. New York: Elsevier, 1981, vol. 12, p. 57-62.
41. Krauzlis RJ, Basso MA, Wurtz RH. Shared motor error for multiple eye movements. Science 276: 1963-1965, 1997.
42. Krauzlis RJ, Basso MA, Wurtz RH. Discharge properties of neurons in the rostral superior colliculus of the monkey during smooth-pursuit eye movements. J Neurophysiol 84: 876-891, 2000.
43. Lefevre P, Quaia C, Optican LM. Distributed model of control of saccades by superior colliculus and cerebellum. Neural Networks 11: 1175-1190, 1998.
44. Lisberger SG. Visual tracking in monkeys: evidence for short-latency suppression of the vestibuloocular reflex. J Neurophysiol 63: 676-688, 1990.
45. Matsuo S, Bergeron A, Guitton D. Evidence for gaze feedback to the cat superior colliculus: discharges reflect gaze trajectory perturbations. J Neurosci 24: 2760-2773, 2004.
46. Meng H, Green AM, Dickman JD, Angelaki DE. Pursuit-vestibular interactions in brain stem neurons during rotation and translation. J Neurophysiol 93: 3418-3433, 2005.
47. Moschovakis AK, Scudder CA, Highstein SM. The microscopic anatomy and physiology of the mammalian saccadic system. Prog Neurobiol 50: 133-254, 1996.
48. Munoz DP, Guitton D. Fixation and orientation control by the tecto-reticulospinal system in the cat whose head is unrestrained. Rev Neurol 145: 567-579, 1989.
49. Munoz DP, Guitton D, Pelisson D. Control of orienting gaze shifts by the tectoreticulospinal system in the head-free cat. III. Spatiotemporal characteristics of phasic motor discharges. J Neurophysiol 66: 1642-1666, 1991.
50. Munoz DP, Waitzman DM, Wurtz RH. Activity of neurons in monkey superior colliculus during interrupted saccades. J Neurophysiol 75: 2562-2580, 1996.
51. Munoz DP, Wurtz RH. Fixation cells in monkey superior colliculus. I. Characteristics of cell discharge. J Neurophysiol 70: 559-575, 1993.
52. Paré M, Guitton D. The fixation area of the cat superior colliculus: effects of electrical stimulation and direct connection with brain stem omnipause neurons. Exp Brain Res 101: 109-122, 1994.
53. Paré M, Guitton D. Brain stem omnipause neurons and the control of combined eye-head gaze saccades in the alert cat. J Neurophysiol 79: 3060-3076, 1998.
54. Pélisson D, Prablanc C, Urquizar C. Vestibuloocular reflex inhibition and gaze saccade control characteristics during eyehead orientation in humans. J Neurophysiol 59: 997-1013, 1988.
55. Phillips JO, Ling L, Fuchs AF, Seibold C, Plorde JJ. Rapid horizontal gaze movement in the monkey. J Neurophysiol 73: 1632-1652, 1995.
56. Quaia C, Lefevre P, Optican LM. Model of the control of saccades by superior colliculus and cerebellum. J Neurophysiol 82: 999-1018, 1999.
57. Raybourn MS, Keller EL. Colliculoreticular organization in primate oculomotor system. J Neurophysiol 40: 861-878, 1977.
58. Robinson DA. Oculomotor control signals. In: Basic Mechanisms of Ocular Motility and Their Clinical Implications, edited by Bach-y-Rita P, Lennerstrand G. New York: Pergamon, 1975, p. 337-374.
59. Ron S, Robinson DA, Skavenski AA. Saccades and the quick phases of nystagmus. Vis Res 12: 2015-22, 1972.
60. Roy JE, Cullen KE. Vestibuloocular reflex signal modulation during voluntary and passive head movements. J Neurophysiol, 87: 2337-2357, 2002.
61. Schiller PH, Stryker M. Single-unit recording and stimulation in superior colliculus of the alert rhesus monkey. J Neurophysiol 35: 915-924, 1972.
62. Schiller PH, True SD, Conway JL. Deficits in eye movements following frontal eye field and superior colliculus ablations. J Neurophysiol 44: 1175-1189, 1980.
63. Scudder CA. A new local feedback model of the saccadic burst generator. J Neurophysiol 59: 1455-1475, 1988.
64. Scudder CA, Kaneko CS, Fuchs AF. The brain stem burst generator for saccadic eye movements: a modern synthesis. Exp Brain Res 142: 439-462, 2002.
65. Strassman A, Highstein SM, McCrea RA. Anatomy and physiology of saccadic burst neurons in the alert squirrel monkey. II. Inhibitory burst neurons. J Comp Neurol 249: 358-380, 1986.
66. Sugiuchi Y, Tazawa Y, Takahashi M, Na J, Shinoda Y. Physiological characterization of synaptic inputs to inhibitory burst neurons from the rostral and caudal superior colliculus. J Neurophysiol 93: 697-712, 2005.
67. Takahashi M, Sugiuchi Y, Izawa Y, Shinoda Y. Synaptic inputs and their pathways from fixation and saccade zones of the superior colliculus to inhibitory burst neurons and pause neurons. Ann NY Acad Sci 1039: 209-219, 2005.
68. Takeichi N, Fukushima K, Sasaki H, Yabe I, Tashiro K, Inuyama Y. Dissociation of smooth pursuit and vestibulo-ocular reflex cancellation in SCA-6. Neurology 54: 860-866, 2000.
69. Tomlinson RD. Combined eye-head gaze shifts in the primate. III. Contributions to the accuracy of gaze saccades. J Neurophysiol 64: 1873-1891, 1990.
70. Tomlinson RD, Bahra PS. Combined eye-head gaze shifts in the primate. I. Metrics. J Neurophysiol 56: 1542-1557, 1986a.
71. Tomlinson RD, Bahra PS. Combined eye-head gaze shifts in the primate. II. Interactions between saccades and the vestibuloocular reflex. J Neurophysiol 56: 1558-1570, 1986b.
72. Tomlinson RD, Robinson DA. Signals in vestibular nucleus meditating vertical eye movements in the monkey. J Neurophysiol 51: 1121-1136, 1984.
73. Tweed D, Glenn B, Vilis T. Eye-head coordination during large gaze shifts. J Neurophysiol 73: 766-799, 1995.
74. Tweed D, Vilis T. A two dimensional model for saccade generation. Biol Cybern 52: 219-227, 1985.
75. Van Gisbergen JA, Robinson DA, Gielen S. A quantitative analysis of generation of saccadic eye movements by burst neurons. J Neurophysiol 45: 417-442, 1981.
76. Van Opstal AJ, Van Gisbergen JA. A model for collicular efferent mechanisms underlying the generation of saccades. Brain Behav Evol 33: 90-94, 1989.
77. Wurtz RH, Goldberg ME. Activity of superior colliculus in behaving monkey. III. Cells discharging before eye movements. J Neurophysiol 35: 575-586, 1972.
78. Yoshida K, Iwamoto Y, Chimoto S, Shimazu H. Saccade-related inhibitory input to pontine omnipause neurons: an intracellular study in alert cats. J Neurophysiol 82: 1198-1208, 1999.
79. Yoshida K, Iwamoto Y, Chimoto S, Shimazu H. Disynaptic inhibition of omnipause neurons following electrical stimulation of the superior colliculus in alert cats. J Neurophysiol 85: 2639-2642, 2001.
80. Zee DS, Optican LM, Cook JD, Robinson DA. Slow saccades in spinocerebellar degeneration. Arch Neurol 33: 243-251, 1976.