Response variability of frontal eye field neurons modulates with sensory input and saccade preparation but not visual search salience

Journal of Neurophysiology

Volumn 108, Issue 10, 2012, Pages 2737-2750

  Purcell, Braden A ^a   Heitz, Richard P ^a   Cohen, Jeremiah Y ^a   Schall, Jeffrey D ^a  

^a VANDERBILT UNIVERSITY   (United States)

Author keywords

Attention; Fano factor; Motor control; Motor preparation; Variability

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; EVOKED VISUAL RESPONSE; FRONTAL EYE FIELD; NERVE CELL; NERVE CELL MEMBRANE POTENTIAL; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; RESPONSE TIME; RHESUS MONKEY; SACCADIC EYE MOVEMENT; SENSORY STIMULATION; SPATIAL ORIENTATION;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; ATTENTION; FRONTAL LOBE; MACACA; MEMORY; NEURONS; PHOTIC STIMULATION; SACCADES; TASK PERFORMANCE AND ANALYSIS; VISUAL ACUITY; VISUAL FIELDS;

EID: 84869191649     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00613.2012     Document Type: Article

References (80)

1. Afshar A, Santhanam G, Yu BM, Ryu SI, Sahani M, Shenoy KV. Single-trial neural correlates of arm movement preparation. Neuron 71: 555-564, 2011.
2. Albrecht DG, Hamilton DB. Striate cortex of monkey and cat: Contrast response function. J Neurophysiol 48: 217-237, 1982.
3. Bichot NP, Schall JD. Effects of similarity and history on neural mechanisms of visual selection. Nat Neurosci 2: 549-554, 1999a.
4. Bichot NP, Schall JD. Priming in macaque frontal cortex during popout visual search: feature-based facilitation and location-based inhibition of return. J Neurosci 22: 4675, 2002.
5. Bichot NP, Schall JD. Saccade target selection in macaque during feature and conjunction visual search. Vis Neurosci 16: 81-89, 1999b.
6. Bichot NP, Thompson KG, Rao SC, Schall JD. Reliability of macaque frontal eye field neurons signaling saccade targets during visual search. J Neurosci 21: 713-725, 2001.
7. Bisley JW, Goldberg ME. Attention, intention, and priority in the parietal lobe. Annu Rev Neurosci 33: 1-21, 2010.
8. Boucher L, Palmeri TJ, Logan GD, Schall JD. Inhibitory control in mind and brain: an interactive race model of countermanding saccades. Psychol Rev 114: 376-397, 2007.
9. Brown JW, Hanes DP, Schall JD, Stuphorn V. Relation of frontal eye field activity to saccade initiation during a countermanding task. Exp Brain Res 190: 135-151, 2008.
10. Brown S, Heathcote A. A ballistic model of choice response time. Psychol Rev 112: 117-128, 2005.
11. Bruce CJ, Goldberg ME. Primate frontal eye fields. I. Single neurons discharging before saccades. J Neurophysiol 53: 603-635, 1985.
12. 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.
13. Bundesen C, Habekost T, Kyllingsbæk S. A neural theory of visual attention: Bridging cognition and neurophysiology. Psychol Rev 112: 291-328, 2005.
14. Buschman TJ, Miller EK. Serial, covert shifts of attention during visual search are reflected by the frontal eye fields and correlated with population oscillations. Neuron 63: 386-396, 2009.
15. Carpenter RH. Contrast, probability, and saccadic latency: evidence for independence of detection and decision. Curr Biol 14: 1576-1580, 2004.
16. Carpenter RHS, Williams MLL. Neural computation of log likelihood in control of saccadic eye movements. Nature 377: 59-62, 1995.
17. Chang MH, Armstrong KM, Moore T. Dissociation of response variability from firing rate effects in frontal eye field neurons during visual stimulation, working memory, and attention. J Neurosci 32: 2204-2216, 2012.
18. Churchland AK, Kiani R, Chaudhuri R, Wang XJ, Pouget A, Shadlen MN. Variance as a signature of neural computations during decision making. Neuron 69: 818-831, 2011.
19. Churchland MM, Byron MY, Cunningham JP, Sugrue LP, Cohen MR, Corrado GS, Newsome WT, Clark AM, Hosseini P, Scott BB. Stimulus onset quenches neural variability: a widespread cortical phenomenon. Nat Neurosci 13: 369-378, 2010.
20. Churchland MM, Byron MY, Ryu SI, Santhanam G, Shenoy KV. Neural variability in premotor cortex provides a signature of motor preparation. J Neurosci 26: 3697-3712, 2006.
21. 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.
22. Cohen JY, Heitz RP, Woodman GF, Schall JD. Neural basis of the set-size effect in frontal eye field: timing of attention during visual search. J Neurophysiol 101: 1699-1704, 2009.
23. Cohen MR, Maunsell JHR. Attention improves performance primarily by reducing interneuronal correlations. Nat Neurosci 12: 1594-1600, 2009.
24. Cohen MR, Newsome WT. Context-dependent changes in functional circuitry in visual area MT. Neuron 60: 162-173, 2008.
25. Compte A, Brunel N, Goldman-Rakic PS, Wang XJ. Synaptic mechanisms and network dynamics underlying spatial working memory in a cortical network model. Cereb Cortex 10: 910-923, 2000.
26. Dean AF. The variability of discharge of simple cells in the cat striate cortex. Exp Brain Res 44: 437-440, 1981.
27. Duncan J, Humphreys GW. Visual search and stimulus similarity. Psychol Rev 96: 433-458, 1989.
28. Efron B, Tibshirani R. An Introduction to the Bootstrap. Boca Raton, FL: Chapman & Hall/CRC, 1993.
29. Findlay JM, Walker R. A model of saccade generation based on parallel processing and competitive inhibition. Behav Brain Sci 22: 661-674, 1999.
30. Gawne TJ, Kjaer TW, Richmond BJ. Latency: another potential code for feature binding in striate cortex. J Neurophysiol 76: 1356-1360, 1996.
31. Gottlieb J. From thought to action: the parietal cortex as a bridge between perception, action, and cognition. Neuron 53: 9-16, 2007.
32. Gregoriou GG, Gotts SJ, Desimone R. Cell-type-specific synchronization of neural activity in FEF with V4 during attention. Neuron 73: 581-594, 2012.
33. Hanes DP, Patterson WF, Schall JD. Role of frontal eye fields in countermanding saccades: visual, movement, and fixation activity. J Neurophysiol 79: 817-834, 1998.
34. Hanes DP, Schall JD. Neural control of voluntary movement initiation. Science 274: 427-430, 1996.
35. Hartveit E, Heggelund P. Response variability of single cells in the dorsal lateral geniculate nucleus of the cat. Comparison with retinal input and effect of brain stem stimulation. J Neurophysiol 72: 1278-1289, 1994.
36. Hikosaka O, Wurtz RH. Visual and oculomotor functions of monkey substantia nigra pars reticulata. IV. Relation of substantia nigra to superior colliculus. J Neurophysiol 49: 1285-1301, 1983.
37. Huerta MF, Krubitzer LA, Kaas JH. Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys II. Cortical connections. J Comp Neurol 265: 332-361, 1987.
38. Hussar C, Pasternak T. Trial-to-trial variability of the prefrontal neurons reveals the nature of their engagement in a motion discrimination task. Proc Natl Acad Sci USA 107: 21842-21847, 2010.
39. Itti L, Koch C. Computational modelling of visual attention. Nat Rev Neurosci 2: 194-203, 2001.
40. Kara P, Reinagel P, Reid RC. Low response variability in simultaneously recorded retinal, thalamic, and cortical neurons. Neuron 27: 635-646, 2000.
41. Maunsell JH, Ghose GM, Assad JA, McAdams CJ, Boudreau CE, Noerager BD. Visual response latencies of magnocellular and parvocellular LGN neurons in macaque monkeys. Vis Neurosci 16: 1-14, 1999.
42. Mitchell JF, Sundberg KA, Reynolds JH. Differential attention-dependent response modulation across cell classes in macaque visual area V4. Neuron 55: 131-141, 2007.
43. Mitchell JF, Sundberg KA, Reynolds JH. Spatial attention decorrelates intrinsic activity fluctuations in macaque area V4. Neuron 63: 879-888, 2009.
44. Moore T, Armstrong KM. Selective gating of visual signals by microstimulation of frontal cortex. Nature 421: 370-373, 2003.
45. Murthy A, Ray S, Shorter SM, Schall JD, Thompson KG. Neural control of visual search by frontal eye field: effects of unexpected target displacement on visual selection and saccade preparation. J Neurophysiol 101: 2485-2506, 2009.
46. Nelder JA, Mead R. A simplex method for function minimization. Comput J 7: 308, 1965.
47. Oram MW, Xiao D, Dritschel B, Payne KR. The temporal resolution of neural codes: does response latency have a unique role? Philos Trans R Soc Lond B Biol Sci 357: 987-1001, 2002.
48. Palmer J, Verghese P, Pavel M. The psychophysics of visual search. Vision Res 40: 1227-1268, 2000.
49. Pouget P, Emeric EE, Stuphorn V, Reis K, Schall JD. Chronometry of visual responses in frontal eye field, supplementary eye field, and anterior cingulate cortex. J Neurophysiol 94: 2086-2092, 2005.
50. Purcell BA, Heitz RP, Cohen JY, Schall JD, Logan GD, Palmeri TJ. Neurally constrained modeling of perceptual decision making. Psychol Rev 117: 1113-1143, 2010a.
51. Purcell BA, Schall JD, Logan GD, Palmeri TJ. From salience to saccades: multiple-alternative gated stochastic accumulator model of visual search. J Neurosci 32: 3433-3446, 2012a.
52. Purcell BA, Heitz RP, Cohen JY, Woodman GF, Schall JD. Timing of attentional selection in frontal eye field and event-related potentials over visual cortex during pop-out search (Abstract). J Vis 10: 97, 2010b.
53. Purcell BA, Weigand PK, Schall JD. Supplementary eye field during visual search: salience, cognitive control, and performance monitoring. J Neurosci 32: 10273-10285, 2012b.
54. Ratcliff R. A theory of memory retrieval. Psychol Rev 85: 59-108, 1978.
55. Ratcliff R, Cherian A, Segraves M. A comparison of macaque behavior and superior colliculus neuronal activity to predictions from models of twochoice decisions. J Neurophysiol 90: 1392-1407, 2003.
56. Reynolds JH, Pasternak T, Desimone R. Attention increases sensitivity of V4 neurons. Neuron 26: 703-714, 2000.
57. Sadagopan S, Ferster D. Feedforward origins of response variability underlying contrast invariant orientation tuning in cat visual cortex. Neuron 74: 911-923.
58. Sato T, Murthy A, Thompson KG, Schall JD. Search efficiency but not response interference affects visual selection in frontal eye field. Neuron 30: 583-591, 2001.
59. Schall JD, Hanes DP, Thompson KG, King DJ. Saccade target selection in frontal eye field of macaque. I. Visual and premovement activation. J Neurosci 15: 6905-6918, 1995a.
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, 1995b.
61. Schall JD, Sato TR, Thompson KG, Vaughn AA, Juan CH. Effects of search efficiency on surround suppression during visual selection in frontal eye field. J Neurophysiol 91: 2765-2769, 2004.
62. Schall JD, Thompson KG. Neural selection and control of visually guided eye movements. Annu Rev Neurosci 22: 241-259, 1999.
63. Schiller PH, Colby CL. The responses of single cells in the lateral geniculate nucleus of the rhesus monkey to color and luminance contrast. Vision Res 23: 1631-1641, 1983.
64. Schmolesky MT, Wang Y, Hanes DP, Thompson KG, Leutgeb S, Schall JD, Leventhal AG. Signal timing across the macaque visual system. J Neurophysiol 79: 3272-3278, 1998.
65. Scudder CA, Kaneko CS, Fuchs AF. The brainstem burst generator for saccadic eye movements: a modern synthesis. Exp Brain Res 142: 439-462, 2002.
66. Softky WR, Koch C. The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. J Neurosci 13: 334-350, 1993.
67. 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, 1988.
68. Steinmetz NA, Moore T. Changes in the response rate and response variability of area V4 neurons during the preparation of saccadic eye movements. J Neurophysiol 103: 1171-1178, 2010.
69. Thompson KG, Bichot NP. A visual salience map in the primate frontal eye field. Prog Brain Res 147: 249-262, 2005.
70. Thompson KG, Bichot NP, Schall JD. Dissociation of visual discrimination from saccade programming in macaque frontal eye field. J Neurophysiol 77: 1046-1050, 1997.
71. Thompson KG, Biscoe KL, Sato TR. Neuronal basis of covert spatial attention in the frontal eye field. J Neurosci 25: 9479, 2005.
72. Thompson KG, Hanes DP, Bichot NP, Schall JD. Perceptual and motor processing stages identified in the activity of macaque frontal eye field neurons during visual search. J Neurophysiol 76: 4040-4055, 1996.
73. Tolhurst DJ, Movshon JA, Dean AF. The statistical reliability of signals in single neurons in cat and monkey visual cortex. Vision Res 23: 775-785, 1983.
74. Treisman AM, Gelade G. A feature-integration theory of attention. Cogn Psychol 12: 97-136, 1980.
75. Wang XJ. Synaptic basis of cortical persistent activity: the importance of NMDA receptors to working memory. J Neurosci 19: 9587-9603, 1999.
76. White BJ, Munoz DP. Separate visual signals for saccade initiation during target selection in the primate superior colliculus. J Neurosci 31: 1570-1578, 2011.
77. Wichmann FA, Hill NJ. The psychometric function: II. Bootstrap-based confidence intervals and sampling. Percept Psychophys 63: 1314-1329, 2001.
78. Wolfe JM. Guided Search 4.0: Current progress with a model of visual search. In: Integrated Models of Cognitive Systems, edited by Gray W. New York: Oxford, 2007, p. 99-119.
79. Wolfe JM. What can 1 million trials tell us about visual search? Psychol Sci 9: 33-39, 1998.
80. Zhou H, Desimone R. Feature-based attention in the frontal eye field and area V4 during visual search. Neuron 70: 1205-1217, 2011.