Horizontal smooth pursuit adaptation in macaques after muscimol inactivation of the dorsolateral pontine nucleus (DLPN)

Journal of Neurophysiology

Volumn 98, Issue 5, 2007, Pages 2918-2932

  Ono, Seiji ^a   Mustari, Michael J ^a,b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUSCIMOL;

ADOLESCENT; ANIMAL EXPERIMENT; ARTICLE; CEREBELLUM; CONTROLLED STUDY; MICROINJECTION; NERVE CELL; NONHUMAN; OCULOMOTOR NUCLEUS; PONS ANGLE; PRIORITY JOURNAL; RHESUS MONKEY; SMOOTH PURSUIT EYE MOVEMENT; STATISTICAL SIGNIFICANCE; STEADY STATE; STUDENT T TEST; VISION; VISUAL ADAPTATION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; FUNCTIONAL LATERALITY; GABA AGONISTS; MACACA MULATTA; MUSCIMOL; PHOTIC STIMULATION; PONS; PURSUIT, SMOOTH; TIME FACTORS;

EID: 36248932611     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00115.2007     Document Type: Article

References (71)

1. Akao T, Mustari MJ, Fukushima J, Kurkin S, Fukushima K. Discharge characteristics of pursuit neurons in MST during vergence eye movements. J Neurophysiol 93: 2415-2434, 2005.
2. Albus JS. A theory of cerebellar function. Math Biosci 10: 25-61, 1971.
3. Arikan R, Blake NM, Erinjeri JP, Woolsey TA, Giraud L, Highstein SM. A method to measure the effective spread of focally injected muscimol into the central nervous system with electrophysiology and light microscopy. J Neurosci Methods 118: 51-57, 2002.
4. Brodal P. The pontocerebellar projection in the rhesus monkey: an experimental study with retrograde axonal transport of horseradish peroxidase. Neuroscience 4: 193-208, 1979.
5. Brodal P. Further observations on the cerebellar projections from the pontine nuclei and the nucleus reticularis tegmenti pontis in the rhesus monkey. J Comp Neurol 204: 44-55, 1982.
6. Büttner U, Büttner-Ennever JA. Present concepts of oculomotor organization. Prog Brain Res 151: 1-42, 2006.
7. Büttner-Ennever JA, Cohen B, Horn AK, Reisine H. Efferent pathways of the nucleus of the optic tract in monkey and their role in eye movements. J Comp Neurol 373: 90-107, 1996.
8. Carey MR, Medina JF, Lisberger SG. Instructive signals for motor learning from visual cortical area MT. Nat Neurosci 8: 813-819, 2005.
9. Chou IH, Lisberger SG. The role of the frontal pursuit area in learning in smooth pursuit eye movements. J Neurosci 24: 4124-4133, 2004.
10. Das VE, Economides JR, Ono S, Mustari MJ. Information processing by parafoveal cells in the primate nucleus of the optic tract. Exp Brain Res 140: 301-310, 2001.
11. Dicke PW, Barash S, Ilg UJ, Thier P. Single-neuron evidence for a contribution of the dorsal pontine nuclei to both types of target-directed eye movements, saccades and smooth-pursuit. Eur J Neurosci 19: 609-624, 2004.
12. Distler C, Mustari MJ, Hoffmann KP. Cortical projections to the nucleus of the optic tract and dorsal terminal nucleus and to the dorsolateral pontine nucleus in macaques: a dual retrograde tracing study. J Comp Neurol 444: 144-158, 2002.
13. Fuchs AF, Robinson DA. A method for measuring horizontal and vertical eye movement chronically in the monkey. J Appl Physiol 21: 1068-1070, 1966.
14. Fukushima K. Frontal cortical control of smooth-pursuit. Curr Opin Neurobiol 13: 647-654, 2003.
15. Fukushima K, Tanaka M, Suzuki Y, Fukushima J, Yoshida T. Adaptive changes in human smooth pursuit eye movement. Neurosci Res 25: 391-398, 1996.
16. Gamlin PD. The pretectum: connection and oculomotor-related roles. Prog Brain Res 151: 379-405, 2006.
17. Giolli RA, Blanks RH, Lui F. The accessory optic system: basic organization with an update on connectivity, neurochemistry, and function. Prog Brain Res 151: 407-440, 2006.
18. Giolli RA, Gregory KM, Suzuki DA, Blanks RH, Lui F, Betelak KF. Cortical and subcortical afferents to the nucleus reticularis tegmenti pontis and basal pontine nuclei in the macaque monkey. Vis Neurosci 18: 725-740, 2001.
19. Glickstein M, Cohen JL, Dixon B, Gibson A, Hollins M, Labossiere E, Robinson F. Corticopontine visual projections in macaque monkeys. J Comp Neurol 190: 209-229, 1980.
20. Glickstein M, Gerrits N, Kralj-Hans I, Mercier B, Stein J, Voogd J. Visual pontocerebellar projections in the macaque. J Comp Neurol 349: 51-72, 1994.
21. Gottlieb JP, MacAvoy MG, Bruce CJ. Neural responses related to smooth-pursuit eye movements and their correspondence with electrically elicited smooth eye movements in the primate frontal eye field. J Neurophysiol 72: 1634-1653, 1994.
22. Hoffmann KP, Behrend K, Schoppmann A. A direct afferent visual pathway from the nucleus of the optic tract to the inferior olive in the cat. Brain Res 115: 150-153, 1976.
23. Hoffmann KP, Distler C, Ilg U. Callosal and superior temporal sulcus contributions to receptive field properties in the macaque monkey's nucleus of the optic tract and dorsal terminal nucleus of the accessory optic tract. J Comp Neurol 321: 150-162, 1992.
24. Ilg UJ, Schumann S, Thier P. Posterior parietal cortex neurons encode target motion in world-centered coordinates. Neuron 43: 145-151, 2004.
25. Ilg UJ, Thier P. Visual tracking neurons in primate area MST are activated by smooth-pursuit eye movements of an "imaginary" target. J Neurophysiol 90: 1489-1502, 2003.
26. Ito M. Neural design of the cerebellar motor control system. Brain Res 40: 81-84, 1972.
27. 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.
28. Kahlon M, Lisberger SG. Coordinate system for learning in the smooth pursuit eye movements of monkeys. J Neurosci 16: 7270-7283, 1996.
29. Kahlon M, Lisberger SG. Changes in the responses of Purkinje cells in the floccular complex of monkeys after motor learning in smooth pursuit eye movements. J Neurophysiol 84: 2945-2960, 2000.
30. Kawano K, Shidara M, Yamane S. Neural activity in dorsolateral pontine nucleus of alert monkey during ocular following responses. J Neurophysiol 67: 680-703, 1992.
31. Keating EG. Frontal eye field lesions impair predictive and visually-guided pursuit eye movements. Exp Brain Res 86: 311-323, 1991.
32. Kobayashi Y, Kawano K, Takemura A, Inoue Y, Kitama T, Gomi H, Kawato M. Temporal firing patterns of Purkinje cells in the cerebellar ventral paraflocculus during ocular following responses in monkeys. II. Complex spikes. J Neurophysiol 80: 832-848, 1998.
33. Komatsu H, Wurtz RH. Relation of cortical areas MT and MST to pursuit eye movements. III. Interaction with full-field visual stimulation. J Neurophysiol 60: 621-644, 1988.
34. Langer T, Fuchs AF, Scudder CA, Chubb MC. Afferents to the flocculus of the cerebellum in the rhesus macaque as revealed by retrograde transport of horseradish peroxidase. J Comp Neurol 235: 1-25, 1985.
35. Leigh RJ, Zee DS. The Neurology of Eye Movements (4th ed.). New York: Oxford Univ. Press, 2006.
36. Lisberger SG, Movshon JA. Visual motion analysis for pursuit eye movements in area MT of macaque monkeys. J Neurosci 19: 2224-2246, 1999.
37. Lynch JC, Tian JR. Cortico-cortical networks and cortico-subcortical loops for the higher control of eye movements. Prog Brain Res 151: 461-501, 2006.
38. Marr D. A theory of cerebellar cortex. J Physiol 202: 437-470, 1969.
39. Maunsell JH, Newsome WT. Visual processing in monkey extrastriate cortex. Annu Rev Neurosci 10: 363-401, 1987.
40. May JG, Andersen RA. Different patterns of corticopontine projections from separate cortical fields within the inferior parietal lobule and dorsal prelunate gyrus of the macaque. Exp Brain Res 63: 265-278, 1986.
41. May JG, Keller EL, Suzuki DA. Smooth-pursuit eye movement deficits with chemical lesions in the dorsolateral pontine nucleus of the monkey. J Neurophysiol 59: 952-977, 1988.
42. Missal M, Heinen SJ. Supplementary eye fields stimulation facilitates anticipatory pursuit. J Neurophysiol 92: 1257-1262, 2004.
43. Mustari MJ, Fuchs AF. Discharge patterns of neurons in the pretectal nucleus of the optic tract (NOT) in the behaving primate. J Neurophysiol 64: 77-90, 1990.
44. Mustari MJ, Fuchs AF, Kaneko CR, Robinson FR. Anatomical connections of the primate pretectal nucleus of the optic tract. J Comp Neurol 349: 111-128, 1994.
45. Mustari MJ, Fuchs AF, Pong M. Response properties of pretectal omnidirectional pause neurons in the behaving primate. J Neurophysiol 77: 116-125, 1997.
46. Mustari MJ, Fuchs AF, Wallman J. Response properties of dorsolateral pontine units during smooth pursuit in the rhesus macaque. J Neurophysiol 60: 664-686, 1988.
47. Mustari MJ, Ono S. The optokinetic system. In: New Encyclopedia of Neuroscience (4th ed.), edited by Squire LR. Amsterdam: Elsevier, 2007.
48. Mustari MJ, Ono S, Das VE, Tusa RJ. Role of the dorsolateral pontine nucleus in visual-vestibular behavior. Ann NY Acad Sci 1004: 196-205, 2003.
49. Mustari MJ, Tusa RJ, Burrows AF, Fuchs AF, Livingston CA. Gaze-stabilizing deficits and latent nystagmus in monkeys with early-onset visual deprivation: role of the pretectal NOT. J Neurophysiol 86: 662-675, 2001.
50. Nagao S, Kitamura T, Nakamura N, Hiramatsu T, Yamada J. Differences of the primate flocculus and ventral paraflocculus in the mossy and climbing fiber input organization. J Comp Neurol 382: 480-498, 1997.
51. Newsome WT, Wurtz RH, Komatsu H. Relation of cortical areas MT and MST to pursuit eye movements. II. Differentiation of retinal from extraretinal inputs. J Neurophysiol 60: 604-620, 1988.
52. Nyby O, Jansen J. An experimental investigation of the cortico-pontine projection in macaca mulatta. Norske Vid Akad Avh I Math Naturv 3: 31-47, 1951.
53. Ogawa T, Fujita M. Adaptive modifications of human postsaccadic pursuit eye movements induced by a step-ramp-ramp paradigm. Exp Brain Res 116: 83-96, 1997.
54. Ono S, Das VE, Economides JR, Mustari MJ. Modeling of smooth pursuit-related neuronal responses in the DLPN and NRTP of the rhesus macaque. J Neurophysiol 93: 108-116, 2005.
55. Ono S, Das VE, Mustari MJ. Role of the dorsolateral pontine nucleus in short-term adaptation of the horizontal vestibuloocular reflex. J Neurophysiol 89: 2879-2885, 2003.
56. Ono S, Das VE, Mustari MJ. Gaze-related response properties of DLPN and NRTP neurons in the rhesus macaque. J Neurophysiol 91: 2484-2500, 2004.
57. Ono S, Mustari MJ. Extraretinal signals in MSTd neurons related to volitional smooth pursuit. J Neurophysiol 96: 2819-2825, 2006.
58. Rashbass C. The relationship between saccadic and smooth tracking eye movements. J Physiol 159: 326-338, 1961.
59. Raymond JL, Lisberger SG. Neural learning rules for the vestibulo-ocular reflex. J Neurosci 18: 9112-9129, 1998.
60. Robinson FR, Straube A, Fuchs AF. Participation of caudal fastigial nucleus in smooth pursuit eye movements. II. Effects of muscimol inactivation. J Neurophysiol 78: 848-859, 1997.
61. Stewart CM, Mustari MJ, Perachio AA. Visual-vestibular interactions during vestibular compensation: role of the pretectal NOT in horizontal VOR recovery after hemilabyrinthectomy in rhesus monkey. J Neurophysiol 94: 2653-2666, 2005.
62. Stone LS, Lisberger SG. Visual responses of Purkinje cells in the cerebellar flocculus during smooth-pursuit eye movements in monkeys. II. Complex spikes. J Neurophysiol 63: 1262-1275, 1990.
63. Suzuki DA, Keller EL. Visual signals in the dorsolateral pontine nucleus of the alert monkey: their relationship to smooth-pursuit eye movements. Exp Brain Res 53: 473-478, 1984.
64. Suzuki DA, May JG, Keller EL, Yee RD. Visual motion response properties of neurons in dorsolateral pontine nucleus of alert monkey. J Neurophysiol 63: 37-59, 1990.
65. Suzuki DA, Yamada T, Yee RD. Smooth-pursuit eye-movement-related neuronal activity in macaque nucleus reticularis tegmenti pontis. J Neurophysiol 89: 2146-2158, 2003.
66. Takagi M, Zee DS, Tamargo RJ. Effects of lesions of the oculomotor cerebellar vermis on eye movements in primate: smooth pursuit. J Neurophysiol 83: 2047-2062, 2000.
67. Thielert CD, Thier P. Patterns of projections from the pontine nuclei and the nucleus reticularis tegmenti pontis to the posterior vermis in the rhesus monkey: a study using retrograde tracers. J Comp Neurol 337: 113-126, 1993.
68. Thier P, Koehler W, Buettner UW. Neuronal activity in the dorsolateral pontine nucleus of the alert monkey modulated by visual stimuli and eye movements. Exp Brain Res 70: 496-512, 1988.
69. Thier P, Möck M. The oculomotor role of the pontine nuclei and the nucleus reticularis tegmenti pontis. Prog Brain Res 151: 293-320, 2006.
70. Tusa RJ, Ungerleider LG. Fiber pathways of cortical areas mediating smooth pursuit eye movements in monkeys. Ann Neurol 23: 174-183, 1988.
71. Yakushin SB, Reisine H, Büttner-Ennever J, Raphan T, Cohen B. Functions of the nucleus of the optic tract (NOT). I. Adaptation of the gain of the horizontal vestibulo-ocular reflex. Exp Brain Res 131: 416-432, 2000.