Comparison of the discharge characteristics of brain stem omnipause neurons and superior colliculus fixation neurons in monkey: Implications for control of fixation and saccade behavior

Journal of Neurophysiology

Volumn 79, Issue 2, 1998, Pages 511-528

  Everling, Stefan ^a   Paré, Martin ^a,b   Dorris, Michael C ^a   Munoz, Douglas P ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b NATIONAL EYE INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN STEM; ELECTROSTIMULATION; EYE FIXATION; HYPOTHESIS; MONKEY; NERVE CELL MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; SACCADIC EYE MOVEMENT; SUPERIOR COLLICULUS;

EID: 0031905704     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1998.79.2.511     Document Type: Article

References (83)

1. BECKER, W., KING, W. M., FUCHS, A. F., JÜRGENS, R., JOHANSON, G., AND KORNHUBER, H. H. Accuracy of goal-directed saccades and mechanisms of error correction. In: Progress in Oculomotor Research, Developments in Neuroscience, edited by A. F. Fuchs and W. Becker. Amsterdam: Elsevier, 1981, p. 29-37.
2. BON, L. AND LUCCHETTI, C. The dorsomedial frontal cortex of the maccaca monkey: fixation and saccade-related activity. Exp. Brain Res. 89: 571-580, 1992.
3. BRUCE C. J. AND GOLDBERG M. E. Primate frontal eye fields. I. Single neurons discharging before saccades. J. Neurophysiol. 53: 603-635, 1985.
4. BÜTTNER-ENNEVER, J. A. AND BÜTTNER, U. A cell group associated with vertical eye movements in the rostral mesencephalic reticular formation of the monkey. Brain Res. 151: 31-47, 1978.
5. BÜTTNER-ENNEVER, J. A., COHEN, B., PAUSE, M., AND FRIES W. Raphe nucleus of the pons containing omnipause neurons of the oculomotor system in the monkey, and its homologue in man. J. Comp. Neurol. 267: 307-321, 1988.
6. BÜTTNER-ENNEVER, J. A. AND HORN, A.K.E. Neuroanatomy of the saccadic omnipause neurons in the nucleus raphe interpositus. In: Contemporary Ocular Motor and Vestibular Research: A Tribute to David A. Robinson, edited by A. F. Fuchs, T. Brandt, U. Büttner, and D. S. Zee. Stuttgart, Germany: Thieme, 1995, p. 488-495.
7. BÜTTNER-ENNEVER, J. A., HORN, A.K.E., AND HENN, V. Differential projections from rostral and caudal superior colliculus to the horizontal saccadic premotor and omnipause neurons in pons of the primate. Soc. Neurosci. Abstr. 23: 1296, 1997.
8. BURMAN, D. D. AND BRUCE, C. J. Suppression of task-related saccades by electrical stimulation in the primate's frontal eye field. J. Neurophysiol. 77: 2252-2267, 1997.
9. CHRIST, C. F., YAMASAKI, D.S.G., KOMATSU, H., AND WURTZ, R. H. A grid system and a microsyringe for single cell recording. J. Neurosci. Methods 26: 117-122, 1988.
10. COHEN, B. AND HENN, V. Unit activity in the pontine reticular formation associated with eye movements. Brain Res. 46: 403-410, 1972.
11. CURTHOYS, I. S., MARKHAM, C. H., AND 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.
12. DIAS, E. C. AND BRUCE, C. J. Physiological correlate of fixation disengagement in the primate's frontal eye field. J. Neurophysiol. 72: 2532-2537, 1994.
13. DORRIS, M. C. AND MUNOZ, D. P. A neural correlate for the gap effect on saccadic reaction times in monkey. J. Neurophysiol. 73: 2558-2562, 1995.
14. DORRIS, M. C., PARÉ, M., AND MUNOZ, D. P. Neuronal activity in monkey superior colliculus related to the initiation of saccadic eye movements. J. Neurosci. 17: 8566-8579, 1997.
15. EDELMAN, J. A. AND KELLER, E. L. Activity of visuomotor burst neurons in the superior colliculus accompanying express saccades. J. Neurophysiol. 76: 908-926, 1996.
16. EVERLING, S., PARÉ, M., DORRIS, M. C., AND MUNOZ, D. P. Visual fixation and motor preparation signals related to saccadic reaction times in monkey. II. Paramedian pontine reticular formation (Abstract). Can. J. Physiol. Pharmacol. 75: Aviii, 1997a.
17. EVERLING, S., PARÉ, M., DORRIS, M. C., AND MUNOZ, D. P. Comparison of activity of superior colliculus fixation neurons and brainstem omnipause neurons in the gap saccade task. Soc. Neurosci. Abstr. 23: 1296, 1997b.
18. EVINGER, C., KANEKO, C.R.S., AND FUCHS, A. F. Activity of omnipause neurons in alert cats during saccadic eye movements and visual stimuli. J. Neurophysiol. 47: 827-844, 1982.
19. FISCHER, B. AND BOCH, R. Saccadic eye movements after extremely short reaction times in the monkey. Brain Res. 260: 21-26, 1983.
20. FUCHS, A. F., KANEKO, C.R.S., AND SCUDDER, C. A. Brainstem control of saccadic eye movements. Annu. Rev. Neurosci. 8: 307-3037, 1985.
21. FUCHS, A. F., LING, L., KANEKO, C.R.S., KING, W. M., AND USHER, S. D. The timing of the response of brainstem omni-pause neurons relative to saccadic eye movements in rhesus monkeys. Soc. Neurosci. Abstr. 17: 462, 1991.
22. FUCHS, A. F. AND ROBINSON, D. A. A method for measuring horizontal and vertical eye movement chronically in the monkey. J. Appl. Physiol. 21: 1068-1070, 1966.
23. FURUYA, N. AND MARKHAM, C. H. Direct inhibitory synaptic linkage of pause neurons with burst inhibitory neurons. Brain Res. 245: 139-143, 1982.
24. GANDHI, N. J. AND KELLER, E. L. Activity during interrupted saccades of rostral superior colliculus neurons projecting to the omnipause region. Soc. Neurosci. Abstr. 22: 579.5, 1996.
25. GONZALO-RUIZ, A., LECHNITZ, G. R., AND SMITH, D. J. Origin of cerebellar projections to the region of the oculomotor complex, medial pontine reticular formation, and superior colliculus in new world monkeys: a retrograde horseradish peroxidase study. J. Comp. Neurol. 174: 607-630, 1988.
26. HANES, D. P. AND SCHALL, J. D. Neural control of voluntary movement initiation. Science 274: 427-430, 1996.
27. HAYS, A. V., RICHMOND, B. J., AND OPTICAN, L. M. A Unix-based multiple process system for real-time data acquisition and control. W ESCON Conf. Proc. 2: 1-10, 1982.
28. HENN, V., BALOH, R. W., AND HEPP, K. The sleep-wake transition in the oculomotor system. Exp. Brain Res. 54: 166-176, 1984.
29. HIKOSAKA, O. AND WURTZ, R. H. Visual and oculomotor functions of monkey substantia nigra pars reticulata. II. Visual responses related to fixation of gaze. J. Neurophysiol. 49: 1254-1267, 1983.
30. HORN, A. K., BÜTTNER-ENNEVER, J. A., WÄHLE, P., AND REICHENBERGER, I. Neurotransmitter profile of saccadic omnipause neurons in nucleus raphe interpositus. J. Neurosci. 14: 2032-2046, 1994.
31. ISTVAN, P. J., DORRIS, M. C., AND MUNOZ, D. P. Functional identification of neurons in the monkey superior colliculus projecting to the paramedian pontine reticular formation. Soc. Neurosci. Abstr. 20: 141, 1994.
32. ITO, J., MARKHAM, C. H., AND CURTHOYS, I. S. Projections to eye movement-related pause neuron region in cat using HRP. Exp. Brain Res. 86: 94-104, 1984.
33. KANEKO, C.R.S. Effects of ibotenic acid lesions of the omnipause neurons on saccadic eye movements in rhesus macaques. J. Neurophysiol. 75: 2229-2242, 1996.
34. KANEKO, C.R.S. AND FUCHS, A. F. Connections of cat omnipause neurons. Brain Res. 241: 166-170, 1982.
35. KAWAGOE, R., TAKIKAWA, Y., MIYASHITA, N., AND HIKOSAKA, O. Dynamics of saccade burst neurons in the basal interstitial nucleus in the monkey cerebellum. Soc. Neurosci. Abstr. 12: 433.3, 1996.
36. KELLER, E. Participation of the medial pontine reticular formation in eye movement generation in the monkey. J. Neurophysiol. 37: 316-332, 1974.
37. KELLER, E. L. Control of saccadic eye movements by midline brain stem neurons. In: Control of Gaze by Brain Stem Neurons, edited by R. Baker and A. Berthoz. Amsterdam: Elsevier, 1977, p. 327-336.
38. KING, W. M. AND FUCHS, A. F. Neuronal activity in the mesencephalon related to vertical eye movements. In: Control of Gaze by Brain Stem Neurons, edited by R. Baker and A. Berthoz. Amsterdam: Elsevier, 1977, p. 319-326.
39. KING, W. M., PRECHT, W., AND DIERINGER, N. Afferent and efferent connections of cat omnipause neurons. Exp. Brain Res. 38: 395-403, 1980.
40. LANGER, T. P. Basal interstitial nucleus of the cerebellum: cerebellar nucleus related to the flocculus. J. Comp. Neurol 235: 38-47, 1985.
41. LANGER, T. P. AND KANEKO, C.R.S. Efferent projections of the cat oculomotor reticular omnipause neuron region: an autoradiographic study. J. Comp. Neurol. 217: 288-306, 1983.
42. LANGER, T. P. AND KANEKO, C.R.S. Brainstem afferents to the omnipause region in the cat: a horseradish peroxidase study. J. Comp. Neurol. 230: 444-458, 1984.
43. LANGER, T. P. AND KANEKO, C.R.S. Brainstem afferents to the oculomotor omnipause neurons in monkey. J. Comp. Neurol. 295: 413-427, 1990.
44. LEE, K. AND TEHOVNIK, E. J. Topographic distribution of fixation-related units in the dorsomedial frontal cortex of the rhesus monkey. Eur. J. Neurosci. 7: 1005-1011, 1995.
45. LEICHNETZ, G. T., GONAZALO-RUIZ, A., DESALLES, A.A.F., AND HAYES, R. L. The origin of brainstem afferents of the paramedian pontine reticular formation in the cat. Brain Res. 422: 389-397, 1987.
46. LUSCHEI, E. S. AND FUCHS, A. F. Activity of brain stem neurons during eye movements of alert monkeys. J. Neurophysiol. 35: 445-461, 1972.
47. LYNCH, J. C., MOUNTCASTLE, V. B., TALBOT, W. H., AND YIN, T. C. Parietal lobe mechanisms for directed visual attention. J. Neurophysiol. 40: 362-389, 1977.
48. MA, T. P. Saccade-related omnivectoral pause neurons in the primate zona incerta. Neuroreport 7: 2713-2716, 1996.
49. MACPHERSON, J. M. AND ALDRIDGE, J. W. A quantitative method of computer analysis of spike train data collected from behaving animals. Brain Res. 175: 183-187, 1979.
50. MATSUMURA, M., KOJIMA, J., GARDINER, T. W., AND HIKOSAKA, O. Visual and oculomotor functions of monkey subthalamic nucleus. J. Neurophysiol. 67: 1615-1632, 1992.
51. MOSCHOVAKIS, A. K. AND HIGHSTEIN, S. M. The anatomy and physiology of primate neurons that control rapid eye movements. Annu. Rev. Neurosci. 17: 465-488, 1994.
52. MOSCHOVAKIS, A. K., KARABELAS, A. B., AND HIGHSTEIN, S. M. Structure-function relationships in the primate superior colliculus. I. Morphological classification of efferent neurons. J. Neurophysiol 60: 232-262, 1988a.
53. MOSCHOVAKIS, A. K., KARABELAS, A. B., AND HIGHSTEIN, S. M. Structure-function relationships in the primate superior colliculus. II. Morphological identity of presaccadic neurons. J. Neurophysiol 60: 263-302, 1988b.
54. MUNOZ, D. P. AND GUITTON, D. Fixation and orientation control by the tecto-reticulo-spinal system in the cat whose head is unrestrained. Rev. Neurol. (Paris) 145: 567-579, 1989.
55. MUNOZ, D. P. AND GUITTON, D. Control of orienting gaze shifts by the tectoreticulospinal system in the head-free cat. II. Sustained discharges during motor preparation and fixation. J. Neurophysiol. 66: 1624-1641, 1991.
56. MUNOZ, D. P. AND WURTZ, R. H. Role of rostral superior colliculus in active visual fixation and execution of express saccades. J. Neurophysiol. 67: 1000-1002, 1992.
57. MUNOZ, D. P. AND WURTZ, R. H. Fixation cells in monkey superior colliculus. I. Characteristics of cell discharge. J. Neurophysiol. 70: 559-575, 1993a.
58. MUNOZ, D. P. AND WURTZ, R. H. Fixation cells in monkey superior colliculus. II. Reversible activation and deactivation. J. Neurophysiol 70: 576-589, 1993b.
59. MUNOZ, D. P. AND WURTZ, R. H. Saccade-related activity in monkey superior colliculus. I. Characteristics of burst and buildup cells. J. Neurophysiol. 73: 2313-2333, 1995a.
60. MUNOZ, D. P. AND WURTZ, R. H. Saccade-related activity in monkey superior colliculus. II. Spread of activity during saccades. J. Neurophysiol. 73: 2334-2348, 1995b.
61. NAKAO, S., CURTHOYS, I., AND MARKHAM, C. Direct inhibitory projection of pause neurons to nystagmus-related pontomedullary reticular burst neurons in the cat. Exp. Brain Res. 40: 283-293, 1980.
62. NAKAO, S., SHFRAISHI, Y., ODA, H., AND INAGAKI, M. Direct inhibitory projection of pontine omnipause neurons to burst neurons in the Forel's field H controlling vertical eye movement-related motoneurons in the cat. Exp. Brain Res. 70: 632-636, 1988.
63. OHGAKI, T., MARKHAM, C. H., AND CURTHOYS, I. S. Anatomy of physiologically identified eye-movement-related pause neurons in the cat: pontomedullary region. J. Comp. Neurol. 266: 56-72, 1987.
64. OHGAKI, T., MARKHAM, C. H., SCHNEIDER, J. S., AND CURTHOYS, I. S. Anatomical evidence of the projection of pontine omnipause neurons to midbrain regions controlling vertical eye movements. J. Comp. Neurol. 289: 610-625, 1989.
65. OLIVIER, E., GRANTYN, A., CHAT, M., AND BERTHOZ, A. The control of slow orienting eye movements by tectoreticulospinal neurons in the cat: behavior, discharge patterns and underlying connections. Exp. Brain Res. 93: 435-449, 1993.
66. PARÉ, M. AND GUITTON, D. The fixation area of the cat superior colliculus: effects of electrical stimulation and direct connection with brainstem omnipause neurons. Exp. Brain Res. 101: 109-122, 1994.
67. PARÉ, M. AND MUNOZ, D. P. Saccadic reaction time in the monkey: advanced preparation of oculomotor programs is primarily responsible for express saccade occurrence. J. Neurophysiol. 76: 3666-3681, 1996.
68. PECK, C. K. Visual responses of neurones in cat superior colliculus in relation to fixation of targets. J. Physiol. (Lond.) 414: 301-315, 1989.
69. RAYBOURN, M. S. AND KELLER, E. Collculoreticular organization in primate oculomotor system. J. Neurophysiol. 40: 861-878, 1977.
70. RICHMOND, B. J. AND OPTICAN, L. M. Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. II. Quantification of response waveform. J. Neurophysiol. 57: 147-161, 1987.
71. SAKATA, H., SHIBUTANI, H., AND KAWANO, K. Spatial properties of visual fixation neurons in posterior parietal association cortex of the monkey. J. Neurophysiol. 43: 1654-1672, 1980.
72. SASLOW, M. G. Effects of components of displacement-step stimuli upon latency of saccadic eye movements. J. Opt. Soc. Am. 57: 1024-1029, 1967.
73. SCUDDER, C. A., MOSCHOVAKIS, A. K., KARABELAS, A. B., AND HIGHSTEIN, S. M. Anatomy and physiology of saccadic long-lead burst neurons recorded in the alert squirrel monkey. I. Descending projections from the mesencephalon. J. Neurophysiol. 76: 332-352, 1996.
74. SCHALL, J. D. Neuronal activity related to visually guided saccadic eye movements in the frontal eye fields of rhesus monkeys: comparison with supplementary eye fields. J. Neurophysiol. 66: 559-579, 1991.
75. SCHILLER, P. H., SANDEL, J. H., AND MAUNSELL J.H.R. The effect of frontal eye field and superior colliculus lesions on saccadic latencies in the rhesus monkey. J. Neurophysiol 57: 1033-1049, 1987.
76. SCHLAG, J. AND SCHLAG-REY, M. Visuomotor functions of central thalamus in monkey. II. Unit activity related to visual events, targeting, and fixation. J. Neurophysiol. 51: 1175-1195, 1984.
77. SCHLAG, J., SCHLAG-REY, M., AND PIGAREV, I. Supplementary eye field: influence of eye position on neural signals of fixation. Exp. Brain Res. 90: 302-306, 1992.
78. SEGRAVES, M. A. Activity of monkey frontal eye field neurons projecting to oculomotor regions in the pons. J. Neurophysiol. 68: 1967-1985, 1992.
79. SPARKS, D. L. Functional properties of neurons in the monkey superior colliculus: coupling of neuronal activity and saccade onset. Brain Res. 156: 1-16, 1978.
80. STANTON, G. B., GOLDBERG, M. E., AND BRUCE, C. J. Frontal eye field efferents in the macaque monkey. II. Topography of terminal fields in midbrain and pons. J. Comp. Neurol. 271: 493-506, 1988.
81. STRASSMAN, A., EVINGER, C., MCCREA, R. A., BAKER, R. G., AND HIGHSTEIN, S. M. Anatomy and physiology of intracellularly labeled omnipause neurons in the cat and squirrel monkey. Exp. Brain Res. 67: 436-440, 1987.
82. SUZUKI, H. AND AZUMA, M. Prefrontal neuronal activity during gazing at a light spot in the monkey. Brain Res. 126: 497-508, 1977.
83. WAITZMAN, D. M., MA, T. P., OPTICAN, L. M., AND WURTZ, R. H. Superior colliculus neurons mediate the dynamic characteristics of saccades. J. Neurophysiol. 66: 1716-1737, 1991.