Distributed population mechanism for the 3-D oculomotor reference frame transformation

Journal of Neurophysiology

Volumn 93, Issue 3, 2005, Pages 1742-1761

  Smith, Michael A ^a,b   Crawford, J Douglas ^a  

^a YORK UNIVERSITY   (Canada)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACCURACY; ARTICLE; ARTIFICIAL NEURAL NETWORK; BRAIN STEM; EXTRAOCULAR MUSCLE; EYE MOVEMENT CONTROL; KINEMATICS; NERVE CELL; NEUROPHYSIOLOGY; PRIORITY JOURNAL; RECEPTIVE FIELD; ROTATION; SUPERIOR COLLICULUS; VISUAL STIMULATION; VISUOMOTOR COORDINATION;

FEEDBACK; FUNCTIONAL LATERALITY; HUMANS; MODELS, NEUROLOGICAL; NEURAL NETWORKS (COMPUTER); ORIENTATION; PSYCHOMOTOR PERFORMANCE; SACCADES; VISUAL FIELDS; VISUAL PERCEPTION;

EID: 14244266614     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00306.2004     Document Type: Article

References (122)

1. Andersen RA. Encoding of intention and spatial location in the posterior parietal cortex. Cereb Cortex 5: 457-469, 1995.
2. Andersen RA, Bracewell RM, Barash S, Gnadt JW, and Fogassi L. Eye position effects on visual, memory, and saccade-related activity in areas LIP and 7a of macaque. J Neurosci 10: 1176-1196, 1990.
3. Angelaki DE and Dickman JD. Premotor neurons encode torsional eye velocity during smooth-pursuit eye movements. J Neurosci 7: 2971-2979, 2003.
4. Batista AP, Buneo CA, Snyder LH, and Andersen RA. Reach plans in eye-centered coordinates. Science 285: 257-260, 1999.
5. 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.
6. Bisley JW and Goldberg ME. The role of the parietal cortex in the neural processing of saccadic eye movements. Adv Neurol 93: 141-157, 2003.
7. Brozovic M, Cohen YE, and Andersen RA. Models of coordinate transformations for reaches toward an auditory target. Program No. 658.1. 2003 Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience 2003. Online.
8. Bruce CJ, Goldberg ME, Bushnell MC, and Stanton GB. Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements. J Neurophysiol 54: 714-734, 1985.
9. Buneo CA, Jarvis MR, Batista AP, and Andersen RA. Direct visuomotor transformations for reaching. Nature 416: 632-636, 2002.
10. Cannon SC and Robinson DA. Loss of the neural integrator of the oculomotor system from brainstem lesions in the monkey. J Neurophysiol 57: 1383-1409, 1987.
11. Cheron G and Godaux E. Disabling of the oculomotor neural integrator by kainic acid injections in the prepositus-vestibular complex of the cat. J Physiol 394: 267-290, 1987.
12. Colby CL, Duhamel JR, and Goldberg ME. Oculocentric spatial representation in parietal cortex. Cereb Cortex 5: 470-481, 1995.
13. Colby CL and Goldberg ME. Space and attention in parietal cortex. Ann Rev Neurosci 22: 319-349, 1999.
14. Crammond DJ and Kalaska JF. Neuronal activity in primate parietal cortex area 5 varies with intended movement direction during an instructed-delay period. Exp Brain Res 76: 458-462, 1989.
15. Crawford JD. The oculomotor neural integrator uses a behavior-related coordinate system. J Neurosci 14: 6911-6923, 1994.
16. Crawford JD, Cadera W, and Vilis T. Generation of torsional and vertical eye position signals by the interstitial nucleus of Cajal. Science 252: 1551-1553, 1991.
17. Crawford JD and Guitton D. Visual-motor transformations required for accurate and kinematically correct saccades. J Neurophysiol 78: 1447-1467, 1997.
18. Crawford JD, Henriques DYP, and Vilis T. Curvature of visual space under vertical eye rotation: implications for spatial vision and visuomotor control. J Neurosci 20: 2360-2368, 2000.
19. Crawford JD, Medendorp WP, and Marotta JJ. Spatial transformations for eye-hand coordination. J Neurophysiol 92: 10-19, 2004.
20. Crawford JD and Vilis T. Axes of eye rotation and Listing's law during rotations of the head. J Neurophysiol 65: 407-423, 1991.
21. Crawford JD and Vilis T. Symmetry of oculomotor burst neuron coordinates about Listing's plane. J Neurophysiol 68: 432-448, 1992.
22. Cullen KE and 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.
23. Cynader M and Berman N. Receptive-field organization of monkey superior colliculus. J Neurophysiol 35: 187-201, 1972.
24. Demer JL, Miller JM, Poukens V, Vinters HV, and Glasgow BJ. Evidence for fibromuscular pulleys of the recti extraocular muscles. Invest Ophthalmol Vis Sci 36: 1125-1136, 1995.
25. Demer JL, Oh SY, and Poukens V. Evidence for active control of rectus extraocular muscle pulleys. Invest Ophthalmol Vis Sci 41: 1280-1290, 2000.
26. Duhamel JR, Bremmer F, BenHamed S, and Graf W. Spatial invariance of visual receptive fields in parietal cortex neurons. Nature 389: 845-848, 1997.
27. Duhamel JR, Colby CL, and Goldberg ME. The updating of the representation of visual space in parietal cortex by intended eye movements. Science 255: 90-92, 1992.
28. Ferman L, Collewijn H, and Van Den Berg AV. A direct test of Listing's law. I. Human ocular torsion measured in static tertiary positions. Vision Res 27: 929-938, 1987.
29. Freedman EG and Sparks DL. Activity of cells in the deeper layers of the superior colliculus of Rhesus monkey: evidence for a gaze displacement command. J Neurophysiol 78: 1669-1690, 1997.
30. Frens MA and Van Opstal AJ. Transfer of short term adaptation in human saccadic eye movements. Exp Brain Res 100: 293-306, 1994.
31. Fukushima K, Harada C, Fukushima J, and Suzuki Y. Spatial properties of vertical eye movement-related neurons in the region of the interstitial nucleus of Cajal. Exp Brain Res 79: 25-42, 1990.
32. Fukushima K, Ohashi T, Fukushima J, and Kase M. Ocular torsion produced by unilateral chemical inactivation of the interstitial nucleus of Cajal in chronically labyrinthectomized cats. Neurosci Res 13: 301-305, 1992.
33. Georgopoulos AP, Kalaska JF, Camaniti R, and Massey JT. On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex. J Neurosci 2: 1527-1537, 1982.
34. Georgopoulos AP, Lurito JT, Petrides M, Schwartz AB, and Massey JT. Mental rotation of the neuronal population vector. Science 243: 234-236, 1989.
35. Georgopoulos AP, Schwartz AB, and Kettner RE. Neuronal population coding of movement direction. Science 233: 1416-1419, 1986.
36. Glasauer S, Dieterich M, and Brandt T. Central positional nystagmus simulated by a mathematical ocular motor model of otolith-dependent modification of Listing's plane. J Neurophysiol 86: 1546-1554, 2001.
37. Goldberg ME, Bisley J, Powell KD, Gottlieb J, and Kusunoki M. The role of the lateral intraparietal area of the monkey in the generation of saccades and visuospatial attention. Ann NY Acad Sci 956: 205-215, 2002.
38. Goldberg ME and Bruce CJ. Primate frontal eye fields. III. Maintenance of a spatially accurate saccade signal. J Neurophysiol 64: 489-508, 1990.
39. Gottlieb J, Kusunoki M, and Goldberg ME. The representation of visual salience in monkey parietal cortex. Nature 391: 481-484, 1998.
40. Grossberg S and Kuperstein M. Neural dynamics of adaptive sensory motor control, ballistic eye movements. North-Holland: Elsevier North-Holland. 1986.
41. Hallet PE and Lightstone AD. Saccadic eye movements towards stimuli triggered by prior saccades. Vision Res 16: 99-106, 1976.
42. Hamed SB, Duhamel JR, Bremmer F, and Graf W. Representation of the visual field in the lateral intraparietal area of macaque monkeys: a quantitative receptive field analysis. Exp Brain Res 140: 127-144, 2001.
43. Henn V, Hepp K, and Vilis T. Rapid eye movement generation in the primate: physiology, pathophysiology and clinical implication. Rev Neurol (Paris) 145: 540-545, 1989.
44. Henriques DYP and Crawford JD. Testing the three-dimensional reference frame transformation for express and memory-delay saccades. Neurocomputing 38-40: 1267-1280, 2001.
45. Hepp K and 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.
46. Hepp K, Suzuki J, Straumann D, and Hess BJM. On the 3-dimensional rapid eye movement generator in the monkey. In: Information Processing Underlying Gaze Control, edited by Delgado-Garcia JM, Godeaux E, and Vidal PP. Oxford, UK: Pergamon, 1994, p. 65-74.
47. Hepp K, Suzuki Y, Straumann D, Hess BJ, and Henn V. Eye position dependence of innervation on-directions of motoneurons in the monkey. Ann NY Acad Sci 781: 629-632, 1996.
48. Hepp K, Van Opstal AJ, Straumann D, Hess BJ, and Henn V. Monkey superior colliculus represents rapid eye movements in a two-dimensional motor map. J Neurophysiol 69: 965-979, 1993.
49. Hubel OH and Wiesel TN. Receptive fields of single neurones in the cat's striate cortex. J Neurophysiol 148: 574-591, 1959.
50. Jürgens R, Becker W, and Kornhuber H. Natural and drug induces variations of velocity and duration of human saccadic eye movements: evidence for a control of the neural pulse generator by local feedback. Biol Cybern 39: 87-96, 1981.
51. Kalaska JF, Caminiti R, and Georgopoulos AP. Cortical mechanisms related to the direction of two-dimensional arm movements: relations in parietal area 5 and comparison with motor cortex. Exp Brain Res 51: 247-260, 1983.
52. Kaneko CRS and Fukushima K. Discharge characteristics of vestibular saccade neurons in alert monkeys. J Neurophysiol 79: 835-847, 1998.
53. King WM, Fuchs AF, and Magnin M. Vertical eye movement-related responses of neurons in midbrain near intestinal nucleus of Cajal. J Neurophysiol 46: 549-562, 1981.
54. Klier EM and Crawford JD. Human oculomotor system accounts for 3-D eye orientation in the visual-motor transformation for saccades. J Neurophysiol 80: 2274-2294, 1998.
55. Klier EM, Wang H, and Crawford JD. The superior colliculus encodes gaze commands in retinal coordinates. Nat Neurosci 4: 627- 632, 2001.
56. Klier EM, Wang H, and Crawford JD. Three-dimensional eye-head coordination is implemented downstream from the superior colliculus. J Neurophysiol 89: 2839-2853, 2003.
57. Krommenhoek KP, Van Opstal AJ, Gielen CC, and Van Gisbergen JA. Remapping of neural activity in the motor colliculus: a neural network study. Vision Res 33: 1287-1298, 1993.
58. Krommenhoek KP and Wiegerinck WA. A neural network study of precollicular saccadic averaging. Biol Cybern 78: 465-477, 1998.
59. Lee C, Rohrer WH, and Sparks DL. Population coding of saccadic eye movements by neurons in the superior colliculus. Nature 332: 357-360, 1988.
60. Lefevre P, Quaia C, and Optican LM. Distributed model of control of saccades by superior colliculus and cerebellum. Neural Networks 11: 1175-1190, 1998.
61. Maunsell JHR and Van Essen DC. Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. J Neurophysiol 49: 1127-1147, 1983.
62. Mays LE and Sparks DL. Saccades are spatially, not retinocentrically, coded. Science 208: 1163-1165, 1980.
63. McLaughlin SC. Parametric adjustment in saccadic eye movements. Percept Psychophys 2: 359-362, 1967.
64. Miller JM, Anstis T, and Templeton WB. Saccadic plasticity: parametric adaptive control by retinal feedback. J Exp Psychol Hum Percept Perform 1: 356-366, 1981.
65. Mitchell J and Zipser D. A model of visual-spatial memory across saccades. Vision Res 41: 1575-1592, 2001.
66. Moschovakis AK. Neural network simulations of the primate oculomotor system. II. Frames of reference. Brain Res Bull 40: 337-343, 1996.
67. Moschovakis AK and Highstein SM. The anatomy and physiology of primate neurons that control rapid eye movements. Annu Rev Neurosci 17: 465-488, 1994.
68. Nakamura K and Colby CL. Updating of the visual representation in monkey striate and extrastriate cortex during saccades. Proc Natl Acad Sci USA 99: 4026-4031, 2002.
69. Nichols JM and Sparks DL. Nonstationary properties of the saccadic system: new constraints on models of saccadic control. J Neurophysiol 73: 431-435, 1995.
70. Optican LM and Quaia C. Distributed model of collicular and cerebellar function during saccades. Ann NY Acad Sci 956: 164-177, 2002.
71. Pouget A, Dayan P, and Zemel RS. Inference and computation with population codes. Annu Rev Neurosci 26: 381-410, 2003.
72. Quaia C, Lefevre P, and Optican LM. Model of the control of saccades by superior colliculus and cerebellum. J Neurophysiol 82: 999-1018, 1999.
73. Quaia C and Optican LM. Commutative saccadic generator is sufficient to control a 3-D ocular plant with pulleys. J Neurophysiol 79: 3197-3215, 1998.
74. Robinson DA. Eye movement control in primates. Science 161: 1219-1224, 1968.
75. Robinson DA. The effect of cerebellectomy on the cat's vestibuloocular integrator. Brain Res 71: 195, 1974.
76. Robinson DA. Oculomotor control signals. In: Basic Mechanisms of Ocular Motility and Their Clinical Implications (Wenner-Gren Centennial International Symposium Series), edited by Bach-y Nospaceritaqq P and Lennerstrand G. Oxford, UK: Pergamon, 1975, p. 337-374.
77. Robinson DA. Implications of neural networks for how we think about brain function. Behav Brain Sci 15: 644-655, 1992.
78. Rumelhart DE, Hinton GE, and Williams RJ. Learning internal representations by error propagation. In: Parallel Distributed Processing, edited by Rumelhart DE and McClelland JL. Cambridge, MA: MIT Press, 1986, vol. 1, p. 318-362.
79. Russo GS and Bruce CJ. Neurons in the supplementary eye field of rhesus monkeys code visual targets and saccadic eye movements in an oculocentric coordinate system. J Neurophysiol 76: 825-848, 1996.
80. Russo GS and Bruce CJ. Supplementary eye field: representation of saccades and relationship between neural response fields and elicited eye movements. J Neurophysiol 84: 2605-2621, 2000.
81. Sabes PN, Breznen B, and Andersen RA. Parietal representation of object-based saccades. J Neurophysiol 88: 1815-1829, 2002.
82. Salinas E and Abbott LF. Coordinate transformations in the visual system: how to generate gain fields and what to compute with them. Prog Brain Res 130: 175-190, 2001.
83. Scherberger H, Goodale MA, and Andersen RA. Target selection for reaching and saccades share a similar behavioral reference frame in the macaque. J Neurophysiol 89: 1456-1466, 2003.
84. Schnyder H, Reisine H, Hepp K, and Henn V. Frontal eye field projection to the paramedian pontine reticular formation traced with wheat germ agglutinin in the monkey. Brain Res 329: 151-160, 1985.
85. Scott SH, Gribble PL, Graham KM, and Cabel DW. Dissociation between hand motion and population vectors from neural activity in motor cortex. Nature 413: 161-165, 2001.
86. Scudder CA. A new local feedback model of the saccadic burst generator. J Neurophysiol 59: 1455-1475, 1988.
87. Smith MA and Crawford JD. Self-organizing task modules and explicit coordinate systems in a neural network model for 3-D saccades. J Comput Neurosci 10: 127-150, 2001a.
88. Smith MA and Crawford JD. Implications of ocular kinematics for the internal updating of visual space. J Neurophysiol 86: 2112-2127, 2001b.
89. Snyder LH, Grieve KL, Brotchie P, and Andersen RA. Separate body- and world-referenced representations of visual space in parietal cortex. Nature 394: 887-891, 1998.
90. Sparks DL. Functional properties of neurons in the monkey superior colliculus: coupling of neuronal activity and saccade onset. Brain Res 156: 1-16, 1978.
91. Sparks DL. Neural cartography: sensory and motor maps in the superior colliculus. Brain Behav Evol 31: 49-56, 1988.
92. Sparks DL. The neural encoding of the location of targets for saccadic eye movements. J Exp Biol 146: 195-207, 1989.
93. Sparks DL. The brainstem control of saccadic eye movements. Nat Rev Neurosci 3: 952-964, 2002.
94. Sparks DL and Gandhi NJ. Single cell signals: an oculomotor perspective. Prog Brain Res 142: 35-53, 2003.
95. Sparks DL, Holland R, and Guthrie BL. Size and distribution of movement fields in the monkey superior colliculus. Brain Res 113: 21-34, 1976.
96. Sparks DL and Mays LE. Signal transformations required for the generation of saccadic eye movements. Anna Rev Neurosci 13: 309-336, 1990.
97. Stanton GB, Goldberg ME, and Bruce CJ. Frontal eye field efferents in the macaque monkey. II. Topography of terminal fields in the midbrain and pons. J Comp Neurol 271: 493-506, 1988.
98. Steinbach MJ. Proprioceptive knowledge of eye position. Vision Res 27: 1737-1744, 1987.
99. Straumann D, Haslwanter T, Hepp-Reymond MC, and Hepp K. Listing's law for eye, head and arm movements and their synergistic control. Exp Brain Res 86: 209-215, 1991.
100. Suzuki Y, Buttner-Ennever JA, Straumann D, Hepp K, Hess BJM, and Henn V. Deficits in torsional and vertical rapid eye movements and shift of Listing's plane after uni- and bilateral lesions of the rostral interstitial nucleus of the medial longitudinal fasciculus. Exp Brain Res 106: 215-232, 1995.
101. Suzuki Y, Straumann D, Simpson JI, Hepp K, Hess BJ, and Henn V. Three-dimensional extraocular motoneuron innervation in the rhesus monkey. I: Muscle rotation axes and on-directions during fixation. Exp Brain Res 126: 187-199, 1999.
102. Tweed D. Three-dimensional model of the human eye-head saccadic system. J Neurophysiol 77: 654-666, 1997.
103. Tweed DB and Vilis T. Implications of rotational kinematics for the oculomotor system in three dimensions. J Neurophysiol 58: 832-849, 1987.
104. Tweed DB and Vilis T. The superior colliculus and the spatiotemporal translation in the saccadic system. Neural Networks 3: 75-86, 1990a.
105. Tweed DB and Vilis T. Geometric relations of eye position and velocity vectors during saccades. Vision Res 30: 111-127, 1990b.
106. Umeno MM and Goldberg ME. Spatial processing in the monkey frontal eye field. I. Predictive visual responses. J Neurophysiol 78: 1373-1383, 1997.
107. Van Gisbergen JA, Robinson DA, and Gielen S. A quantitative analysis of generation of saccadic eye movements by burst neurons. J Neurophysiol 3: 417-442, 1981.
108. Van Gisberger JAM, Van Opstal AJ, and Tax AAM. Collicular ensemble coding of saccades based on vector summation. Neuroscience 21: 541-555, 1987.
109. Van Opstal AJ, Hepp K, Hess BJ, Straumann D, and Henn V. Two-rather than three-dimensional representation of saccades in monkey superior colliculus. Science 252: 1313-1315, 1991.
110. Van Opstal AJ, Hepp K, Suzuki Y, and Henn V. Influence of eye position on activity in monkey superior colliculus. J Neurophysiol 74: 1593-1610, 1995.
111. Van Opstal AJ, Hepp K, Suzuki Y, and Henn V. Role of monkey nucleus reticularis tegmenti pontis in the stabilization of Listing's plane. J Neurosci 16: 7284-7296, 1996.
112. Vilis T, Yates S, and Hore J. Visual patching of one eye produces changes in saccadic properties in the unseeing eye. Brain Res 349: 290-292, 1985.
113. Waitzman DM, Ma TP, Optican LM, and Wurtz RH. Superior colliculus neurons mediate the dynamic characteristics of saccades. J Neurophysiol 66: 1716-1737, 1991.
114. Walker MF, FitzGibbon EJ, and Goldberg ME. Neurons in the monkey superior colliculus predict the result of impending saccadic eye movements. J Neurophysiol 73: 1988-2003, 1995.
115. Westheimer G. Kinematics of the eye. J Opt Soc Am 47: 967-974, 1957.
116. Westheimer G and Blair SM. Oculomotor defects in cerebellectomized monkeys. Invest Ophthalmol 12: 618, 1973.
117. White RL III and Snyder LH. A neural network model of flexible spatial updating. J Neurophysiol 91: 1608-1619, 2004.
118. Wurtz RH and Albano JE. Visual-motor function of the primate superior colliculus. Anna Rev Neurosci 3: 189-226, 1980.
119. Xing J and Andersen RA. Memory activity of LIP neurons for sequential eye movements simulated with neural networks. J Neurophysiol 84: 651-665, 2000a.
120. Xing J and Andersen RA. Models of the posterior parietal cortex which perform multimodal integration and represent space in several coordinate frames. J Cogn Neurosci 12: 601-614, 2000b.
121. Zee DS, Optican LM, Cook JD, Robinson DA, and Engel WK. Slow saccades in spinocerebellar degeneration. Arch Neurol 33: 243-251, 1976.
122. Zipser D and Andersen RA. A back-propagation programmed network that simulates response properties of a subset of posterior parietal neurons. Nature 331: 679-684, 1988.