The brain stem saccadic burst generator encodes gaze in three-dimensional space

Journal of Neurophysiology

Volumn 99, Issue 5, 2008, Pages 2602-2616

  Van Horn, Marion R ^a   Sylvestre, Pierre A ^a   Cullen, Kathleen E ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b McIntyre Medical Research Building ^*  (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ABDUCENS NERVE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN STEM; COMPUTER PROGRAM; CONTROLLED STUDY; GAZE; MOTONEURON; NERVE CONDUCTION; NONHUMAN; PREMOTOR CORTEX; PRIORITY JOURNAL; SACCADIC EYE MOVEMENT; VISUOMOTOR COORDINATION; ALGORITHM; ANIMAL; CYTOLOGY; DEPTH PERCEPTION; EYE FIXATION; MACACA; MONOCULAR VISION; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE; STATISTICAL ANALYSIS; VISION; VISUAL SYSTEM;

ABDUCENS NERVE; ALGORITHMS; ANIMALS; BRAIN STEM; DATA INTERPRETATION, STATISTICAL; FIXATION, OCULAR; MACACA MULATTA; MOTOR NEURONS; PSYCHOMOTOR PERFORMANCE; SACCADES; SPACE PERCEPTION; VISION, MONOCULAR; VISUAL PATHWAYS; VISUAL PERCEPTION;

EID: 47549108281     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01379.2007     Document Type: Article

References (86)

1. Busettini C, Mays LE. Pontine omnipause activity during conjugate and disconjugate eye movements in macaques. J Neurophysiol 90: 3838-3853, 2003.
2. Busettini C, Mays LE. Saccade-vergence interactions in macaques. I. Test of the omnipause Multiply Model. J Neurophysiol 94: 2295-2311, 2005a.
3. Busettini C, Mays LE. Saccade-vergence interactions in macaques. II. Vergence enhancement as the product of a local feedback vergence motor error and a weighted saccadic burst. J Neurophysiol 94: 2312-2330, 2005b.
4. Carpenter J, Bithell J. Bootstrap confidence intervals: when, which, what? A practical guide for medical statisticians. Stat Med 19: 1141-1164, 2000.
5. Chaturvedi V, Van Gisbergen J. Perturbation of combined saccade-vergence movements by microstimulation in monkey superior colliculus. J Neurophysiol 81: 2279-2296, 1999.
6. Chaturvedi V, Van Gisbergen J. Stimulation in the rostral pole of monkey superior colliculus: effects on vergence eye movements. Exp Brain Res 132: 72-78, 2000.
7. Collewijn H, Erkelens CJ, Steinman RM. Voluntary binocular gaze-shifts in the plane of regard: dynamics of version and vergence. Vision Res 35: 3335-3358, 1995.
8. Collewijn H, Erkelens CJ, Steinman RM. Trajectories of the human binocular fixation point during conjugate and non-conjugate gaze-shifts. Vision Res 37: 1049-1069, 1997.
9. Cova A, Galiana H. Providing distinct vergence and version dynamics in a bilateral oculomotor network. Vision Res 35: 3359-3371, 1995.
10. Cova A, Galiana H. A bilateral model integrating vergence and the vestibuloocular reflex. Exp Brain Res 107: 435-452, 1996.
11. Crawford JR, Howell DC, Garthwaite PH. Payne and Jones revisited: estimating the abnormality of test score differences using a modified paired samples t test. J Clin Exp Neuropsychol 20: 898-905, 1998.
12. Cullen K, 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.
13. Cullen K, Guitton D, Rey C, Jiang W. Gaze-related activity of putative inhibitory burst neurons in the head-free cat. J Neurophysiol 70: 2678-2683, 1993b.
14. Cullen K, McCrea R. Firing behavior of brain stem neurons during voluntary cancellation of the horizontal vestibuloocular reflex. I. Secondary vestibular neurons. J Neurophysiol 70: 828-843, 1993.
15. Cullen KE, Chen-Huang C, McCrea RA. Firing behavior of brain stem neurons during voluntary cancellation of the horizontal vestibuloocular reflex. II. Eye movement related neurons. J Neurophysiol 70: 844-856, 1993.
16. Cullen KE, Guitton D. Inhibitory burst neuron activity encodes gaze, not eye, metrics and dynamics during passive head on body rotation. Evidence that vestibular signals supplement visual information in the control of gaze shifts. Ann NY Acad Sci 781: 601-606, 1996.
17. 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, 1997.
18. Cullen KE, Rey CG, Guitton D, Galiana HL. The use of system identification techniques in the analysis of oculomotor burst neuron spike train dynamics. J Comput Neurosci 3: 347-368, 1996.
19. Eckmiller R, Blair S, Westheimer G. Fine structure of saccade bursts in macaque pontine neurons. Brain Res 181: 460-464, 1980.
20. Eckmiller R, Mackeben M. Pre-motor single unit activity in the monkey brain stem correlated with eye velocity during pursuit. Brain Res 184: 210-214, 1980.
21. Enright J. Changes in vergence mediated by saccades. J Physiol 350: 9-31, 1984.
22. Enright JT. The remarkable saccades of asymmetrical vergence. Vision Res 32: 2261-2276, 1992.
23. Erkelens CJ, Van der Steen J, Steinman RM, Collewijn H. Ocular vergence under natural conditions. I. Continuous changes of target distance along the median plane. Proc R Soc Lond B Biol Sci 236: 417-440, 1989.
24. Ferraina S, Paré M, Wurtz R. Disparity sensitivity of frontal eye field neurons. J Neurophysiol 83: 625-629, 2000.
25. Fuchs AF, Robinson DA. A method for measuring horizontal and vertical eye movements in the monkey. J Physiol 191: 609-631, 1966.
26. Fuchs AF, Robinson DA, Straube A. Role of the caudal fastigial nucleus in saccade generation. I. Neuronal discharge pattern. J Neurophysiol 70: 1723-1740, 1993.
27. Gamlin PD. Subcortical neural circuits for ocular accommodation and vergence in primates. Ophthalmic Physiol Opt 19: 81-89, 1999.
28. Gamlin PD, Gnadt JW, Mays LE. Abducens internuclear neurons carry an inappropriate signal for ocular convergence. J Neurophysiol 62: 70-81, 1989.
29. Gamlin PD, Yoon K. An area for vergence eye movement in primate frontal cortex. Nature 407: 1003-1007, 2000.
30. Gnadt JW, Beyer J. Eye movements in depth: what does the monkey's parietal cortex tell the superior colliculus? Neuroreport 9: 233-238, 1998.
31. Gnadt JW, Gamlin PD, Mays LE, Zhang Y. Vergence-related cells near the abducens nuclei. Soc Neurosci Abstr 14: 612, 1988.
32. Hayes AV, Richmond BJ, Optican LM. A UNIX-based multiple process system for real-time data acquisition and control. In: Proceedings of the Western Electronic Show and Conference (Wescon/82), Anaheim, California, Sept. 15, 1982. El Segundo, CA: Electronic Conventions, 1982, p. 2/1-1-2/1-10.
33. Hazel T, Sklavos S, Dean P. Estimation of premotor synaptic drives to simulated abducens motoneurons for control of eye position. Exp Brain Res 146: 184-196, 2002.
34. Hepp K, Henn V. Spatio-temporal recoding of rapid eye movement signals in the monkey paramedian pontine reticular formation (PPRF). Exp Brain Res 52: 105-120, 1983.
35. Highstein SM, Baker R. Excitatory termination of abducens internuclear neurons on medial rectus motoneurons: relationship to syndrome of internuclear ophthalmoplegia. J Neurophysiol 41: 1647-1661, 1978.
36. Judge SJ, Richmond BJ, Chu FC. Implantation of magnetic search coils for measurement of eye position: an improved method. Vision Res 20: 535-538, 1980.
37. Kaneko CR, Evinger C, Fuchs AF. Role of cat pontine burst neurons in generation of saccadic eye movements. J Neurophysiol 46: 387-408, 1981.
38. Keller EL. Participation of medial pontine reticular formation in eye movement generation in monkey. J Neurophysiol 37: 316-332, 1974.
39. Kenyon R, Ciuffreda K, Stark L. Unequal saccades during vergence. Am J Optom Physiol Opt 57: 586-594, 1980.
40. King WM, Zhou W. New ideas about binocular coordination of eye movements: is there a chameleon in the primate family tree? Anat Rec 261: 153-161, 2000.
41. King WM, Zhou W. Neural basis of disjunctive eye movements. Ann NY Acad Sci 956: 273-283, 2002.
42. Kumar AN, Han Y, Dell'Osso LF, Durand DM, Leigh RJ. Directional asymmetry during combined saccade-vergence movements. J Neurophysiol 93: 2797-2808, 2005.
43. Kumar AN, Han YH, Kirsch RF, Dell'Osso LF, King WM, Leigh RJ. Tests of models for saccade-vergence interaction using novel stimulus conditions. Biol Cybern 95: 143-157, 2006.
44. Langer TP, Kaneko CR, Scudder CA, Fuchs AF. Afferents to the abducens nucleus in the monkey and cat. J Comp Neurol 245: 379-400, 1986.
45. Leigh RJ, Zee DS. The Neurology of Eye Movements. New York: Oxford Univ. Press, 1999, p. 286-320.
46. Luque MA, Perez-Perez MP, Herrero L, Waitzman DM, Torres B. Eye movements evoked by electrical microstimulation of the mesencephalic reticular formation in goldfish. Neuroscience 137: 1051-1073, 2006.
47. Luschei E, Fuchs AF. Activity of brain stem neurons during eye movements of alert monkeys. J Neurophysiol 35: 445-461, 1972.
48. Maxwell JS, King WM. Dynamics and efficacy of saccade-facilitated vergence eye movements in monkeys. J Neurophysiol 68: 1248-1260, 1992.
49. Mays LE, Gamlin PD. Neuronal circuitry controlling the near response. Curr Opin Neurobiol 5: 763-768, 1995.
50. Mays LE, Porter JD. Neural control of vergence eye movements: activity of abducens and oculomotor neurons. J Neurophysiol 52: 743-761, 1984.
51. Mays LE, Porter JD, Gamlin PD, Tello CA. Neural control of vergence eye movements: neurons encoding vergence velocity. J Neurophysiol 56: 1007-1021, 1986.
52. McConville KM, Tomlinson D, King WM, Paige GD, Na E-Q. Eye position signals in the vestibular nuclei: consequences for models of integrator function. J Vestib Res 4: 391-400, 1994.
53. McFarland J, Fuchs A. Discharge patterns in nucleus prepositus hypoglossi and adjacent medial vestibular nucleus during horizontal eye movement in behaving macaques. J Neurophysiol 68: 319-332, 1992.
54. Moschovakis AK, Karabelas AB, Highstein SM. Structure-function relationships in the primate superior colliculus. II. Morphological identity of presaccadic neurons. J Neurophysiol 60: 263-302, 1988.
55. Noda H, Sugita S, Ikeda Y. Afferent and efferent connections of the oculomotor region of the fastigial nucleus in the macaque monkey. J Comp Neurol 302: 330-348, 1990.
56. Ono H, Nakamizo S, Steinbach MJ. Nonadditivity of vergence and saccadic eye movement. Vision Res 18: 735-739, 1978.
57. Oohira A. Vergence eye movements facilitated by saccades. Jpn J Ophthalmol 37: 400-413, 1993.
58. Press LJ. Effect of VDUs on the eyes. Optom Vis Sci 74: 130-131, 1997.
59. Ramat S, Somers JT, Das VE, Leigh RJ. Conjugate ocular oscillations during shifts of the direction and depth of visual fixation. Invest Ophthalmol Vis Sci 40: 1681-1686, 1999.
60. Robinson DA. Models of the saccadic eye movement control system. Kybernetik 14: 71-83, 1973.
61. Roy JE, Cullen KE. Vestibuloocular reflex signal modulation during voluntary and passive head movements. J Neurophysiol 87: 2337-2357, 2002.
62. Roy JE, Cullen KE. Brain stem pursuit pathways: dissociating visual, vestibular, and proprioceptive inputs during combined eye-head gaze tracking. J Neurophysiol 90: 271-290, 2003.
63. Schiller PH, Stryker M. Single-unit recording and stimulation in superior colliculus of the alert rhesus monkey. J Neurophysiol 35: 915-924, 1972.
64. Scudder CA. A new local feedback model of the saccadic burst generator. J Neurophysiol 59: 1455-1475, 1988.
65. Scudder CA, Fuchs AF. Physiological and behavioral identification of vestibular nucleus neurons mediating the horizontal vestibuloocular reflex in trained rhesus monkeys. J Neurophysiol 68: 244-264, 1992.
66. Scudder CA, Fuchs AF, Langer TP. Characteristics and functional identification of saccadic inhibitory burst neurons in the alert monkey. J Neurophysiol 59: 1430-1454, 1988.
67. Scudder CA, Kaneko CRS, Fuchs AF. The brainstem burst generator for saccadic eye movements: a modern synthesis. Exp Brain Res 142: 439-462, 2002.
68. Sokal RR, Rohlf FJ. Biometry: The Principles and Practice of Statistics in Biological Research. New York: Freeman, 1995, p. xix.
69. Strassman A, Highstein SM, McCrea RA. Anatomy and physiology of saccadic burst neurons in the alert squirrel monkey. I. Excitatory burst neurons. J Comp Neurol 249: 337-357, 1986a.
70. 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, 1986b.
71. Suzuki S, Suzuki Y, Ohtsuka K. Convergence eye movements evoked by microstimulation of the rostral superior colliculus in the cat. Neurosci Res 49: 39-45, 2004.
72. Sylvestre PA, Choi JT, Cullen KE. Discharge dynamics of oculomotor neural integrator neurons during conjugate and disjunctive saccades and fixation. J Neurophysiol 90: 739-754, 2003.
73. Sylvestre PA, Cullen KE. Quantitative analysis of abducens neuron discharge dynamics during saccadic and slow eye movements. J Neurophysiol 82: 2612-2632, 1999.
74. Sylvestre PA, Cullen KE. Dynamics of abducens nucleus neuron discharges during disjunctive saccades. J Neurophysiol 88: 3452-3468, 2002.
75. Sylvestre PA, Galiana HL, Cullen KE. Conjugate and vergence oscillations during saccades and gaze shifts: implications for integrated control of binocular movement. J Neurophysiol 87: 257-272, 2002.
76. 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.
77. Van Opstal A, Van Gisbergen J, Eggermont J. Reconstruction of neural control signals for saccades based on an inverse method. Vision Res 25: 789-801, 1985.
78. Wackerly DD, Mendenhall W, Scheaffer RL. Mathematical Statistics with Applications. Belmont, CA: Duxbury Press, 1996, p. xvi.
79. Waitzman DM, Van Horn M, Cullen KE. Evidence for independent control of saccadic eye movement in the primate central mesencephalic reticular formation (cMRF). Soc Neurosci Abstr 33: 718, 2007.
80. Walton MM, Mays LE. Discharge of saccade-related superior colliculus neurons during saccades accompanied by vergence. J Neurophysiol 90: 1124-1139, 2003.
81. Yoshida K, McCrea R, Berthoz A, Vidal PP. Morphological and physiological characteristics of inhibitory burst neurons controlling horizontal rapid eye movements in the alert cat. J Neurophysiol 48: 761-784, 1982.
82. Zee DS, Fitzgibbon EJ, Optican LM. Saccade-vergence interactions in humans. J Neurophysiol 68: 1624-1641, 1992.
83. Zhang H, Gamlin PD. Neurons in the posterior interposed nucleus of the cerebellum related to vergence and accommodation. I. Steady-state characteristics. J Neurophysiol 79: 1255-1269, 1998.
84. Zhang Y, Mays LE, Gamlin PD. Characteristics of near response cells projecting to the oculomotor nucleus. J Neurophysiol 67: 944-960, 1992.
85. Zhou W, King WM. Premotor commands encode monocular eye movements. Nature 393: 692-695, 1998.
86. Zuber B, Semmlow J, Stark L. Frequency characteristics of the saccadic eye movement. Biophys J 8: 1288-1298, 1968.