Context-dependent urgency influences speed-accuracy trade-offs in decision-making and movement execution

Journal of Neuroscience

Volumn 34, Issue 49, 2014, Pages 16442-16454

  Thura, David ^a   Cos, Ignasi ^a,b   Trung, Jessica ^a   Cisek, Paul ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b UNIVERSITÉ PIERRE ET MARIE CURIE   (France)

Author keywords

Decision making; Monkey; Reaching; Reward rate; Saccades; Urgency

Indexed keywords

ACCURACY; ADAPTATION; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; CONTROLLED STUDY; DECISION MAKING; KINEMATICS; LATENT PERIOD; MALE; MATHEMATICAL COMPUTING; MOTOR SYSTEM; MOVEMENT (PHYSIOLOGY); NERVE CONDUCTION; NONHUMAN; REACTION TIME; RHESUS MONKEY; SACCADIC EYE MOVEMENT; SENSORY FEEDBACK; SIGNAL PROCESSING; SPATIAL MEMORY TEST; STIMULUS RESPONSE; ANIMAL; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE;

ANIMALS; DECISION MAKING; MACACA MULATTA; MALE; MOVEMENT; PSYCHOMOTOR PERFORMANCE; REACTION TIME; SACCADES;

EID: 84914680247     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0162-14.2014     Document Type: Article

References (63)

1. Bahill AT, Clark MR, Stark L (1975) The main sequence, a tool for studying human eye movements. Math Biosci 24:191-204.CrossRef
2. Balci F, Simen P, Niyogi R, Saxe A, Hughes JA, Holmes P, Cohen JD (2011) Acquisition of decision making criteria: reward rate ultimately beats accuracy. Atten Percept Psychophys 73:640-657. CrossRef Medline
3. Barto AG (1995) Adaptive critics and the basal ganglia. In: Models of information processing in the basal ganglia (Houk JC, Davis JL, Beiser DG, eds), pp 215-232. Cambridge, MA: MIT.
4. Bogacz R, Gurney K (2007) The basal ganglia and cortex implement optimal decision making between alternative actions. Neural Comput 19:442-477. CrossRef Medline
5. Bogacz R, Brown E, Moehlis J, Holmes P, Cohen JD (2006) The physics of optimal decision making: a formal analysis of models of performance in two-alternative forced-choice tasks. Psychol Rev 113:700-765. CrossRef Medline
6. Bogacz R, Wagenmakers EJ, Forstmann BU, Nieuwenhuis S (2010) The neural basis of the speed-accuracy tradeoff. Trends Neurosci 33:10-16. CrossRef Medline
7. Casini L, Vidal F (2011) The SMAs: neural substrate of the temporal accumulator? Front Integr Neurosci 5:35. Medline Chittka L, Skorupski P, Raine NE (2009) Speed-accuracy tradeoffs in animal decision making. Trends Ecol Evol 24:400-407. CrossRef Medline
8. Choi JE, Vaswani PA, Shadmehr R (2014) Vigor of movements and the cost of time in decision making. J Neurosci 34:1212-1223. CrossRef Medline
9. Churchland AK, Kiani R, Shadlen MN (2008) Decision-making with multiple alternatives. Nat Neurosci 11:693-702. CrossRef Medline
10. Churchland AK, Kiani R, Chaudhuri R, Wang XJ, Pouget A, Shadlen MN (2011) Variance as a signature of neural computations during decision making. Neuron 69:818-831. CrossRef Medline
11. Cisek P, Puskas GA, El-Murr S (2009) Decisions in changing conditions: the urgency-gating model. J Neurosci 29:11560-11571. CrossRef Medline
12. Daw ND, Doya K (2006) The computational neurobiology of learning and reward. Curr Opin Neurobiol 16:199-204. CrossRef Medline
13. Desmurget M, Turner RS (2010) Motor sequences and the basal ganglia: kinematics, not habits. J Neurosci 30:7685-7690. CrossRef Medline
14. Ditterich J (2006) Evidence for time-variant decision making. Eur J Neurosci 24:3628-3641. CrossRef Medline
15. Doya K (2000) Complementary roles of basal ganglia and cerebellum in learning and motor control. Curr Opin Neurobiol 10:732-739. CrossRef Medline
16. Drugowitsch J, Moreno-Bote R, Churchland AK, Shadlen MN, Pouget A (2012) The cost of accumulating evidence in perceptual decision making. J Neurosci 32:3612-3628. CrossRef Medline
17. Fitts PM (1954) The information capacity of the human motor system in controlling the amplitude of movement. J Exp Psychol 47:381-391. CrossRef Medline
18. Georgopoulos AP, Kalaska JF, Massey JT (1981) Spatial trajectories and reaction times of aimed movements: effects of practice, uncertainty, and change in target location. J Neurophysiol 46:725-743.Medline
19. Ghose GM (2006) Strategies optimize the detection of motion transients. J Vis 6(4):10 429-440. CrossRef Medline
20. Gold JI, Shadlen MN (2002) Banburismus and the brain: decoding the relationship between sensory stimuli, decisions, and reward. Neuron 36: 299-308. CrossRef Medline
21. Gold JI, Shadlen MN (2007) The neural basis of decision making. Annu Rev Neurosci 30:535-574. CrossRef Medline
22. Graybiel AM (1998) The basal ganglia and chunking of action repertoires. Neurobiol Learn Mem 70:119-136. CrossRef Medline
23. Graybiel AM, Aosaki T, Flaherty AW, Kimura M (1994) The basal ganglia and adaptive motor control. Science 265:1826-1831. CrossRef Medline
24. Haith AM, Reppert TR, Shadmehr R (2012) Evidence for hyperbolic temporal discounting of reward in control of movements. J Neurosci 32: 11727-11736. CrossRef Medline
25. 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. CrossRef Medline
26. Hanks T, Kiani R, Shadlen MN (2014) A neural mechanism of speedaccuracy tradeoff in macaque area LIP. Elife (Cambridge) 3:e02260. CrossRef Medline
27. Harris CM, Wolpert DM (2006) The main sequence of saccades optimizes speed-accuracy trade-off. Biol Cybern 95:21-29. CrossRef Medline
28. Hayden BY, Pearson JM, Platt ML (2011) Neuronal basis of sequential foraging decisions in a patchy environment. Nat Neurosci 14:933-939. CrossRef Medline
29. Heitz RP, Schall JD (2012) Neural mechanisms of speed-accuracy tradeoff. Neuron 76:616-628. CrossRef Medline
30. Horak FB, Anderson ME (1984) Influence of globus pallidus on arm movements in monkeys: II. Effects of stimulation. J Neurophysiol 52:305-322.Medline
31. Janssen P, Shadlen MN (2005) Arepresentation of the hazard rate of elapsed time in macaque area LIP. Nat Neurosci 8:234-241. CrossRef Medline
32. Lebedev MA, O’Doherty JE, Nicolelis MA (2008) Decoding of temporal intervals from cortical ensemble activity. J Neurophysiol 99:166-186.Medline
33. Leon MI, Shadlen MN (2003) Representation of time by neurons in the posterior parietal cortex of the macaque. Neuron 38:317-327. CrossRef Medline
34. Ludwig CJ, Gilchrist ID, McSorley E, Baddeley RJ (2005) The temporal impulse response underlying saccadic decisions. J Neurosci 25:9907-9912. CrossRef Medline
35. Maimon G, Assad JA (2006) A cognitive signal for the proactive timing of action in macaque LIP. Nat Neurosci 9:948-955. CrossRef Medline
36. Mazurek ME, Roitman JD, Ditterich J, Shadlen MN (2003) A role for neural integrators in perceptual decision making. Cereb Cortex 13:1257-1269. CrossRef Medline
37. Mazzoni P, Hristova A, Krakauer JW (2007) Why don’t we move faster? Parkinson’s disease, movement vigor, and implicit motivation. J Neurosci 27:7105-7116. CrossRef Medline
38. Miller P, Katz DB (2013) Accuracy and response-time distributions for decision-making: linear perfect integrators versus nonlinear attractor-based neural circuits. J Comput Neurosci 35:261-294. CrossRef Medline
39. Mita A, Mushiake H, Shima K, Matsuzaka Y, Tanji J (2009) Interval time coding by neurons in the presupplementary and supplementary motor areas. Nat Neurosci 12:502-507. CrossRef Medline
40. Myerson J, Green L (1995) Discounting of delayed rewards: models of individual choice. J Exp Anal Behav 64:263-276. CrossRef Medline
41. Nagano-Saito A, Cisek P, Perna AS, Shirdel FZ, Benkelfat C, Leyton M, Dagher A (2012) From anticipation to action, the role of dopamine in perceptual decision making: an fMRI-tyrosine depletion study. J Neurophysiol 108:501-512. CrossRef Medline
42. Niv Y, Daw ND, Joel D, Dayan P (2007) Tonic dopamine: opportunity costs and the control of response vigor. Psychopharmacology (Berl) 191:507-520. CrossRef Medline
43. Pachella RG (1974) The interpretation of reaction time in information processing research. In: Human information processing: tutorials in performance and cognition (Kantowitz BH, ed), pp 41-82. Hillsdale, NJ: Erlbaum.
44. Palmer J, Huk AC, Shadlen MN (2005) The effect of stimulus strength on the speed and accuracy of a perceptual decision. J Vis 5(5):1 376-404. CrossRef Medline
45. Ratcliff R (1978) A theory of memory retrieval. Psychol Rev 85:59-108. CrossRef
46. Ratcliff R, McKoon G (2008) The diffusion decision model: theory and data for two-choice decision tasks. Neural Comput 20:873-922. CrossRef Medline
47. Reddi BA, Carpenter RH (2000) The influence of urgency on decision time. Nat Neurosci 3:827-830. CrossRef Medline
48. Renoult L, Roux S, Riehle A (2006) Time is a rubberband: neuronal activity in monkey motor cortex in relation to time estimation. Eur J Neurosci 23:3098-3108. CrossRef Medline
49. Salinas E, Scerra VE, Hauser CK, Costello MG, Stanford TR (2014) Decoupling speed and accuracy in an urgent decision-making task reveals multiple contributions to their trade-off. Front Neurosci 8:85. CrossRef Medline
50. Shadmehr R (2010) Control of movements and temporal discounting of reward. Curr Opin Neurobiol 20:726-730. CrossRef Medline
51. Shadmehr R, Orban de Xivry JJ, Xu-Wilson M, Shih TY (2010) Temporal discounting of reward and the cost of time in motor control. J Neurosci 30:10507-10516. CrossRef Medline
52. Simen P, Cohen JD, Holmes P (2006) Rapid decision threshold modulation by reward rate in a neural network. Neural Netw 19:1013-1026. CrossRef Medline
53. Smith EA, Winterhalder B (1992) Evolutionary ecology and human behavior. New York: Aldine de Gruyter.
54. Stanford TR, Shankar S, Massoglia DP, Costello MG, Salinas E (2010) Perceptual decision making in less than 30 milliseconds. Nat Neurosci 13: 379-385. CrossRef Medline
55. Stephens DW, Krebs JR (1986) Foraging theory. Princeton, NJ: Princeton UP.
56. Takikawa Y, Kawagoe R, Itoh H, Nakahara H, Hikosaka O (2002) Modulation of saccadic eye movements by predicted reward outcome. Exp Brain Res 142:284-291. CrossRef Medline
57. Thura D, Cisek P (2010) Monkey frontal cortex reflects the time course of changing evidence for reach decisions. Soc Neurosci Abstr 805.91/JJJ35.
58. Thura D, Cisek P (2011) Neural activity during adjustment of the speedaccuracy trade-off in a reach decision task. Soc Neurosci Abstr 609.17/VV73.
59. Thura D, Cisek P (2012) Neural bases of speed/accuracy trade-offs adjustments during decision-making and movement execution in monkeys. Soc Neurosci Abstr 730.08.
60. Thura D, Cisek P (2014) Deliberation and commitment in the premotor and primary motor cortex during dynamic decision making. Neuron 81: 1401-1416. CrossRef Medline
61. Thura D, Beauregard-Racine J, Fradet CW, Cisek P (2012) Decision making by urgency gating: theory and experimental support. J Neurophysiol 108: 2912-2930. CrossRef Medline
62. Turner RS, Desmurget M (2010) Basal ganglia contributions to motor control: a vigorous tutor. Curr Opin Neurobiol 20:704-716. CrossRef Medline
63. Wickelgren WA (1977) Speed-accuracy trade-off and information processing dynamics. Acta Psychologica 41:67-85. CrossRef