Division of labor in frontal eye field neurons during presaccadic remapping of visual receptive fields

Journal of Neurophysiology

Volumn 108, Issue 8, 2012, Pages 2144-2159

  Shin, SooYoon ^a,b   Sommer, Marc A ^a,c  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Duke University   (United States)

Author keywords

Microcircuitry; Perception; Saccades; Vision

Indexed keywords

ACTION POTENTIAL; ANIMAL EXPERIMENT; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN MAPPING; CONTROLLED STUDY; FRONTAL EYE FIELD; LATENT PERIOD; MALE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RECEPTIVE FIELD; RHESUS MONKEY; SACCADIC EYE MOVEMENT; SIGNAL NOISE RATIO; TASK PERFORMANCE;

ANIMALS; EVOKED POTENTIALS, VISUAL; MACACA MULATTA; MALE; NEURONS; SACCADES; VISUAL CORTEX; VISUAL FIELDS; VISUAL PATHWAYS;

EID: 84867700161     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00204.2012     Document Type: Article

References (85)

1. Bacci A, Rudolph U, Huguenard JR, Prince DA. Major differences in inhibitory synaptic transmission onto two neocortical interneuron subclasses. J Neurosci 23: 9664-9674, 2003.
2. Bartho P, Hirase H, Monconduit L, Zugaro M, Harris KD, Buzsaki G. Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. J Neurophysiol 92: 600-608, 2004.
3. Beierlein M, Gibson JR, Connors BW. A network of electrically coupled interneurons drives synchronized inhibition in neocortex. Nat Neurosci 3: 904-910, 2000.
4. Beierlein M, Gibson JR, Connors BW. Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J Neurophysiol 90: 2987-3000, 2003.
5. Benevento LA, Fallon JH. The ascending projections of the superior colliculus in the rhesus monkey (Macaca mulatta). J Comp Neurol 160: 339-361, 1975.
6. Bruce CJ, Goldberg ME. Primate frontal eye fields. I. Single neurons discharging before saccades. J Neurophysiol 53: 603-635, 1985.
7. Bruno RM, Simons DJ. Feedforward mechanisms of excitatory and inhibitory cortical receptive fields. J Neurosci 22: 10966-10975, 2002.
8. Bullier J, Henry GH. Ordinal position of neurons in cat striate cortex. J Neurophysiol 42: 1251-1263, 1979.
9. Cardin JA. Dissecting local circuits in vivo: integrated optogenetic and electrophysiology approaches for exploring inhibitory regulation of cortical activity. J Physiol Paris 106: 104-111, 2012.
10. Cavanagh P, Hunt AR, Afraz A, Rolfs M. Visual stability based on remapping of attention pointers. Trends Cogn Sci 14: 147-153, 2010.
11. Chen Y, Martinez-Conde S, Macknik SL, Bereshpolova Y, Swadlow HA, Alonso JM. Task difficulty modulates the activity of specific neuronal populations in primary visual cortex. Nat Neurosci 11: 974-982, 2008.
12. Churan J, Guitton D, Pack CC. Context dependence of receptive field remapping in superior colliculus. J Neurophysiol 106: 1862-1874, 2011.
13. Cohen JY, Pouget P, Heitz RP, Woodman GF, Schall JD. Biophysical support for functionally distinct cell types in the frontal eye field. J Neurophysiol 101: 912-916, 2009.
14. Connors BW, Gutnick MJ. Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci 13: 99-104, 1990.
15. Constantinidis C, Goldman-Rakic PS. Correlated discharges among putative pyramidal neurons and interneurons in the primate prefrontal cortex. J Neurophysiol 88: 3487-3497, 2002.
16. Crapse TB, Sommer MA. Frontal eye field neurons assess visual stability across saccades. J Neurosci 32: 2835-2845, 2012.
17. Crapse TB, Sommer MA. The frontal eye field as a prediction map. Prog Brain Res 171: 383-390, 2008.
18. Ding L, Gold JI. Neuronal correlates of perceptual decision making before, during, and after decision commitment in monkey frontal eye field. Cereb Cortex 22: 1052-1067, 2012.
19. Douglas RJ, Martin KAC. Neuronal circuits of the neocortex. Annu Rev Neurosci 27: 419-451, 2004.
20. Duhamel JR, Colby CL, Goldberg ME. The updating of the representation of visual space in parietal cortex by intended eye movements. Science 255: 90-92, 1992.
21. Dunn CA, Hall NJ, Colby CL. Spatial updating in monkey superior colliculus in the absence of the forebrain commissures: dissociation between superficial and intermediate layers. J Neurophysiol 104: 1267-1285, 2010.
22. Everling S, Munoz DP. Neuronal correlates for preparatory set associated with pro-saccades and anti-saccades in the primate frontal eye field. J Neurosci 20: 387-400, 2000.
23. Fenno L, Yizhar O, Deisseroth K. The development and application of optogenetics. Annu Rev Neurosci 34: 389-412, 2011.
24. Ferraina S, Paré M, Wurtz RH. Comparison of cortico-cortical and corticocollicular signals for the generation of saccadic eye movements. J Neurophysiol 87: 845-858, 2002.
25. Ferster D, Lindström S. An intracellular analysis of geniculo-cortical connectivity in area 17 of the cat. J Physiol 342: 181-215, 1983.
26. Frank LM, Brown EN, Wilson MA. A comparison of the firing properties of putative excitatory and inhibitory neurons from CA1 and the entorhinal cortex. J Neurophysiol 86: 2029-2040, 2001.
27. Fries W. Cortical projections to the superior colliculus in the macaque monkey: a retrograde study using horseradish peroxidase. J Comp Neurol 230: 55-76, 1984.
28. Galarreta M, Hestrin S. A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 402: 72-75, 1999.
29. Gibson JR, Beierlein M, Connors BW. Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402: 75-79, 1999.
30. Giguere M, Goldman-Rakic PS. Mediodorsal nucleus: areal, laminar, and tangential distribution of afferents and efferents in the frontal lobe of rhesus monkeys. J Comp Neurol 277: 195-213, 1988.
31. Goldberg ME, Bushnell MC. Behavioral enhancement of visual responses in monkey cerebral cortex. II. Modulation in frontal eye fields specifically related to saccades. J Neurophysiol 46: 773-787, 1981.
32. Goldman-Rakic PS, Porrino LJ. The primate mediodorsal (MD) nucleus and its projection to the frontal lobe. J Comp Neurol 242: 535-560, 1985.
33. Gonzalez-Burgos G, Krimer LS, Povysheva NV, Barrionuevo G, Lewis DA. Functional properties of fast spiking interneurons and their synaptic connections with pyramidal cells in primate dorsolateral prefrontal cortex. J Neurophysiol 93: 942-953, 2005.
34. Hall NJ, Colby CL. Remapping for visual stability. Philos Trans R Soc Lond B Biol Sci 366: 528-539, 2011.
35. Hays AV, Richmond BJ, Optican BJ. A UNIX-based multiple process system for real-time data acquisition and control. WESCON Conf Proc 2: 1-10, 1982.
36. Heinzle J, Hepp K, Martin KAC. A microcircuit model of the frontal eye fields. J Neurosci 27: 9341-9353, 2007.
37. Heiser LM, Berman RA, Saunders RC, Colby CL. Dynamic circuitry for updating spatial representations. II. Physiological evidence for interhemispheric transfer in area LIP of the split-brain macaque. J Neurophysiol 94: 3249-3258, 2005.
38. Holdefer RN, Miller LE, Chen LL, Houk JC. Functional connectivity between cerebellum and primary motor cortex in the awake monkey. J Neurophysiol 84: 585-590, 2000.
39. Johnson JL, Welsh JP. Independently movable multielectrode array to record multiple fast-spiking neurons in the cerebral cortex during cognition. Methods 30: 64-78, 2003.
40. Johnston K, DeSouza JF, Everling S. Monkey prefrontal cortical pyramidal and putative interneurons exhibit differential patterns of activity between prosaccade and antisaccade tasks. J Neurosci 29: 5516-5524, 2009.
41. Kawaguchi Y. Groupings of nonpyramidal and pyramidal cells with specific physiological and morphological characteristics in rat frontal cortex. J Neurophysiol 69: 416-431, 1993.
42. Keith GP, Blohm G, Crawford JD. Influence of saccade efference copy on the spatiotemporal properties of remapping: a neural network study. J Neurophysiol 103: 117-139, 2010.
43. Keith GP, Crawford JD. Saccade-related remapping of target representations between topographic maps: a neural network study. J Comput Neurosci 24: 157-178, 2008.
44. Klier EM, Angelaki DE. Spatial updating and the maintenance of visual constancy. Neuroscience 156: 801-818, 2008.
45. Krimer LS, Zaitsev AV, Czanner G, Kröner S, González-Burgos G, Povysheva NV, Iyengar S, Barrionuevo G, Lewis DA. Cluster analysisbased physiological classification and morphological properties of inhibitory neurons in layers 2-3 of monkey dorsolateral prefrontal cortex. J Neurophysiol 94: 3009-3022, 2005.
46. Kusunoki M, Goldberg ME. The time course of perisaccadic receptive field shifts in the lateral intraparietal area of the monkey. J Neurophysiol 89: 1519-1527, 2003.
47. 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.
48. Lemon R. Methods for Neuronal Recording in Conscious Animals. New York: Wiley, 1984.
49. Lipski J. Antidromic activation of neurones as an analytic tool in the study of the central nervous system. J Neurosci Methods 4: 1-32, 1981.
50. Mays LE, Sparks DL. Dissociation of visual and saccade-related responses in superior colliculus neurons. J Neurophysiol 43: 207-232, 1980.
51. McCormick DA, Connors BW, Lighthall JW, Prince DA. Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 54: 782-806, 1985.
52. Merriam EP, Colby CL. Active vision in parietal and extrastriate cortex. Neuroscientist 11: 484-493, 2005.
53. Mitchell JF, Sundberg KA, Reynolds JH. Differential attention-dependent response modulation across cell classes in macaque visual area V4. Neuron 55: 131-141, 2007.
54. Nakamura K, Colby CL. Updating of the visual representation in monkey striate and extrastriate cortex during saccades. Proc Natl Acad Sci USA 99: 4026-4031, 2002.
55. Nowak LG, Azouz R, Sanchez-Vives MV, Gray CM, McCormick DA. Electrophysiological classes of cat primary visual cortical neurons in vivo as revealed by quantitative analyses. J Neurophysiol 89: 1541-1566, 2003.
56. Quaia C, Optican LM, Goldberg ME. The maintenance of spatial accuracy by the perisaccadic remapping of visual receptive fields. Neural Netw 11: 1229-1240, 1998.
57. Rao SG, Williams GV, Goldman-Rakic PS. Isodirectional tuning of adjacent interneurons and pyramidal cells during working memory: evidence for microcolumnar organization in PFC. J Neurophysiol 81: 1903-1916, 1999.
58. Sasaki K, Jinnai K, Gemba H, Hashimoto S, Mizuno N. Projection of the cerebellar dentate nucleus onto the frontal association cortex in monkeys. Exp Brain Res 37: 193-198, 1979.
59. Sasaki K, Kawaguchi S, Matsuda Y, Mizuno N. Electrophysiological studies on cerebello-cerebral projections in the cat. Exp Brain Res 16: 75-88, 1972.
60. Schall JD, Morel A, King DJ, Bullier J. Topography of visual cortex connections with frontal eye field in macaque: convergence and segregation of processing streams. J Neurosci 15: 4464-4487, 1995.
61. Segraves MA, Goldberg ME. Functional properties of corticotectal neurons in the monkey's frontal eye field. J Neurophysiol 58: 1387-1419, 1987.
62. Segraves MA, Park K. The relationship of monkey frontal eye field activity to saccade dynamics. J Neurophysiol 69: 1880-1889, 1993.
63. Simons DJ. Response properties of vibrissa units in rat SI somatosensory neocortex. J Neurophysiol 41: 798-820, 1978.
64. Singer W, Tretter F, Cynader M. Organization of cat striate cortex: a correlation of receptive-field properties with afferent and efferent connections. J Neurophysiol 38: 1080-1098, 1975.
65. Sommer MA, Wurtz RH. A pathway in primate brain for internal monitoring of movements. Science 296: 1480-1482, 2002.
66. Sommer MA, Wurtz RH. Brain circuits for the internal monitoring of movements. Annu Rev Neurosci 31: 317-338, 2008.
67. 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.
68. Sommer MA, Wurtz RH. Frontal eye field neurons orthodromically activated from the superior colliculus. J Neurophysiol 80: 3331-3335, 1998.
69. 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.
70. Sommer MA, Wurtz RH. Influence of the thalamus on spatial visual processing in frontal cortex. Nature 444: 374-377, 2006.
71. Sommer MA, Wurtz RH. What the brain stem tells the frontal cortex. I. Oculomotor signals sent from superior colliculus to frontal eye field via mediodorsal thalamus. J Neurophysiol 91: 1381-1402, 2004a.
72. Sommer MA, Wurtz RH. What the brain stem tells the frontal cortex. II. Role of the SC-MD-FEF pathway in corollary discharge. J Neurophysiol 91: 1403-1423, 2004b.
73. Song JH, McPeek RM. Roles of narrow- and broad-spiking dorsal premotor area neurons in reach target selection and movement production. J Neurophysiol 103: 2124-2138, 2010.
74. Swadlow HA. Efferent neurons and suspected interneurons in S-1 vibrissa cortex of the awake rabbit: receptive fields and axonal properties. J Neurophysiol 62: 288-308, 1989.
75. Swadlow HA. Fast-spike interneurons and feedforward inhibition in awake sensory neocortex. Cereb Cortex 13: 25-32, 2003.
76. Tamas G, Buhl EH, Lorincz A, Somogyi P. Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons. Nat Neurosci 3: 366-371, 2000.
77. Tamura H, Kaneko H, Kawasaki K, Fujita I. Presumed inhibitory neurons in the macaque inferior temporal cortex: visual response properties and functional interactions with adjacent neurons. J Neurophysiol 91: 2782-2796, 2004.
78. Tan Z, Hu H, Huang ZJ, Agmon A. Robust but delayed thalamocortical activation of dendritic-targeting inhibitory interneurons. Proc Natl Acad Sci USA 105: 2187-2192, 2008.
79. Umeno MM, Goldberg ME. Spatial processing in the monkey frontal eye field. I. Predictive visual responses. J Neurophysiol 78: 1373-1383, 1997.
80. Umeno MM, Goldberg ME. Spatial processing in the monkey frontal eye field. II. Memory responses. J Neurophysiol 86: 2344-52, 2001.
81. Vigneswaran G, Kraskov A, Lemon RN. Large identified pyramidal cells in macaque motor and premotor cortex exhibit "thin spikes": implications for cell type classification. J Neurosci 31: 14235-14242, 2011.
82. Walker MF, Fitzgibbon EJ, Goldberg ME. Neurons in the monkey superior colliculus predict the visual result of impending saccadic eye movements. J Neurophysiol 73: 1988-2003, 1995.
83. Wurtz RH, Mohler CW. Enhancement of visual responses in monkey striate cortex and frontal eye fields. J Neurophysiol 39: 766-772, 1976.
84. Wurtz RH, Sommer MA, Cavanaugh J. Drivers from the deep: the contribution of collicular input to thalamocortical processing. Prog Brain Res 149: 207-225, 2005.
85. Zirnsak M, Lappe M, Hamker FH. The spatial distribution of receptive field changes in a model of peri-saccadic perception: predictive remapping and shifts towards the saccade target. Vision Res 50: 1328-1337, 2010.