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A mechanism for decision rule discrimination by supplementary eye field neurons

Abstract

A decision to select an action from alternatives is often guided by rules that flexibly map sensory inputs to motor outputs when certain conditions are satisfied. However, the neural mechanisms underlying rule-based decision making remain poorly understood. Two complementary types of neurons in the supplementary eye field (SEF) of macaques have been identified that modulate activity differentially to interpret rules in an ocular go–nogo task, which stipulates that the animal either visually pursue a moving object if it intersects a visible zone (‘go’), or maintain fixation if it does not (‘nogo’). These neurons discriminate between go and nogo rule-states by increasing activity to signal their preferred (agonist) rule-state and decreasing activity to signal their non-preferred (antagonist) rule-state. In the current study, we found that SEF neurons decrease activity in anticipation of the antagonist rule-state, and do so more rapidly when the rule-state is easier to predict. This rapid decrease in activity could underlie a process of elimination in which trajectories that do not invoke the preferred rule-state receive no further computational resources. Furthermore, discrimination between difficult and easy trials in the antagonist rule-state occurs prior to when discrimination within the agonist rule-state occurs. A winner-take-all like model that incorporates a pair of mutually inhibited integrators to accumulate evidence in favor of either the decision to pursue or the decision to continue fixation accounts for the observed neural phenomena.

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References

  1. Albantakis L, Deco G (2011) Changes of mind in an attractor network of decision-making. PLoS Comput Biol 7:e1002086

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  2. Asaad WF, Rainer G, Miller EK (1998) Neural activity in the primate prefrontal cortex during associative learning. Neuron 21:1399–1407

    CAS  PubMed  Article  Google Scholar 

  3. Asaad WF, Rainer G, Miller EK (2000) Task-specific neural activity in the primate prefrontal cortex. J Neurophysiol 84:451–459

    CAS  PubMed  Google Scholar 

  4. Badre D, Kayser AS, D’Esposito M (2010) Frontal cortex and the discovery of abstract action rules. Neuron 66:315–326

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  5. Bengtsson SL, Haynes J-D, Sakai K, Buckley MJ, Passingham RE (2009) The representation of abstract task rules in the human prefrontal cortex. Cereb Cortex 19:1929–1936

    PubMed Central  PubMed  Article  Google Scholar 

  6. Bennur S, Gold JI (2011) Distinct representations of a perceptual decision and the associated oculomotor plan in the monkey lateral intraparietal area. J Neurosci 31:913–921

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  7. Bodis-Wollner I (2008) Pre-emptive perception. Perception 37:462–478

    PubMed  Article  Google Scholar 

  8. Bogacz R, Usher M, Zhang J, McClelland JL (2007) Extending a biologically inspired model of choice: multi-alternatives, nonlinearity and value-based multidimensional choice. Philos Trans R Soc Lond B Biol Sci 362:1655–1670

    PubMed Central  PubMed  Article  Google Scholar 

  9. Boucher L, Palmeri TJ, Logan GD, Schall JD (2007) Inhibitory control in mind and brain: an interactive race model of countermanding saccades. Psychol Rev 114:376–397

    PubMed  Article  Google Scholar 

  10. Brainard DH (1997) The psychophysics toolbox. Spat Vis 10:433–436

    CAS  PubMed  Article  Google Scholar 

  11. Bremmer F, Distler C, Hoffmann KP (1997) Eye position effects in monkey cortex. II. Pursuit- and fixation-related activity in posterior parietal areas LIP and 7A. J Neurophysiol 77:962–977

    CAS  PubMed  Google Scholar 

  12. Britten KH, Shadlen MN, Newsome WT, Movshon JA (1992) The analysis of visual motion: a comparison of neuronal and psychophysical performance. J Neurosci 12:4745–4765

    CAS  PubMed  Google Scholar 

  13. Bunge SA (2004) How we use rules to select actions: a review of evidence from cognitive neuroscience. Cogn Affect Behav Neurosci 4:564–579

    PubMed  Article  Google Scholar 

  14. Bunge SA, Kahn I, Wallis JD, Miller EK, Wagner AD (2003) Neural circuits subserving the retrieval and maintenance of abstract rules. J Neurophysiol 90:3419–3428

    PubMed  Article  Google Scholar 

  15. Chen LL, Wise SP (1995) Neuronal activity in the supplementary eye field during acquisition of conditional oculomotor associations. J Neurophysiol 73:1101–1121

    CAS  PubMed  Google Scholar 

  16. Chen LL, Wise SP (1996) Evolution of directional preferences in the supplementary eye field during acquisition of conditional oculomotor associations. J Neurosci 16:3067–3081

    CAS  PubMed  Google Scholar 

  17. Cisek P (2006) Integrated neural processes for defining potential actions and deciding between them: a computational model. J Neurosci 26:9761–9770

    CAS  PubMed  Article  Google Scholar 

  18. Cisek P (2007) Cortical mechanisms of action selection: the affordance competition hypothesis. Philos Trans R Soc Lond B Biol Sci 362:1585–1599

    PubMed Central  PubMed  Article  Google Scholar 

  19. Cisek P, Kalaska JF (2005) Neural correlates of reaching decisions in dorsal premotor cortex: specification of multiple direction choices and final selection of action. Neuron 45:801–814

    CAS  PubMed  Article  Google Scholar 

  20. Cisek P, Kalaska JF (2010) Neural mechanisms for interacting with a world full of action choices. Annu Rev Neurosci 33:269–298

    CAS  PubMed  Article  Google Scholar 

  21. Coe B, Tomihara K, Matsuzawa M, Hikosaka O (2002) Visual and anticipatory bias in three cortical eye fields of the monkey during an adaptive decision-making task. J Neurosci 22:5081–5090

    CAS  PubMed  Google Scholar 

  22. Cromer JA, Roy JE, Miller EK (2010) Representation of multiple, independent categories in the primate prefrontal cortex. Neuron 66:796–807

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  23. Cui H, Andersen RA (2007) Posterior parietal cortex encodes autonomously selected motor plans. Neuron 56:552–559

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  24. de Hemptinne C, Lefèvre P, Missal M (2008) Neuronal bases of directional expectation and anticipatory pursuit. J Neurosci 28:4298–4310

    PubMed  Article  CAS  Google Scholar 

  25. Deco G, Rolls ET, Albantakis L, Romo R (2012). Brain mechanisms for perceptual and reward-related decision-making. Progr Neurobiol. doi:10.1016/j.pneurobio.2012.01.010

  26. Dicke PW, Barash S, Ilg UJ, Thier P (2004) 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

    PubMed  Article  Google Scholar 

  27. Ding L, Gold JI (2010) Caudate encodes multiple computations for perceptual decisions. J Neurosci 30:15747–15759

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  28. Ding L, Gold JI (2011) Neural correlates of perceptual decision making before, during, and after decision commitment in monkey frontal eye field. Cereb Cortex 22:1052–1067

    PubMed Central  PubMed  Article  Google Scholar 

  29. Ditterich J (2010) A comparison between mechanisms of multi-alternative perceptual decision making: ability to explain human behavior, predictions for neurophysiology, and relationship with decision theory. Front Neurosci 4(184):1–24

    Google Scholar 

  30. Duffy CJ, Wurtz RH (1997a) Medial superior temporal area neurons respond to speed patterns in optic flow. J Neurosci 17:2839–2851

    CAS  PubMed  Google Scholar 

  31. Duffy CJ, Wurtz RH (1997b) Planar directional contributions to optic flow responses in MST neurons. J Neurophysiol 77:782–796

    CAS  PubMed  Google Scholar 

  32. Duque J, Ivry RB (2009) Role of corticospinal suppression during motor preparation. Cereb Cortex 19:2013–2024

    PubMed Central  PubMed  Article  Google Scholar 

  33. Feng S, Holmes P, Rorie A, Newsome WT (2009) Can monkeys choose optimally when faced with noisy stimuli and unequal rewards? PLoS Comput Biol 5:e1000284

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  34. Ferrera VP, Yanike M, Cassanello C (2009) Frontal eye field neurons signal changes in decision criteria. Nat Neurosci 12:1458–1462

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  35. Freedman DJ, Assad JA (2006) Experience-dependent representation of visual categories in parietal cortex. Nature 443:85–88

    CAS  PubMed  Article  Google Scholar 

  36. Freedman DJ, Riesenhuber M, Poggio T, Miller EK (2001) Categorical representation of visual stimuli in the primate prefrontal cortex. Science 312:291–316

    Google Scholar 

  37. Fukushima J, Akao T, Takeichi N, Kurkin S, Kaneko CRS, Fukushima K (2004) Pursuit-related neurons in the supplementary eye fields: discharge during pursuit and passive whole body rotation. J Neurophysiol 91:2809–2825

    PubMed  Article  Google Scholar 

  38. Fukushima J, Akao T, Shichinohe N, Kurkin S, Kaneko CRS, Fukushima K (2011) Neuronal activity in the caudal frontal eye fields of monkeys during memory-based smooth pursuit eye movements: comparison with the supplementary eye fields. Cereb Cortex 21:1910–1924

    PubMed Central  PubMed  Article  Google Scholar 

  39. Genovesio A, Tsujimoto S, Wise SP (2011) Prefrontal cortex activity during the discrimination of relative distance. J Neurosci 31:3968–3980

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  40. Gold JI, Shadlen MN (2003) The influence of behavioral context on the representation of a perceptual decision in developing oculomotor commands. J Neurosci 23:632–651

    CAS  PubMed  Google Scholar 

  41. Gold JI, Shadlen MN (2007) The neural basis of decision making. Annu Rev Neurosci 30:535–574

    CAS  PubMed  Article  Google Scholar 

  42. Gottlieb JP, MacAvoy MG, Bruce CJ (1994) 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

    CAS  PubMed  Google Scholar 

  43. Green DM, Swets JA (1966) Signal detectability and psychophysics. Wiley, New York

    Google Scholar 

  44. Hanes DP, Schall JD (1996) Neural control of voluntary movement initiation. Science 274:427–430

    CAS  PubMed  Article  Google Scholar 

  45. Hanks TD, Mazurek ME, Kiani R, Hopp E, Shadlen MN (2011) Elapsed decision time affects the weighting of prior probability in a perceptual decision task. J Neurosci 31:6339–6352

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  46. Hasegawa RP, Peterson BW, Goldberg ME (2004) Prefrontal neurons coding suppression of specific saccades. Neuron 43:415–425

    CAS  PubMed  Article  Google Scholar 

  47. Heinen SJ (1995) Single neuron activity in the dorsomedial frontal cortex during smooth pursuit eye movements. Exp Brain Res 104:357–361

    CAS  PubMed  Article  Google Scholar 

  48. Heinen SJ, Liu M (1997) Single-neuron activity in the dorsomedial frontal cortex during smooth-pursuit eye movements to predictable target motion. Vis Neurosci 14:853–866

    CAS  PubMed  Article  Google Scholar 

  49. Heinen SJ, Hwang H, Yang S (2011) Flexible interpretation of a decision rule by supplementary eye field neurons. J Neurophysiol 106:2992–3000

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  50. Horwitz GD, Newsome WT (1999) Separate signals for target selection and movement specification in the superior colliculus. Science 284:1158–1161

    CAS  PubMed  Article  Google Scholar 

  51. Horwitz GD, Batista AP, Newsome WT (2004) Representation of an abstract perceptual decision in macaque superior colliculus. J Neurophysiol 91:2281–2296

    PubMed  Article  Google Scholar 

  52. Huerta MF, Kaas JH (1990) Supplementary eye field as defined by intracortical microstimulation: connections in macaques. J Comp Neurol 293:299–330

    CAS  PubMed  Article  Google Scholar 

  53. Jantz JJ, Watanabe M, Everling S, Munoz DP (2013) Threshold mechanism for saccade initiation in the frontal eye field and superior colliculus. J Neurophysiol

  54. Keating EG (1991) Frontal eye field lesions impair predictive and visually-guided pursuit eye movements. Exp Brain Res 86:311–323

    CAS  PubMed  Article  Google Scholar 

  55. Khayat PS, Spekreijse H, Roelfsema PR (2006) Attention lights up new object representations before the old ones fade away. J Neurosci 26:138–142

    CAS  PubMed  Article  Google Scholar 

  56. Kim JN, Shadlen MN (1999) Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque. Nat Neurosci 2:176–185

    PubMed  Article  Google Scholar 

  57. Kim YG, Badler JB, Heinen SJ (2005) Trajectory interpretation by supplementary eye field neurons during ocular baseball. J Neurophysiol 94:1385–1391

    PubMed  Article  Google Scholar 

  58. Klaes C, Westendorff S, Chakrabarti S, Gail A (2011) Choosing goals, not rules: deciding among rule-based action plans. Neuron 70:536–548

    CAS  PubMed  Article  Google Scholar 

  59. Koch G, Franca M, Del Olmo MF, Cheeran B, Milton R, Sauco MA, Rothwell JC (2006) Time course of functional connectivity between dorsal premotor and contralateral motor cortex during movement selection. J Neurosci 26:7452–7459

    CAS  PubMed  Article  Google Scholar 

  60. Krauzlis RJ (2001) Extraretinal inputs to neurons in the rostral superior colliculus of the monkey during smooth-pursuit eye movements. J Neurophysiol 86:2629–2633

    CAS  PubMed  Google Scholar 

  61. Krauzlis RJ, Dill N (2002) Neural correlates of target choice for pursuit and saccades in the primate superior colliculus. Neuron 35:355–363

    CAS  PubMed  Article  Google Scholar 

  62. 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

    CAS  PubMed  Google Scholar 

  63. Leichnetz GR, Smith DJ, Spencer RF (1984) Cortical projections to the paramedian tegmental and basilar pons in the monkey. J Comp Neurol 228:388–408

    CAS  PubMed  Article  Google Scholar 

  64. Lo CC, Wang XJ (2006) Cortico-basal ganglia circuit mechanism for a decision threshold in reaction time tasks. Nat Neurosci 9:956–963

    CAS  PubMed  Article  Google Scholar 

  65. Loh M, Deco G (2005) Cognitive flexibility and decision-making in a model of conditional visuomotor associations. Eur J Neurosci 22:2927–2936

    PubMed  Article  Google Scholar 

  66. Machens CK, Romo R, Brody CD (2005) Flexible control of mutual inhibition: a neural model of two-interval discrimination. Science 307:1121–1124

    CAS  PubMed  Article  Google Scholar 

  67. MacMillan NA, Creelman CD (1991) Detection theory: a user’s guide. Cambridge University Press, Cambridge

    Google Scholar 

  68. Maunsell JH, Van Essen DC (1983a) Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. J Neurophysiol 49:1127–1147

    CAS  PubMed  Google Scholar 

  69. Maunsell JH, Van Essen DC (1983b) The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey. J Neurosci 3:2563–2586

    CAS  PubMed  Google Scholar 

  70. Mazurek ME, Roitman JD, Ditterich J, Shadlen MN (2003) A role for neural integrators in perceptual decision making. Cereb Cortex 13:1257–1269

    PubMed  Article  Google Scholar 

  71. Mcmillen T, Holmes P (2006) The dynamics of choice among multiple alternatives. J Math Psychol 50:30–57

    Article  Google Scholar 

  72. McPeek RM (2006) Incomplete suppression of distractor-related activity in the frontal eye field results in curved saccades. J Neurophysiol 96:2699–2711

    PubMed Central  PubMed  Article  Google Scholar 

  73. Missal M, Heinen SJ (2001) Facilitation of smooth pursuit initiation by electrical stimulation in the supplementary eye fields. J Neurophysiol 86:2413–2425

    CAS  PubMed  Google Scholar 

  74. Mitz AR, Godschalk M, Wise SP (1991) Learning-dependent neuronal activity in the premotor cortex: activity during the acquisition of conditional motor associations. J Neurosci 11:1855–1872

    CAS  PubMed  Google Scholar 

  75. Motter BC (1994) Neural correlates of attentive selection for color or luminance in extrastriate area V4. J Neurosci 14:2178–2189

    CAS  PubMed  Google Scholar 

  76. Muhammad R, Wallis JD, Miller EK (2006) A comparison of abstract rules in the prefrontal cortex, premotor cortex, inferior temporal cortex, and striatum. J Cogn Neurosci 18:974–989

    PubMed  Article  Google Scholar 

  77. Munoz DP, Wurtz RH (1995) Saccade-related activity in monkey superior colliculus. I. Characteristics of burst and buildup cells. J Neurophysiol 73:2313–2333

    CAS  PubMed  Google Scholar 

  78. Murthy A, Ray S, Shorter SM, Schall JD, Thompson KG (2009) 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

    PubMed Central  PubMed  Article  Google Scholar 

  79. Newsome WT, Paré EB (1988) A selective impairment of motion perception following lesions of the middle temporal visual area (MT). J Neurosci 8:2201–2211

    CAS  PubMed  Google Scholar 

  80. Ono S, Mustari MJ (2006) Extraretinal signals in MSTd neurons related to volitional smooth pursuit. J Neurophysiol 96:2819–2825

    PubMed  Article  Google Scholar 

  81. Ono S, Mustari MJ (2009) Smooth pursuit-related information processing in frontal eye field neurons that project to the NRTP. Cereb Cortex 19:1186–1197

    PubMed Central  PubMed  Article  Google Scholar 

  82. Orban GA (2008) Higher order visual processing in macaque extrastriate cortex. Physiol Rev 88:59–89

    PubMed  Article  Google Scholar 

  83. Orban GA, Lagae L, Raiguel S, Xiao D, Maes H (1995) The speed tuning of medial superior temporal (MST) cell responses to optic-flow components. Perception 24:269–286

    CAS  PubMed  Article  Google Scholar 

  84. Oster M, Douglas R, Liu SC (2009) Computation with spikes in a winner-take-all network. Neural Comput 21:2437–2465

    PubMed  Article  Google Scholar 

  85. Pouget P, Emeric EE, Stuphorn V, Reis K, Schall JD (2005) Chronometry of visual responses in frontal eye field, supplementary eye field, and anterior cingulate cortex. J Neurophysiol 94:2086–2092

    PubMed  Article  Google Scholar 

  86. Purcell BA, Schall JD, Logan GD, Palmeri TJ (2012) From salience to saccades: multiple-alternative gated stochastic accumulator model of visual search. J Neurosci 32:3433–3446

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  87. Ratcliff R, Cherian A, Segraves MA (2003) A comparison of macaque behavior and superior colliculus neuronal activity to predictions from models of two-choice decisions. J neurophysiol 90(3):1392–1407

  88. Ratcliff R, Hasegawa YT, Hasegawa RP, Smith PL, Segraves MA (2007) Dual diffusion model for single-cell recording data from the superior colliculus in a brightness-discrimination task. J neurophysiol 97(2):1756–1774

  89. Ray S, Pouget P, Schall JD (2009) Functional distinction between visuomovement and movement neurons in macaque frontal eye field during saccade countermanding. J Neurophysiol 102:3091–3100

    PubMed Central  PubMed  Article  Google Scholar 

  90. Ray S, Bhutani N, Murthy A (2012) Mutual inhibition and capacity sharing during parallel preparation of serial eye movements. J Vis 12(3):17

    PubMed  Article  Google Scholar 

  91. Recanzone GH, Wurtz RH, Schwarz U (1997) Responses of MT and MST neurons to one and two moving objects in the receptive field. J Neurophysiol 78:2904–2915

    CAS  PubMed  Google Scholar 

  92. Roitman JD, Shadlen MN (2002) Response of neurons in the lateral intraparietal area during a combined visual discrimination reaction time task. J Neurosci 22:9475–9489

    CAS  PubMed  Google Scholar 

  93. Romo R, Merchant H, Zainos A, Hernández A (1997) Categorical perception of somesthetic stimuli: psychophysical measurements correlated with neuronal events in primate medial premotor cortex. Cereb Cortex 7:317–326

    CAS  PubMed  Article  Google Scholar 

  94. Roxin A, Ledberg A (2008) Neurobiological models of two-choice decision making can be reduced to a one-dimensional nonlinear diffusion equation. PLoS Comput Biol 4(3):e1000046

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  95. Roy JE, Riesenhuber M, Poggio T, Miller EK (2010) Prefrontal cortex activity during flexible categorization. J Neurosci 30:8519–8528

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  96. Sakata H, Shibutani H, Kawano K (1983) Functional properties of visual tracking neurons in posterior parietal association cortex of the monkey. J Neurophysiol 49:1364–1380

    CAS  PubMed  Google Scholar 

  97. Salinas E, Romo R (1998) Conversion of sensory signals into motor commands in primary motor cortex. J Neurosci 18:499–511

    CAS  PubMed  Google Scholar 

  98. Salzman CD, Britten KH, Newsome WT (1990) Cortical microstimulation influences perceptual judgements of motion direction. Nature 346:174–177

    CAS  PubMed  Article  Google Scholar 

  99. Sato TR, Schall JD (2003) Effects of stimulus-response compatibility on neural selection in frontal eye field. Neuron 38:637–648

    CAS  PubMed  Article  Google Scholar 

  100. Schall JD (2004) On building a bridge between brain and behavior. Annu Rev Psychol 55:23–50

    PubMed  Article  Google Scholar 

  101. Schlag J, Schlag-Rey M (1987) Evidence for a supplementary eye field. J Neurophysiol 57:179–200

    CAS  PubMed  Google Scholar 

  102. Shadlen MN, Newsome WT (2001) Neural basis of a perceptual decision in the parietal cortex (Area LIP) of the rhesus monkey. J Neurophysiol 86:1916–1936

    CAS  PubMed  Google Scholar 

  103. Shichinohe N, Akao T, Kurkin S, Fukushima J, Kaneko CRS, Fukushima K (2009) Memory and decision making in the frontal cortex during visual motion processing for smooth pursuit eye movements. Neuron 62:717–732

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  104. Shook BL, Schlag-Rey M, Schlag J (1990) Primate supplementary eye field: I. Comparative aspects of mesencephalic and pontine connections. J Comp Neurol 301:618–642

    CAS  PubMed  Article  Google Scholar 

  105. Smith PL, Ratcliff R (2004) Psychology and neurobiology of simple decisions. Trends Neurosci 27:161–168

    CAS  PubMed  Article  Google Scholar 

  106. So N-Y, Stuphorn V (2010) Supplementary eye field encodes option and action value for saccades with variable reward. J Neurophysiol 104:2634–2653

    PubMed Central  PubMed  Article  Google Scholar 

  107. Song JH, McPeek RM (2010) Roles of narrow- and broad-spiking dorsal premotor area neurons in reach target selection and movement production. J Neurophysiol 103:2124–2138

    PubMed Central  PubMed  Article  Google Scholar 

  108. Suzuki DA, Yamada T, Yee RD (2003) Smooth-pursuit eye-movementrelated neuronal activity in macaque nucleus reticularis tegmenti pontis. J Neurophysiol 89:2146–2158

    PubMed  Article  Google Scholar 

  109. Tanaka M, Fukushima K (1998) Neuronal responses related to smooth pursuit eye movements in the periarcuate cortical area of monkeys. J Neurophysiol 80:28–47

    CAS  PubMed  Google Scholar 

  110. Tanaka M, Lisberger SG (2002) Role of arcuate frontal cortex of monkeys in smooth pursuit eye movements. I. Basic response properties to retinal image motion and position. J Neurophysiol 87:2684–2699

    PubMed Central  PubMed  Google Scholar 

  111. Tanaka K, Saito HA (1989) Analysis of motion of the visual field by direction, expansion/contraction, and rotation cells clustered in the dorsal part of the medial superior temporal area of the macaque monkey. J Neurophysiol 62:626–641

    CAS  PubMed  Google Scholar 

  112. Teller DY (1984) Linking propositions. Vision Res 24:1233–1246

    CAS  PubMed  Article  Google Scholar 

  113. Tian JR, Lynch JC (1995) Slow and saccadic eye movements evoked by microstimulation in the supplementary eye field of the cebus monkey. J Neurophysiol 74:2204–2210

    CAS  PubMed  Google Scholar 

  114. Usher M, McClelland JL (2001) The time course of perceptual choice: the leaky, competing accumulator model. Psychol Rev 108:550–592

    CAS  PubMed  Article  Google Scholar 

  115. Wallis JD, Miller EK (2003) From rule to response: neuronal processes in the premotor and prefrontal cortex. J Neurophysiol 90:1790–1806

    PubMed  Article  Google Scholar 

  116. Wallis JD, Anderson KC, Miller EK (2001) Single neurons in prefrontal cortex encode abstract rules. Nature 411:953–956

    CAS  PubMed  Article  Google Scholar 

  117. Wang XJ (2002) Probabilistic decision making by slow reverberation in cortical circuits. Neuron 36:955–968

    CAS  PubMed  Article  Google Scholar 

  118. White IM, Wise SP (1999) Rule-dependent neuronal activity in the prefrontal cortex. Exp Brain Res 126:315–335

    CAS  PubMed  Article  Google Scholar 

  119. Yang S-n, Hwang H, Ford J, Heinen S (2010) Supplementary eye field activity reflects a decision rule governing smooth pursuit but not the decision. J Neurophysiol 103:2458–2469

    PubMed Central  PubMed  Article  Google Scholar 

  120. Zhang J (2012) The effects of evidence bounds on decision-making: theoretical and empirical developments. Front Psychol 3

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Acknowledgments

This study was supported by grants from National Eye Institute (EY-117720) and The Smith-Kettlewell Eye Research Institute.

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Correspondence to Supriya Ray.

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Ray, S., Heinen, S.J. A mechanism for decision rule discrimination by supplementary eye field neurons. Exp Brain Res 233, 459–476 (2015). https://doi.org/10.1007/s00221-014-4127-2

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Keywords

  • Abstract rule
  • Accumulator model
  • Decision making
  • Primates
  • Smooth pursuit
  • Supplementary eye field