Experimental Brain Research

, Volume 233, Issue 2, pp 459–476 | Cite as

A mechanism for decision rule discrimination by supplementary eye field neurons

  • Supriya Ray
  • Stephen J. Heinen
Research Article


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.


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



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


  1. Albantakis L, Deco G (2011) Changes of mind in an attractor network of decision-making. PLoS Comput Biol 7:e1002086PubMedCentralPubMedCrossRefGoogle Scholar
  2. Asaad WF, Rainer G, Miller EK (1998) Neural activity in the primate prefrontal cortex during associative learning. Neuron 21:1399–1407PubMedCrossRefGoogle Scholar
  3. Asaad WF, Rainer G, Miller EK (2000) Task-specific neural activity in the primate prefrontal cortex. J Neurophysiol 84:451–459PubMedGoogle Scholar
  4. Badre D, Kayser AS, D’Esposito M (2010) Frontal cortex and the discovery of abstract action rules. Neuron 66:315–326PubMedCentralPubMedCrossRefGoogle 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 19:1929–1936PubMedCentralPubMedCrossRefGoogle 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 31:913–921PubMedCentralPubMedCrossRefGoogle Scholar
  7. Bodis-Wollner I (2008) Pre-emptive perception. Perception 37:462–478PubMedCrossRefGoogle 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 362:1655–1670PubMedCentralPubMedCrossRefGoogle 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 114:376–397PubMedCrossRefGoogle Scholar
  10. Brainard DH (1997) The psychophysics toolbox. Spat Vis 10:433–436PubMedCrossRefGoogle 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 77:962–977PubMedGoogle 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 12:4745–4765PubMedGoogle Scholar
  13. Bunge SA (2004) How we use rules to select actions: a review of evidence from cognitive neuroscience. Cogn Affect Behav Neurosci 4:564–579PubMedCrossRefGoogle 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 90:3419–3428PubMedCrossRefGoogle Scholar
  15. Chen LL, Wise SP (1995) Neuronal activity in the supplementary eye field during acquisition of conditional oculomotor associations. J Neurophysiol 73:1101–1121PubMedGoogle Scholar
  16. Chen LL, Wise SP (1996) Evolution of directional preferences in the supplementary eye field during acquisition of conditional oculomotor associations. J Neurosci 16:3067–3081PubMedGoogle Scholar
  17. Cisek P (2006) Integrated neural processes for defining potential actions and deciding between them: a computational model. J Neurosci 26:9761–9770PubMedCrossRefGoogle Scholar
  18. Cisek P (2007) Cortical mechanisms of action selection: the affordance competition hypothesis. Philos Trans R Soc Lond B Biol Sci 362:1585–1599PubMedCentralPubMedCrossRefGoogle 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 45:801–814PubMedCrossRefGoogle Scholar
  20. Cisek P, Kalaska JF (2010) Neural mechanisms for interacting with a world full of action choices. Annu Rev Neurosci 33:269–298PubMedCrossRefGoogle 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 22:5081–5090PubMedGoogle Scholar
  22. Cromer JA, Roy JE, Miller EK (2010) Representation of multiple, independent categories in the primate prefrontal cortex. Neuron 66:796–807PubMedCentralPubMedCrossRefGoogle Scholar
  23. Cui H, Andersen RA (2007) Posterior parietal cortex encodes autonomously selected motor plans. Neuron 56:552–559PubMedCentralPubMedCrossRefGoogle Scholar
  24. de Hemptinne C, Lefèvre P, Missal M (2008) Neuronal bases of directional expectation and anticipatory pursuit. J Neurosci 28:4298–4310PubMedCrossRefGoogle 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 19:609–624PubMedCrossRefGoogle Scholar
  27. Ding L, Gold JI (2010) Caudate encodes multiple computations for perceptual decisions. J Neurosci 30:15747–15759PubMedCentralPubMedCrossRefGoogle 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 22:1052–1067PubMedCentralPubMedCrossRefGoogle 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):1–24Google Scholar
  30. Duffy CJ, Wurtz RH (1997a) Medial superior temporal area neurons respond to speed patterns in optic flow. J Neurosci 17:2839–2851PubMedGoogle Scholar
  31. Duffy CJ, Wurtz RH (1997b) Planar directional contributions to optic flow responses in MST neurons. J Neurophysiol 77:782–796PubMedGoogle Scholar
  32. Duque J, Ivry RB (2009) Role of corticospinal suppression during motor preparation. Cereb Cortex 19:2013–2024PubMedCentralPubMedCrossRefGoogle 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:e1000284PubMedCentralPubMedCrossRefGoogle Scholar
  34. Ferrera VP, Yanike M, Cassanello C (2009) Frontal eye field neurons signal changes in decision criteria. Nat Neurosci 12:1458–1462PubMedCentralPubMedCrossRefGoogle Scholar
  35. Freedman DJ, Assad JA (2006) Experience-dependent representation of visual categories in parietal cortex. Nature 443:85–88PubMedCrossRefGoogle Scholar
  36. Freedman DJ, Riesenhuber M, Poggio T, Miller EK (2001) Categorical representation of visual stimuli in the primate prefrontal cortex. Science 312:291–316Google 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 91:2809–2825PubMedCrossRefGoogle 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 21:1910–1924PubMedCentralPubMedCrossRefGoogle Scholar
  39. Genovesio A, Tsujimoto S, Wise SP (2011) Prefrontal cortex activity during the discrimination of relative distance. J Neurosci 31:3968–3980PubMedCentralPubMedCrossRefGoogle 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 23:632–651PubMedGoogle Scholar
  41. Gold JI, Shadlen MN (2007) The neural basis of decision making. Annu Rev Neurosci 30:535–574PubMedCrossRefGoogle 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 72:1634–1653PubMedGoogle Scholar
  43. Green DM, Swets JA (1966) Signal detectability and psychophysics. Wiley, New YorkGoogle Scholar
  44. Hanes DP, Schall JD (1996) Neural control of voluntary movement initiation. Science 274:427–430PubMedCrossRefGoogle 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 31:6339–6352PubMedCentralPubMedCrossRefGoogle Scholar
  46. Hasegawa RP, Peterson BW, Goldberg ME (2004) Prefrontal neurons coding suppression of specific saccades. Neuron 43:415–425PubMedCrossRefGoogle Scholar
  47. Heinen SJ (1995) Single neuron activity in the dorsomedial frontal cortex during smooth pursuit eye movements. Exp Brain Res 104:357–361PubMedCrossRefGoogle 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 14:853–866PubMedCrossRefGoogle Scholar
  49. Heinen SJ, Hwang H, Yang S (2011) Flexible interpretation of a decision rule by supplementary eye field neurons. J Neurophysiol 106:2992–3000PubMedCentralPubMedCrossRefGoogle Scholar
  50. Horwitz GD, Newsome WT (1999) Separate signals for target selection and movement specification in the superior colliculus. Science 284:1158–1161PubMedCrossRefGoogle Scholar
  51. Horwitz GD, Batista AP, Newsome WT (2004) Representation of an abstract perceptual decision in macaque superior colliculus. J Neurophysiol 91:2281–2296PubMedCrossRefGoogle Scholar
  52. Huerta MF, Kaas JH (1990) Supplementary eye field as defined by intracortical microstimulation: connections in macaques. J Comp Neurol 293:299–330PubMedCrossRefGoogle 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 NeurophysiolGoogle Scholar
  54. Keating EG (1991) Frontal eye field lesions impair predictive and visually-guided pursuit eye movements. Exp Brain Res 86:311–323PubMedCrossRefGoogle Scholar
  55. Khayat PS, Spekreijse H, Roelfsema PR (2006) Attention lights up new object representations before the old ones fade away. J Neurosci 26:138–142PubMedCrossRefGoogle Scholar
  56. Kim JN, Shadlen MN (1999) Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque. Nat Neurosci 2:176–185PubMedCrossRefGoogle Scholar
  57. Kim YG, Badler JB, Heinen SJ (2005) Trajectory interpretation by supplementary eye field neurons during ocular baseball. J Neurophysiol 94:1385–1391PubMedCrossRefGoogle Scholar
  58. Klaes C, Westendorff S, Chakrabarti S, Gail A (2011) Choosing goals, not rules: deciding among rule-based action plans. Neuron 70:536–548PubMedCrossRefGoogle 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 26:7452–7459PubMedCrossRefGoogle Scholar
  60. Krauzlis RJ (2001) Extraretinal inputs to neurons in the rostral superior colliculus of the monkey during smooth-pursuit eye movements. J Neurophysiol 86:2629–2633PubMedGoogle Scholar
  61. Krauzlis RJ, Dill N (2002) Neural correlates of target choice for pursuit and saccades in the primate superior colliculus. Neuron 35:355–363PubMedCrossRefGoogle 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 84:876–891PubMedGoogle Scholar
  63. Leichnetz GR, Smith DJ, Spencer RF (1984) Cortical projections to the paramedian tegmental and basilar pons in the monkey. J Comp Neurol 228:388–408PubMedCrossRefGoogle Scholar
  64. Lo CC, Wang XJ (2006) Cortico-basal ganglia circuit mechanism for a decision threshold in reaction time tasks. Nat Neurosci 9:956–963PubMedCrossRefGoogle Scholar
  65. Loh M, Deco G (2005) Cognitive flexibility and decision-making in a model of conditional visuomotor associations. Eur J Neurosci 22:2927–2936PubMedCrossRefGoogle Scholar
  66. Machens CK, Romo R, Brody CD (2005) Flexible control of mutual inhibition: a neural model of two-interval discrimination. Science 307:1121–1124PubMedCrossRefGoogle Scholar
  67. MacMillan NA, Creelman CD (1991) Detection theory: a user’s guide. Cambridge University Press, CambridgeGoogle 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 49:1127–1147PubMedGoogle 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 3:2563–2586PubMedGoogle Scholar
  70. Mazurek ME, Roitman JD, Ditterich J, Shadlen MN (2003) A role for neural integrators in perceptual decision making. Cereb Cortex 13:1257–1269PubMedCrossRefGoogle Scholar
  71. Mcmillen T, Holmes P (2006) The dynamics of choice among multiple alternatives. J Math Psychol 50:30–57CrossRefGoogle Scholar
  72. McPeek RM (2006) Incomplete suppression of distractor-related activity in the frontal eye field results in curved saccades. J Neurophysiol 96:2699–2711PubMedCentralPubMedCrossRefGoogle Scholar
  73. Missal M, Heinen SJ (2001) Facilitation of smooth pursuit initiation by electrical stimulation in the supplementary eye fields. J Neurophysiol 86:2413–2425PubMedGoogle 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 11:1855–1872PubMedGoogle Scholar
  75. Motter BC (1994) Neural correlates of attentive selection for color or luminance in extrastriate area V4. J Neurosci 14:2178–2189PubMedGoogle 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 18:974–989PubMedCrossRefGoogle Scholar
  77. Munoz DP, Wurtz RH (1995) Saccade-related activity in monkey superior colliculus. I. Characteristics of burst and buildup cells. J Neurophysiol 73:2313–2333PubMedGoogle 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 101:2485–2506PubMedCentralPubMedCrossRefGoogle Scholar
  79. Newsome WT, Paré EB (1988) A selective impairment of motion perception following lesions of the middle temporal visual area (MT). J Neurosci 8:2201–2211PubMedGoogle Scholar
  80. Ono S, Mustari MJ (2006) Extraretinal signals in MSTd neurons related to volitional smooth pursuit. J Neurophysiol 96:2819–2825PubMedCrossRefGoogle Scholar
  81. Ono S, Mustari MJ (2009) Smooth pursuit-related information processing in frontal eye field neurons that project to the NRTP. Cereb Cortex 19:1186–1197PubMedCentralPubMedCrossRefGoogle Scholar
  82. Orban GA (2008) Higher order visual processing in macaque extrastriate cortex. Physiol Rev 88:59–89PubMedCrossRefGoogle 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 24:269–286PubMedCrossRefGoogle Scholar
  84. Oster M, Douglas R, Liu SC (2009) Computation with spikes in a winner-take-all network. Neural Comput 21:2437–2465PubMedCrossRefGoogle 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 94:2086–2092PubMedCrossRefGoogle 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 32:3433–3446PubMedCentralPubMedCrossRefGoogle 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):1392–1407Google Scholar
  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):1756–1774Google Scholar
  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 102:3091–3100PubMedCentralPubMedCrossRefGoogle 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):17PubMedCrossRefGoogle 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 78:2904–2915PubMedGoogle 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 22:9475–9489PubMedGoogle 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 7:317–326PubMedCrossRefGoogle 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):e1000046PubMedCentralPubMedCrossRefGoogle Scholar
  95. Roy JE, Riesenhuber M, Poggio T, Miller EK (2010) Prefrontal cortex activity during flexible categorization. J Neurosci 30:8519–8528PubMedCentralPubMedCrossRefGoogle 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 49:1364–1380PubMedGoogle Scholar
  97. Salinas E, Romo R (1998) Conversion of sensory signals into motor commands in primary motor cortex. J Neurosci 18:499–511PubMedGoogle Scholar
  98. Salzman CD, Britten KH, Newsome WT (1990) Cortical microstimulation influences perceptual judgements of motion direction. Nature 346:174–177PubMedCrossRefGoogle Scholar
  99. Sato TR, Schall JD (2003) Effects of stimulus-response compatibility on neural selection in frontal eye field. Neuron 38:637–648PubMedCrossRefGoogle Scholar
  100. Schall JD (2004) On building a bridge between brain and behavior. Annu Rev Psychol 55:23–50PubMedCrossRefGoogle Scholar
  101. Schlag J, Schlag-Rey M (1987) Evidence for a supplementary eye field. J Neurophysiol 57:179–200PubMedGoogle 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 86:1916–1936PubMedGoogle 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 62:717–732PubMedCentralPubMedCrossRefGoogle 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 301:618–642PubMedCrossRefGoogle Scholar
  105. Smith PL, Ratcliff R (2004) Psychology and neurobiology of simple decisions. Trends Neurosci 27:161–168PubMedCrossRefGoogle Scholar
  106. So N-Y, Stuphorn V (2010) Supplementary eye field encodes option and action value for saccades with variable reward. J Neurophysiol 104:2634–2653PubMedCentralPubMedCrossRefGoogle 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 103:2124–2138PubMedCentralPubMedCrossRefGoogle Scholar
  108. Suzuki DA, Yamada T, Yee RD (2003) Smooth-pursuit eye-movementrelated neuronal activity in macaque nucleus reticularis tegmenti pontis. J Neurophysiol 89:2146–2158PubMedCrossRefGoogle Scholar
  109. Tanaka M, Fukushima K (1998) Neuronal responses related to smooth pursuit eye movements in the periarcuate cortical area of monkeys. J Neurophysiol 80:28–47PubMedGoogle 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 87:2684–2699PubMedCentralPubMedGoogle 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 62:626–641PubMedGoogle Scholar
  112. Teller DY (1984) Linking propositions. Vision Res 24:1233–1246PubMedCrossRefGoogle 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 74:2204–2210PubMedGoogle Scholar
  114. Usher M, McClelland JL (2001) The time course of perceptual choice: the leaky, competing accumulator model. Psychol Rev 108:550–592PubMedCrossRefGoogle Scholar
  115. Wallis JD, Miller EK (2003) From rule to response: neuronal processes in the premotor and prefrontal cortex. J Neurophysiol 90:1790–1806PubMedCrossRefGoogle Scholar
  116. Wallis JD, Anderson KC, Miller EK (2001) Single neurons in prefrontal cortex encode abstract rules. Nature 411:953–956PubMedCrossRefGoogle Scholar
  117. Wang XJ (2002) Probabilistic decision making by slow reverberation in cortical circuits. Neuron 36:955–968PubMedCrossRefGoogle Scholar
  118. White IM, Wise SP (1999) Rule-dependent neuronal activity in the prefrontal cortex. Exp Brain Res 126:315–335PubMedCrossRefGoogle 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 103:2458–2469PubMedCentralPubMedCrossRefGoogle Scholar
  120. Zhang J (2012) The effects of evidence bounds on decision-making: theoretical and empirical developments. Front Psychol 3Google Scholar

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© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.The Smith-Kettlewell Eye Research InstituteSan FranciscoUSA
  2. 2.Centre of Behavioural and Cognitive SciencesUniversity of AllahabadAllahabadIndia

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