Bilateral saccadic deficits following large and reversible inactivation of unilateral frontal eye field

Journal of Neurophysiology

Volumn 111, Issue 2, 2014, Pages 415-433

  Peel, Tyler R ^a,c   Johnston, Kevin ^a,c   Lomber, Stephen G ^a,c   Corneil, Brian D ^a,b,c  

^a Brain and Mind Institute   (Canada)

^b ROBARTS RESEARCH INSTITUTE   (Canada)

^c UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Frontal eye field; Reversible inactivation; Saccade generation

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASSOCIATION; CONTROLLED STUDY; EYE MOVEMENT DISORDER; FRONTAL EYE FIELD; FRONTAL EYE FIELD INACTIVATION; HAPLORHINI; MALE; MEMORY; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; REACTION TIME; RHESUS MONKEY; SACCADIC DEFICIT; SACCADIC EYE MOVEMENT;

FRONTAL EYE FIELD; REVERSIBLE INACTIVATION; SACCADE GENERATION;

ANIMALS; CUES; DENERVATION; FRONTAL LOBE; FUNCTIONAL LATERALITY; MACACA MULATTA; MALE; MEMORY; PSYCHOMOTOR PERFORMANCE; SACCADES; VISUAL FIELDS;

EID: 84892620434     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00398.2013     Document Type: Article

References (95)

1. Aizawa H, Wurtz RH. Reversible inactivation of monkey superior colliculus. I. Curvature of saccadic trajectory. J Neurophysiol 79: 2082-2096, 1998.
2. Albano JE, Mishkin M, Westbrook LE, Wurtz RH. Visuomotor deficits following ablation of monkey superior colliculus. J Neurophysiol 48: 338-351, 1982.
3. Albano JE, Wurtz RH. Deficits in eye position following ablation of monkey superior colliculus, pretectum, and posterior-medial thalamus. J Neurophysiol 48: 318-337, 1982.
4. Ashmore RC, Sommer MA. Delay activity of saccade-related neurons in the caudal dentate nucleus of the macaque cerebellum. J Neurophysiol 109: 2129-2144, 2013.
5. Beckstead RM, Edwards SB, Frankfurter A. A comparison of the intranigral distribution of nigrotectal neurons labeled with horseradish peroxidase in the monkey, cat, and rat. J Neurosci 1: 121-125, 1981.
6. Boulanger M, Bergeron A, Guitton D. Ipsilateral head and centring eye movements evoked from monkey premotor cortex. Neuroreport 20: 669-673, 2009.
7. Bruce CJ, Goldberg ME. Primate frontal eye fields. I. Single neurons discharging before saccades. J Neurophysiol 53: 603-635, 1985.
8. Bruce CJ, Goldberg ME, Bushnell MC, Stanton GB. Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements. J Neurophysiol 54: 714-734, 1985.
9. Burman DD, Bruce CJ. Suppression of task-related saccades by electrical stimulation in the primate's frontal eye field. J Neurophysiol 77: 2252-2267, 1997.
10. Cavanaugh J, Joiner WM, Wurtz RH. Suppressive surrounds of receptive fields in monkey frontal eye field. J Neurosci 32: 12284-12293, 2012a.
11. Cavanaugh J, Monosov IE, McAlonan K, Berman R, Smith MK, Cao V, Wang KH, Boyden ES, Wurtz RH. Optogenetic inactivation modifies monkey visuomotor behavior. Neuron 76: 901-907, 2012b.
12. Chevalier G, Deniau JM, Thierry AM, Feger J. The nigro-tectal pathway. An electrophysiological reinvestigation in the rat. Brain Res 213: 253-263, 1981.
13. Cohen JY, Crowder EA, Heitz RP, Subraveti CR, Thompson KG, Woodman GF, Schall JD. Cooperation and competition among frontal eye field neurons during visual target selection. J Neurosci 30: 3227-3238, 2010.
14. Collin NG, Cowey A, Latto R, Marzi C. The role of frontal eye-fields and superior colliculi in visual search and non-visual search in rhesus monkeys. Behav Brain Res 4: 177-193, 1982.
15. Crapse TB, Sommer MA. Frontal eye field neurons with spatial representations predicted by their subcortical input. J Neurosci 29: 5308-5318, 2009.
16. Dassonville P, Schlag J, Schlag-Rey M. The frontal eye field provides the goal of saccadic eye movement. Exp Brain Res 89: 300-310, 1992.
17. Deng SY, Goldberg ME, Segraves MA, Ungerleider LG, Mishkin M. The effect of unilateral ablation of the frontal eye fields on saccadic performance in the monkey. In: Adaptive Processes in the Visual and Oculomotor Systems, edited by Keller EL, Zee DS. Oxford, UK: Pergamon, 1986, p. 201-208.
18. Dias EC, Bruce CJ. Physiological correlate of fixation disengagement in the primate's frontal eye field. J Neurophysiol 72: 2532-2537, 1994.
19. Dias EC, Kiesau M, Segraves MA. Acute activation and inactivation of macaque frontal eye field with GABA-related drugs. J Neurophysiol 74: 2744-2748, 1995.
20. Dias EC, Segraves MA. Muscimol-induced inactivation of monkey frontal eye field: effects on visually and memory-guided saccades. J Neurophysiol 81: 2191-2214, 1999.
21. Elsley JK, Nagy B, Cushing SL, Corneil BD. Widespread presaccadic recruitment of neck muscles by stimulation of the primate frontal eye fields. J Neurophysiol 98: 1333-1354, 2007.
22. Fujii N, Mushiake H, Tanji J. An oculomotor representation area within the ventral premotor cortex. Proc Natl Acad Sci USA 95: 12034-12037, 1998.
23. Fujii N, Mushiake H, Tanji J. Rostrocaudal distinction of the dorsal premotor area based on oculomotor involvement. J Neurophysiol 83: 1764-1769, 2000.
24. Funahashi S, Bruce CJ, Goldman-Rakic PS. Neuronal activity related to saccadic eye movements in the monkey's dorsolateral prefrontal cortex. J Neurophysiol 65: 1464-1483, 1991.
25. Gaymard B, Ploner CJ, Rivaud-Pechoux S, Pierrot-Deseilligny C. The frontal eye field is involved in spatial short-term memory but not in reflexive saccade inhibition. Exp Brain Res 129: 288-301, 1999.
26. Gottlieb JP, MacAvoy MG, Bruce CJ. Neural responses related to smoothpursuit eye movements and their correspondence with electrically elicited smooth eye movements in the primate frontal eye field. J Neurophysiol 72: 1634-1653, 1994.
27. Graybiel AM, Ragsdale CW Jr. Histochemically distinct compartments in the striatum of human, monkeys, and cat demonstrated by acetylthiocholinesterase staining. Proc Natl Acad Sci USA 75: 5723-5726, 1978.
28. Graziano MS, Taylor CS, Moore T. Complex movements evoked by microstimulation of precentral cortex. Neuron 34: 841-851, 2002.
29. Halsband U, Passingham R. The role of premotor and parietal cortex in the direction of action. Brain Res 240: 368-372, 1982.
30. Hanes DP, Patterson WF 2nd, Schall JD. Role of frontal eye fields in countermanding saccades: visual, movement, and fixation activity. J Neurophysiol 79: 817-834, 1998.
31. Hanes DP, Wurtz RH. Interaction of the frontal eye field and superior colliculus for saccade generation. J Neurophysiol 85: 804-815, 2001.
32. Heitz RP, Schall JD. Neural mechanisms of speed-accuracy tradeoff. Neuron 76: 616-628, 2012.
33. Hikosaka O, Wurtz RH. Effects on eye movements of a GABA agonist and antagonist injected into monkey superior colliculus. Brain Res 272: 368-372, 1983.
34. Hikosaka O, Wurtz RH. Saccadic eye movements following injection of lidocaine into the superior colliculus. Exp Brain Res 61: 531-539, 1986.
35. Huerta MF, Krubitzer LA, Kaas JH. Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys. I. Subcortical connections. J Comp Neurol 253: 415-439, 1986.
36. Izawa Y, Suzuki H, Shinoda Y. Suppression of visually and memory-guided saccades induced by electrical stimulation of the monkey frontal eye field. II. Suppression of bilateral saccades. J Neurophysiol 92: 2261-2273, 2004.
37. Izawa Y, Suzuki H, Shinoda Y. Response properties of fixation neurons and their location in the frontal eye field in the monkey. J Neurophysiol 102: 2410-2422, 2009.
38. Jayaraman A, Batton RR 3rd, Carpenter MB. Nigrotectal projections in the monkey: an autoradiographic study. Brain Res 135: 147-152, 1977.
39. Jiang H, Stein BE, McHaffie JG. Opposing basal ganglia processes shape midbrain visuomotor activity bilaterally. Nature 423: 982-986, 2003.
40. Johnston K, Koval MJ, Lomber SG, Everling S. Macaque dorsolateral prefrontal cortex does not suppress saccade-related activity in the superior colliculus. Cereb Cortex (January 10, 2013). doi:10.1093/cercor/bhs424.
41. Koyama M, Hasegawa I, Osada T, Adachi Y, Nakahara K, Miyashita Y. Functional magnetic resonance imaging of macaque monkeys performing visually guided saccade tasks: comparison of cortical eye fields with humans. Neuron 41: 795-807, 2004.
42. Kunzle H, Akert K. Efferent connections of cortical, area 8 (frontal eye field) in Macaca fascicularis. A reinvestigation using the autoradiographic technique. J Comp Neurol 173: 147-164, 1977.
43. Latto R, Cowey A. Visual field defects after frontal eye-field lesions in monkeys. Brain Res 30: 1-24, 1971.
44. Lee KM, Ahn KH, Keller EL. Saccade generation by the frontal eye fields in rhesus monkeys is separable from visual detection and bottom-up attention shift. PLoS One 7: e39886, 2012.
45. Leichnetz GR, Spencer RF, Hardy SG, Astruc J. The prefrontal corticotectal projection in the monkey; an anterograde and retrograde horseradish peroxidase study. Neuroscience 6: 1023-1041, 1981.
46. Leichnetz GR, Spencer RF, Smith DJ. Cortical projections to nuclei adjacent to the oculomotor complex in the medial dien-mesencephalic tegmentum in the monkey. J Comp Neurol 228: 359-387, 1984.
47. Liu P, Basso MA. Substantia nigra stimulation influences monkey superior colliculus neuronal activity bilaterally. J Neurophysiol 100: 1098-1112, 2008.
48. Lomber SG. The advantages and limitations of permanent or reversible deactivation techniques in the assessment of neural function. J Neurosci Methods 86: 109-117, 1999.
49. Lomber SG, Payne BR, Horel JA. The cryoloop: an adaptable reversible cooling deactivation method for behavioral or electrophysiological assessment of neural function. J Neurosci Methods 86: 179-194, 1999.
50. Lynch JC. Saccade initiation and latency deficits after combined lesions of the frontal and posterior eye fields in monkeys. J Neurophysiol 68: 1913-1916, 1992.
51. Lynch JC, Hoover JE, Strick PL. Input to the primate frontal eye field from the substantia nigra, superior colliculus, and dentate nucleus demonstrated by transneuronal transport. Exp Brain Res 100: 181-186, 1994.
52. May PJ, Hartwich-Young R, Nelson J, Sparks DL, Porter JD. Cerebellotectal pathways in the macaque: implications for collicular generation of saccades. Neuroscience 36: 305-324, 1990.
53. Mays LE, Sparks DL. Dissociation of visual and saccade-related responses in superior colliculus neurons. J Neurophysiol 43: 207-232, 1980.
54. Moll L, Kuypers HG. Premotor cortical ablations in monkeys: contralateral changes in visually guided reaching behavior. Science 198: 317-319, 1977.
55. Moschovakis AK, Gregoriou GG, Ugolini G, Doldan M, Graf W, Guldin W, Hadjidimitrakis K, Savaki HE. Oculomotor areas of the primate frontal lobes: a transneuronal transfer of rabies virus and [14C]-2-deoxyglucose functional imaging study. J Neurosci 24: 5726-5740, 2004.
56. Munoz DP, Dorris MC, Pare M, Everling S. On your mark, get set: brainstem circuitry underlying saccadic initiation. Can J Physiol Pharmacol 78: 934-944, 2000.
57. Nassi JJ, Lomber SG, Born RT. Corticocortical feedback contributes to surround suppression in V1 of the alert primate. J Neurosci 33: 8504-8517, 2013.
58. Olfert E, Cross B, McWilliam A. Guide to the Care and Use of Experimental Animals. Ottawa, ON, Canada: Canadian Council on Animal Care, 1993.
59. Pandya DN, Vignolo LA. Intra-and interhemispheric projections of the precentral, premotor and arcuate areas in the rhesus monkey. Brain Res 26: 217-233, 1971.
60. Peel TR, Lomber SG, Corneil BD. Behavioural effects of unilateral cryogenic inactivation of primate frontal eye fields (Abstract). Soc Neurosci Abstr 2010: 779.17, 2010.
61. Peel TR, Lomber SG, Corneil BD. Functional contribution of the frontal eye fields to activity in the intermediate superior colliculus (Abstract). Soc Neurosci Abstr 2012: 373.10, 2012.
62. Pierrot-Deseilligny C, Rivaud S, Gaymard B, Agid Y. Cortical control of reflexive visually-guided saccades. Brain 114: 1473-1485, 1991.
63. Ponce CR, Hunter JN, Pack CC, Lomber SG, Born RT. Contributions of indirect pathways to visual response properties in macaque middle temporal area MT. J Neurosci 31: 3894-3903, 2011.
64. Prevosto V, Graf W, Ugolini G. Cerebellar inputs to intraparietal cortex areas LIP and MIP: functional frameworks for adaptive control of eye movements, reaching, and arm/eye/head movement coordination. Cereb Cortex 20: 214-228, 2010.
65. Quaia C, Aizawa H, Optican LM, Wurtz RH. Reversible inactivation of monkey superior colliculus. II. Maps of saccadic deficits. J Neurophysiol 79: 2097-2110, 1998.
66. Rivaud S, Muri RM, Gaymard B, Vermersch AI, Pierrot-Deseilligny C. Eye movement disorders after frontal eye field lesions in humans. Exp Brain Res 102: 110-120, 1994.
67. Rizzolatti G, Matelli M, Pavesi G. Deficits in attention and movement following the removal of postarcuate (area 6) and prearcuate (area 8) cortex in macaque monkeys. Brain 106: 655-673, 1983.
68. Robinson DA, Fuchs AF. Eye movements evoked by stimulation of frontal eye fields. J Neurophysiol 32: 637-648, 1969.
69. Schall JD. The neural selection and control of saccades by the frontal eye field. Philos Trans R Soc Lond B Biol Sci 357: 1073-1082, 2002.
70. Schieber MH. Inactivation of the ventral premotor cortex biases the laterality of motoric choices. Exp Brain Res 130: 497-507, 2000.
71. Schiller PH, Chou IH. The effects of frontal eye field and dorsomedial frontal cortex lesions on visually guided eye movements. Nat Neurosci 1: 248-253, 1998.
72. Schiller PH, True SD, Conway JL. Deficits in eye movements following frontal eye-field and superior colliculus ablations. J Neurophysiol 44: 1175-1189, 1980.
73. Schlag J, Dassonville P, Schlag-Rey M. Interaction of the two frontal eye fields before saccade onset. J Neurophysiol 79: 64-72, 1998.
74. Schmahmann JD, Pandya DN. Anatomic organization of the basilar pontine projections from prefrontal cortices in rhesus monkey. J Neurosci 17: 438-458, 1997.
75. Schnyder H, Reisine H, Hepp K, 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.
76. Schwartz EL. Computational anatomy and functional architecture of striate cortex: a spatial mapping approach to perceptual coding. Vision Res 20: 645-669, 1980.
77. Segraves MA. Activity of monkey frontal eye field neurons projecting to oculomotor regions of the pons. J Neurophysiol 68: 1967-1985, 1992.
78. Segraves MA, Goldberg ME. Functional properties of corticotectal neurons in the monkey's frontal eye field. J Neurophysiol 58: 1387-1419, 1987.
79. Segraves MA, Park K. The relationship of monkey frontal eye field activity to saccade dynamics. J Neurophysiol 69: 1880-1889, 1993.
80. Seidemann E, Arieli A, Grinvald A, Slovin H. Dynamics of depolarization and hyperpolarization in the frontal cortex and saccade goal. Science 295: 862-865, 2002.
81. Shi D, Friedman HR, Bruce CJ. Deficits in smooth-pursuit eye movements after muscimol inactivation within the primate's frontal eye field. J Neurophysiol 80: 458-464, 1998.
82. Sommer MA, Tehovnik EJ. Reversible inactivation of macaque frontal eye field. Exp Brain Res 116: 229-249, 1997.
83. Sommer MA, Wurtz RH. Composition and topographic organization of signals sent from the frontal eye field to the superior colliculus. J Neurophysiol 83: 1979-2001, 2000.
84. Sommer MA, Wurtz RH. Frontal eye field sends delay activity related to movement, memory, and vision to the superior colliculus. J Neurophysiol 85: 1673-1685, 2001.
85. Stanton GB, Goldberg ME, Bruce CJ. Frontal eye field efferents in the macaque monkey: I. Subcortical pathways and topography of striatal and thalamic terminal fields. J Comp Neurol 271: 473-492, 1988a.
86. Stanton GB, Goldberg ME, Bruce CJ. Frontal eye field efferents in the macaque monkey: II. Topography of terminal fields in midbrain and pons. J Comp Neurol 271: 493-506, 1988b.
87. Tanaka M. Inactivation of the central thalamus delays self-timed saccades. Nat Neurosci 9: 20-22, 2006.
88. Tanaka M. Cognitive signals in the primate motor thalamus predict saccade timing. J Neurosci 27: 12109-12118, 2007.
89. Tanaka M, Fukushima K. Neuronal responses related to smooth pursuit eye movements in the periarcuate cortical area of monkeys. J Neurophysiol 80: 28-47, 1998.
90. van der Steen J, Russell IS, James GO. Effects of unilateral frontal eye-field lesions on eye-head coordination in monkey. J Neurophysiol 55: 696-714, 1986.
91. Weinrich M, Wise SP. The premotor cortex of the monkey. J Neurosci 2: 1329-1345, 1982.
92. Weinrich M, Wise SP, Mauritz KH. A neurophysiological study of the premotor cortex in the rhesus monkey. Brain 107: 385-414, 1984.
93. White JM, Sparks DL, Stanford TR. Saccades to remembered target locations: an analysis of systematic and variable errors. Vision Res 34: 79-92, 1994.
94. Wurtz RH, Goldberg ME. Activity of superior colliculus in behaving monkey. IV. Effects of lesions on eye movements. J Neurophysiol 35: 587-596, 1972.
95. Xiong G, Hiramatsu T, Nagao S. Corticopontocerebellar pathway from the prearcuate region to hemispheric lobule VII of the cerebellum: an anterograde and retrograde tracing study in the monkey. Neurosci Lett 322: 173-176, 2002.