Electrical stimulation of the supplementary eye fields in the head-free macaque evokes kinematically normal gaze shifts

Journal of Neurophysiology

Volumn 89, Issue 6, 2003, Pages 2961-2974

  Martinez Trujillo, Julio C ^a   Wang, Hongying ^a   Crawford, J Douglas ^a  

^a YORK UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; ELECTROSTIMULATION; EYE MOVEMENT CONTROL; FRONTAL CORTEX; GAZE; HEAD MOVEMENT; KINEMATICS; MACACA; NERVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; SACCADIC EYE MOVEMENT; SUPPLEMENTARY EYE FIELD; VISUOMOTOR COORDINATION;

ANIMALS; BIOMECHANICS; ELECTRIC STIMULATION; EYE MOVEMENTS; FRONTAL LOBE; HEAD MOVEMENTS; MACACA MULATTA; ORIENTATION; PSYCHOMOTOR PERFORMANCE; ROTATION;

EID: 0038617819     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.01065.2002     Document Type: Article

References (70)

1. Balliet R and Nakayama K. Training of voluntary torsion. Invest Ophthalmol Vis Sci 17: 303-314, 1978.
2. Bon L and Lucchetti C. The dorsomedial frontal cortex of the macaque monkey: fixation and saccade-related activity. Exp Brain Res 89: 571-580, 1992.
3. Bon L and Lucchetti C. Attention-related neurons in the supplementary eye field of the macaque monkey. Exp Brain Res 113: 180-185, 1997.
4. Ceylan M, Henriques DY, Tweed DB, and Crawford JD. Task-dependent constraints in motor control: pinhole goggles make the head move like an eye. J Neurosci 20: 2719-2730, 2000.
5. Chen LL and Sparks DL. Supplementary eye field contribution to gaze shifts studied by electrical microstimulation in head-free monkeys. Neural Control Move Abstr D11, 2001.
6. Chen LL and Wise SP. Supplementary eye field contrasted with the frontal eye field during acquisition of conditional oculomotor associations. J Neurophysiol 73: 1122-1134, 1995a.
7. Chen LL and Wise SP. Neuronal activity in the supplementary eye field during acquisition of conditional oculomotor associations. J Neurophysiol 73: 1101-1121, 1995b.
8. Coe B, Tomihara K, Matsuzawa M, and Hikosaka O. Visual and anticipatory bias in three cortical eye fields of the monkey during an adaptive decision-making task. J Neurosci 22: 5081-5090, 2002.
9. Constantin AG, Wang H, Klier EM, and Crawford JD. Context dependent adaptation of eye-head coordination in gaze saccades evoked by superior colliculus stimulation. Socr Neurosci Abstr 26: 1992, 2000.
10. 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.
11. Crawford JD, Ceylan MZ, Klier EM, and Guitton D. Three-dimensional eye-head coordination during gaze saccades in the primate. J Neurophysiol 81: 1760-1782, 1999.
12. Crawford JD and Guitton D. Primate head-free saccade generator implements a desired (post-VOR) eye position command by anticipating intended head motion. J Neurophysiol 78: 2811-2816, 1997.
13. Crawford JD and Vilis T. Axes of eye rotation and Listing's law during rotations of the head. J Neurophysiol 65: 407-423, 1991.
14. Donders FC. Beitrag sur Lehre von den Bewegungen des menschlichen Auges. Holland Beitr Anat Physiol Wiss 1: 105-145, 1848.
15. Ferman L, Collewijn H, and Van den Berg AV. A direct test of Listing's law. II. Human ocular torsion measured under dynamic conditions. Vision Res 27: 939-951, 1987a.
16. 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, 1987b.
17. Freedman EG and Sparks DL. Eye-head coordination during head-unrestrained gaze shifts in rhesus monkeys. J Neurophysiol 77: 2328-2348, 1997.
18. Freedman EG, Stanford TR, and Sparks DL. Combined eye-head gaze shifts produced by electrical stimulation of the superior colliculus in rhesus monkeys. J Neurophysiol 76: 927-952, 1996.
19. Fuller JH. Head movement propensity. Exp Brain Res 92: 152-164, 1992.
20. Fuller JH. Comparison of horizontal head movements evoked by auditory and visual targets. J Vestib Res 6: 1-13, 1996.
21. Fujii N, Mushiake H, Tamai M, and Tanji J. Microstimulation of the supplementary eye field during saccade preparation. Neuroreport 6: 2565-2568, 1995.
22. Gandhi NJ and Sparks DL. Experimental control of eye and head positions prior to head unrestrained gaze shifts in monkey. Vision Res 41: 3243-3254, 2001.
23. Gandolfo F, Li C, Benda BJ, Schioppa CP, and Bizzi E. Cortical correlates of learning in monkeys adapting to a new dynamical environment. Proc Natl Acad Sci USA 97: 2259-2263, 2000.
24. Georgopoulos AP. Neural aspects of cognitive motor control. Curr Opin Neurobiol 10: 238-241, 2000.
25. Glenn B and Vilis T. Violations of Listing's law after large eye and head gaze shifts. J Neurophysiol 68: 309-318, 1992.
26. Guillaume A and Pelisson D. Gaze shifts evoked by electrical stimulation of the superior colliculus in the head-unrestrained cat. II. Effect of muscimol inactivation of the caudal fastigial nucleus. Eur J Neurosci 14: 1345-1359, 2001a.
27. Guillaume A and Pelisson D. Gaze shifts evoked by electrical stimulation of the superior colliculus in the head-unrestrained cat. I. Effect of the locus and of the parameters of stimulation. Eur J Neurosci 14: 1331-1344, 2001b.
28. Guitton D. Control of eye-head coordination during orienting gaze shifts. Trends Neurosci 15:174-179, 1992.
29. Helmholtz H. Treatise of Physiological Optics [English translation], translated by Southall JPC. Rochester, NY: Opt Soc Am, 1867.
30. Kermadi I, Liu Y, Tempini A, Calciati E, and Rouiller EM. Neuronal activity in the primate supplementary motor area and the primary motor cortex in relation to spatio-temporal bimanual coordination. Somatosens Mot Res 15: 287-308, 1998.
31. Klier EM, Wang H, Constantin AG, and Crawford JD. Midbrain control of three-dimensional head orientation. Science 295: 1314-1316, 2002a.
32. Klier EM, Wang H, and Crawford JD. The superior colliculus encodes gaze commands in retinal coordinates. Nat Neurosci 4: 627-632, 2001.
33. Klier EM, Wang H, and Crawford JD. Neural mechanisms of three-dimensional eye and head movements. Ann NY Acad Sci 956: 512-514, 2002b.
34. Levinsohn G. Uber die Bezihehungen der Grosshirnrinde beim Affen zu den Bewegungen des Auges. Graefe Arch Ophthalmol 71: 313-378, 1909.
35. Li CS, Padoa-Schioppa C, and Bizzi E. Neuronal correlates of motor performance and motor learning in the primary motor cortex of monkeys adapting to an external force field. Neuron 30: 593-607, 2001.
36. Lu X, Matsuzawa M, and Hikosaka O. A neural correlate of oculomotor sequences in supplementary eye field. Neuron 34: 317-325, 2002.
37. Marotta JJ, Medendorp WP, and Crawford JD. Contribution of the upper and lower arm to grasp orientation. Soc Neurosci Abstr 268.8, 2002.
38. Martinez-Trujillo JC, Klier EM, Wang H, and Crawford JD. Gaze shifts evoked by electrical stimulation of the SEF in the macaque monkey. Soc Neurosci Abstr 11.9, 2002.
39. Medendorp WO, Melis BJM, Gielen CCAM, and Van Gisbergen JAM. Off-centric rotation axis in natural head movements: implications for vestibular reafference and kinematics redundancy. J Neurophysiol 79: 2025-2039, 1998.
40. Missal M and Heinen SJ. Facilitation of smooth pursuit initiation by electrical stimulation in the supplementary eye fields. J Neurophysiol 86: 2413-2425, 2001.
41. Misslisch H, Tweed D, and Vilis T. Neural constraints on eye motion in human eye-head saccades. J Neurophysiol 79: 859-869, 1998.
42. Mitz AR and Godschalk M. Eye-movement representation in the frontal lobe of rhesus monkeys. Neurosci Lett 106: 157-162, 1989.
43. Olson CR and Gettner SN. Macaque SEF neurons encode object-centered directions of eye movements regardless of the visual attributes of instructional cues. J Neurophysiol 81: 2340-2346, 1999.
44. Olson CR and Tremblay L. Macaque supplementary eye field neurons encode object-centered locations relative to both continuous and discontinuous objects. J Neurophysiol 83: 2392-2411, 2000.
45. Pelisson D, Guitton D, and Munoz DP. Compensatory eye and head movements generated by the cat following stimulation-induced perturbations in gaze position. Exp Brain Res 78: 654-658, 1989.
46. Radau P, Tweed D, and Vilis T. Three dimensional eye, head and chest orientation after large gaze shifts and the underlying neural strategies. J Neurophysiol 72: 2840-2852, 1994.
47. Robinson FR and Fuchs AF. The role of the cerebellum in voluntary eye movements. Annu Rev Neurosci 24: 981-1004, 2001.
48. Roucoux A, Guitton D, and Crommelinck M. Stimulation of the superior colliculus in the alert cat. II. Eye and head movements evoked when the head is unrestrained. Exp Brain Res 39: 75-85. 1980.
49. Russo GS and Bruce CJ. Effect of eye position within the orbit on electrically elicited saccadic eye movements: a comparison of the macaque monkey's frontal and supplementary eye fields J Neurophysiol 69: 800-818, 1993.
50. 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.
51. 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.
52. Schall JD. Neuronal activity related to visually guided saccades in the frontal eye fields of rhesus monkeys: comparison with supplementary eye fields. J Neurophysiol 66: 559-579, 1991.
53. Schiller PH and Tehovnik EJ. Look and see: how the brain moves your eyes about. Prog Brain Res 134: 127-142, 2001.
54. Schlag JD. Neurons that program what to do and in what order. Neuron 34: 177-178, 2002.
55. Schlag J and Schlag-Rey M. Evidence for a supplementary eye field. J Neurophysiol 57: 179-200, 1987.
56. Segraves MA. Activity of monkey frontal eye field neurons projecting to oculomotor regions of the pons. J Neurophysiol 68: 1967-1985, 1992.
57. Shook BL, Schlag-Rey M, and Schlag J. Primate supplementary eye field. I. Comparative aspects of mesencephalic and pontine connections. J Comp Neurol 301: 618-642, 1990.
58. Sparks DL, Barton EJ, Gandhi NJ, and Nelson J. Studies of the role of the paramedian pontine reticular formation in the control of head-restrained and head-unrestrained gaze shifts. Ann NY Acad Sci 956: 85-98, 2002.
59. Sparks DL, Freedman DG, Chen LL, and Gandhi NJ. Cortical and subcortical contributions to coordinated eye and head movements. Vision Res 41: 3295-3305, 2001.
60. Stahl JS. Eye-head coordination and the variation of eye-movement accuracy with orbital eccentricity. Exp Brain Res 136: 200-210, 2001.
61. Tehovnik EJ, Lee K, and Schiller PH. Stimulation-evoked saccades from the dorsomedial frontal cortex of the rhesus monkey following lesions of the frontal eye fields and superior colliculus. Exp Brain Res 98: 179-190, 1994.
62. Tehovnik EJ, Slocum WM, Tolias AS, and Schiller PH. Saccades induced electrically from the dorsomedial frontal cortex: evidence for a head-centered representation. Brain Res 795: 287-291, 1998.
63. Tehovnik EJ, Slocum WM, and Schiller PH. Behavioural conditions affecting saccadic eye movements elicited electrically from the frontal lobes of primates. Eur J Neurosci 11: 2431-2443, 1999.
64. Theeuven M, Miller LE, and Gielen CCAM. Is the orientation of head and arm coupled during pointing movements? J Mot Behav 24: 242-250, 1993.
65. Tomlinson RD and Bahra PS. Combined eye-head gaze shifts in the primate. 1. Metrics. J Neurophysiol 56: 1542-1557, 1986.
66. Tremblay L, Gettner SN, and Olson CR. Neurons with object-centered spatial selectivity in macaque SEF: do they represent locations or rules? J Neurophysiol 87: 333-350, 2002.
67. Tweed D. Three-dimensional model of the human eye-head saccadic system. J Neurophysiol 77: 654-666, 1997.
68. 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.
69. Tweed D and Vilis T. Geometric relations of eye positions and velocity vectors during saccades. Vision Res 30: 111-127, 1990.
70. Tu TA and Keating EG. Electrical stimulation of the frontal eye field in a monkey produces combined eye and head movements. J Neurophysiol 84: 1103-1106, 2000.