Visual fixation as equilibrium: Evidence from superior colliculus inactivation

Journal of Neuroscience

Volumn 32, Issue 31, 2012, Pages 10627-10636

  Goffart, Laurent ^a   Hafed, Ziad M ^b   Krauzlis, Richard J ^c,d  

^a AIX MARSEILLE UNIVERSITÉ   (France)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^d NATIONAL EYE INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; EYE FIXATION; EYE POSITION; GAZE; MACACA MULATTA; MALE; NONHUMAN; OCULOGRAPHY; OCULOMOTOR SYSTEM; PRIORITY JOURNAL; SACCADIC EYE MOVEMENT; SUPERIOR COLLICULUS; VISUAL STIMULATION;

ACTION POTENTIALS; ANIMALS; BRAIN MAPPING; EYE MOVEMENTS; FIXATION, OCULAR; FUNCTIONAL LATERALITY; GABA-A RECEPTOR AGONISTS; MACACA MULATTA; MALE; MUSCIMOL; NEURONS; PATTERN RECOGNITION, VISUAL; PHOTIC STIMULATION; POSTURAL BALANCE; REACTION TIME; SUPERIOR COLLICULI;

EID: 84864422857     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0696-12.2012     Document Type: Article

References (72)

1. Aizawa H, Wurtz RH (1998) Reversible inactivation of monkey superior colliculus. I. Curvature of saccadic trajectory. J Neurophysiol 79:2082-2096.
2. Albano JE, Wurtz RH (1982) Deficits in eye position following ablation of monkey superior colliculus, pretectum, and posterior-medial thalamus. J Neurophysiol 48:318-337.
3. Basso MA, Krauzlis RJ, Wurtz RH (2000) Activation and inactivation of rostral superior colliculus neurons during smooth-pursuit eye movements in monkeys. J Neurophysiol 84:892-908.
4. Brainard DH (1997) The psychophysics toolbox. Spat Vis 10:433-436.
5. Büttner-Ennever JA, Horn AK, Henn V, Cohen B (1999) Projections from the superior colliculus motor map to omnipause neurons in monkey. J Comp Neurol 413:55-67.
6. Carello CD, Krauzlis RJ (2004) Manipulating intent: evidence for a causal role of the superior colliculus in target selection. Neuron 43:575-583.
7. Cavanaugh J, Wurtz RH (2004) Subcortical modulation of attention counters change blindness. J Neurosci 24:11236-11243.
8. Chen LL, Goffart L, Sparks DL (2001) A simple method for constructing microinjectrodes for reversible inactivation in behaving monkeys. J Neu-rosci Methods 107:81-85.
9. Dias EC, Segraves MA (1999) Muscimol-induced inactivation of monkey frontal eye field: effects on visually and memory-guided saccades. J Neu-rophysiol 81:2191-2214.
10. Dorris MC, Munoz DP (1995) A neural correlate for the gap effect on sac-cadic reaction times in monkey. J Neurophysiol 73:2558-2562.
11. Everling S, Paré M, Dorris MC, Munoz DP (1998) Comparison of the discharge characteristics of brain stem omnipause neurons and superior colliculus fixation neurons inmonkey: implications for controloffixation and saccade behavior. J Neurophysiol 79:511-528.
12. Fuchs AF, Robinson DA (1966) A method for measuring horizontal and vertical eye movement chronically in the monkey. J Appl Physiol 21:1068-1070.
13. Fuchs AF, Brettler S, Ling L (2010) Head-free gaze shifts provide further insights into the role of the medial cerebellum in the control of primate saccadic eye movements. J Neurophysiol 103:2158-2173.
14. Gandhi NJ, Katnani HA (2011) Motor functions of the superior colliculus. Annu Rev Neurosci 34:203-229.
15. Gandhi NJ, Keller EL (1997) Spatial distribution and discharge characteristics of superior colliculus neurons antidromically activated from the om-nipause region in monkey. J Neurophysiol 78:2221-2225.
16. Gandhi NJ, Keller EL (1999) Comparison of saccades perturbed by stimulation of the rostral superior colliculus, the caudal superior colliculus, and the omnipause neuron region. J Neurophysiol 82:3236-3253.
17. Gandhi NJ, Sparks DL (2007) Dissociation of eye and head components of gaze shifts by stimulation of the omnipause neuron region. J Neuro-physiol 98:360-373.
18. Goffart L, Chen LL, Sparks DL (2004) Deficits in saccades and fixation during muscimol inactivation of the caudal fastigial nucleus in the rhesus monkey. J Neurophysiol 92:3351-3367.
19. Goffart L, Quinet J, Chavane F, Masson GS (2006) Influence of background illumination on fixation and visually guided saccades in the rhesus monkey. Vision Res 46:149-162.
20. Guerrasio L, Quinet J, Büttner U, Goffart L (2010) The fastigial oculomotor region and the control of foveation during fixation. J Neurophysiol 103:1988-2001.
21. Hafed ZM, Krauzlis RJ (2008) Goal representations dominate superior col-liculus activity during extrafoveal tracking. J Neurosci 28:9426-9439.
22. Hafed ZM, Krauzlis RJ (2012) Similarity of superior colliculus involvement in microsaccade and saccade generation. J Neurophysiol 107:1904-1916.
23. Hafed ZM, Goffart L, Krauzlis RJ (2008) Superior colliculus inactivation causes stable offsets in eye position during tracking. J Neurosci 28:8124-8137.
24. Hafed ZM, Goffart L, Krauzlis RJ (2009) A neural mechanism for microsac-cade generation in the primate superior colliculus. Science 323:940-943.
25. Hall WE, Moschovakis AK (2004) The superior colliculus: new approaches for studying sensorimotor integration. Boca Raton, FL: CRC.
26. Hartwich-Young R, Nelson JS, Sparks DL (1990) The perihypoglossal projection to the superior colliculus in the rhesus monkey. Vis Neurosci 4:29-42.
27. Hikosaka O, Wurtz RH (1985) Modification of saccadic eye movements by GABA-related substances. I. Effect of muscimol and bicuculline in monkey superior colliculus. J Neurophysiol 53:266-291.
28. Izawa Y, Suzuki H, Shinoda Y (2009) Response properties of fixation neurons and their location in the frontal eye field in the monkey. J Neuro-physiol 102:2410-2422.
29. Judge SJ, Richmond BJ, Chu FC (1980) Implantation of magnetic search coils for measurement of eye position: an improved method. Vision Res 20:535-538.
30. Kaneko CR (1996) Effect of ibotenic acid lesions of the omnipause neurons on saccadic eye movements in rhesus macaques. J Neurophysiol 75:2229-2242.
31. Keating EG, Gooley SG (1988) Saccadic disorders caused by cooling the superior colliculus or the frontal eye field, or from combined lesions of both structures. Brain Res 438:247-255.
32. Keating EG, Kenney DV, Gooley SG, Pratt SE, McGillis SL (1986) Targeting errors and reduced oculomotor range following ablations of the superior colliculus or pretectum/thalamus. Behav Brain Res 22:191-210.
33. Krauzlis RJ (2003) Neuronal activity in the rostral superior colliculus related to the initiation of pursuit and saccadic eye movements. J Neurosci 23:4333-4344.
34. Krauzlis RJ, Miles FA (1996) Release of fixation for pursuit and saccades in humans: evidence for shared inputs acting on different neural substrates. J Neurophysiol 76:2822-2833.
35. Krauzlis RJ, Basso MA, Wurtz RH (1997) Shared motor error for multiple eye movements. Science 276:1693-1695.
36. Krauzlis RJ, Basso MA, Wurtz RH (2000) Discharge properties of neurons in the rostral superior colliculus of the monkey during smooth-pursuit eye movements. J Neurophysiol 84:876-891.
37. Krauzlis RJ, Liston D, Carello CD (2004) Target selection and the superior colliculus: goals, choices and hypotheses. Vis Res 44:1445-1451.
38. Lee C, Rohrer WH, Sparks DL (1988) Population coding of saccadic eye movements by neurons in the superior colliculus. Nature 332:357-360.
39. Lovejoy LP, Krauzlis RJ (2010) Inactivation of primate superior colliculus impairs covert selection ofsignals for perceptual judgments. Nat Neurosci 13:261-266.
40. Martin JH (1991) Autoradiographic estimation of the extent of reversible inactivation produced by microinjections of lidocaine and muscimol in the rat. Neurosci Lett 127:160-164.
41. May PJ (2006) The mammalian superior colliculus: laminar structure and connections. Progr Brain Res 151:321-378.
42. May PJ, Hartwich-Young R, Nelson J, Sparks DL, Porter JD (1990) Cerebel-lotectal pathwaysin the macaque: implications for collicular generation of saccades. Neuroscience 36:305-324.
43. McPeek RM, Keller EL (2004) Deficits in saccade target selection after inac-tivation of superior colliculus. Nat Neurosci 7:757-763.
44. Müller JR, Philiastides MG, Newsome WT (2005) Microstimulation of the superior colliculus focuses attention without moving the eyes. Proc Natl Acad Sci U S A 102:524-529.
45. Munoz DP, Guitton D (1991) Controloforienting gaze shifts bythe tectore-ticulospinal system in the head-free cat. II. Sustained discharges during motor preparation and fixation. J Neurophysiol 66:1624-1641.
46. Munoz DP, Wurtz RH (1993a) Fixation cells in monkey superior colliculus. I.Characteristics of cell discharge. J Neurophysiol 70:559-575.
47. Munoz DP, Wurtz RH (1993b) Fixation cellsin monkey superior colliculus. II. Reversible activation and deactivation. J Neurophysiol 70:576-589.
48. Nummela SU, Krauzlis RJ (2010) Inactivation of primate superior collicu- lus biases target choice for smooth pursuit, saccades, and button press responses. J Neurophysiol 104:1538-1548.
49. Paré M, Guitton D (1994) The fixation area of the cat superior colliculus: effects of electrical stimulation and direct connection with brainstem om-nipause neurons. Exp Brain Res 101:109-122.
50. Paré M, Guitton D (1998) Brain stem omnipause neurons and the control of combined eye-head gaze saccades in the alert cat. J Neuro-physiol 79:3060-3076.
51. Pelli DG (1997) The Video Toolbox software for visual psychophysics: transforming numbers into movies. Spat Vis 10:437-442.
52. Phillips JO, Ling L, Fuchs AF (1999) Action of the brain stem saccade generator during horizontal gaze shifts. I. Discharge patterns of omnidirectional pause neurons. J Neurophysiol 81:1284-1295.
53. Quaia C, Aizawa H, Optican LM, Wurtz RH (1998) Reversible inactivation of monkey superior colliculus. II. Maps of saccadic deficits. J Neuro-physiol 79:2097-2110.
54. Robinson DA (1972) Eye movements evoked by collicular stimulation in the alert monkey. Vision Res 12:1795-1808.
55. Robinson FR, Straube A, Fuchs AF (1993) Role of the caudal fastigial nucleus in saccade generation. II. Effects of muscimol inactivation. J Neuro-physiol 70:1741-1758.
56. Sandrine H, Barthélémy F, Masson GS, Goffart L (2006) Fixational saccades in the head restrained monkey: effects of target size. Soc Neurosci Abstr 32:48.11.
57. Sato H, Noda H (1992) Saccadic dysmetria induced by transient functional decortication of the cerebellar vermis. Exp Brain Res 88:455-458.
58. Schiff D, Cohen B, Büttner-Ennever J, Matsuo V (1990) Effects of lesions of the nucleus of the optic tract on optokinetic nystagmus and after-nystagmus in the monkey. Exp Brain Res 79:225-239.
59. Schiller PH, Stryker M (1972) Single-unit recording and stimulation in superior colliculus of the alert rhesus monkey. J Neurophysiol 35:915-924.
60. Segraves MA (1992) Activity of monkey frontal eye field neurons projecting to oculomotor regions of the pons. J Neurophysiol 68:1967-1985.
61. Segraves MA, Goldberg ME (1987) Functional properties of corticotectal neurons in the monkey's frontal eye field. J Neurophysiol 58:1387-1419.
62. Soetedjo R, Kaneko CR, Fuchs AF (2000) Evidence that the superior collicu-lus participatesin the feedback control of saccadic eye movements. J Neu-rophysiol 87:679-695.
63. Sparks DL (1986) Translation of sensory signals into commands for control of saccadic eye movements: role of primate superior colliculus. Physiol Rev 66:118-171.
64. Sparks DL, Holland R, Guthrie BL (1976) Size and distribution of movement fields in the monkey superior colliculus. Brain Res 113:21-34.
65. Sparks DL, Lee C, Rohrer WC (1990) Population coding of the direction, amplitude and velocity of saccadic eye movements by neurons in the superior colliculus. Cold Spring Harbor Symp Quant Biol 55:805-811.
66. Stanford TR, Freedman EG, Sparks DL (1996) Site and parameters of microstimulation: evidence for independent effects on the properties of saccades evoked from the primate superior colliculus. J Neuro-physiol 76:3360-3381.
67. Stanton GB, Goldberg ME, Bruce CJ (1988) Frontal eye field efferents in the macaque monkey: II. Topography of terminal fields in midbrain and pons. J Comp Neurol 271:493-506.
68. Strassman A, Evinger C, McCrea RA, Baker RG, Highstein SM (1987) Anatomy and physiology of intracellularly labelled omnipause neurons in the cat and squirrel monkey. Exp Brain Res 67:436-440.
69. Sugiuchi Y, Izawa Y, Takahashi M, Na J, Shinoda Y (2005) Physiological characterization of synaptic inputs to inhibitory burst neurons from the rostral and caudal superior colliculus. J Neurophysiol 93:697-712.
70. Takahashi M, Sugiuchi Y, Shinoda Y (2010) Topographic organization of excitatory and inhibitory commissural connections in the superior col-liculi and their functional roles in saccade generation. J Neurophysiol 104:3146-3167.
71. Van Horn MR, Cullen KE (2012) Coding of microsaccades in three-dimensional space by premotor saccadic neurons. J Neurosci 32: 1974-1980.
72. Wurtz RH, Goldberg ME (1972) Activity of superior colliculus in behaving monkey. 3. Cells discharging before eye movements. J Neurophysiol 35: 575-586.