From anticipation to action, the role of dopamine in perceptual decision making: An fMRI-tyrosine depletion study

Journal of Neurophysiology

Volumn 108, Issue 2, 2012, Pages 501-512

  Nagano Saito, Atsuko ^a,b   Cisek, Paul ^c   Perna, Andrea S ^b   Shirdel, Fatemeh Z ^a   Benkelfat, Chawki ^b   Leyton, Marco ^b   Dagher, Alain ^a  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Basal ganglia; Functional magnetic resonance imaging; Motion discrimination; Reward

Indexed keywords

AMINO ACID MIXTURE; DOPAMINE; TYROSINE;

ADULT; ANTICIPATION; ARTICLE; BASAL GANGLION; COMPUTER PROGRAM; CORPUS STRIATUM; DECISION MAKING; DOPAMINERGIC TRANSMISSION; FEMALE; FRONTAL LOBE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; INFORMATION PROCESSING; MALE; NORMAL HUMAN; PERCEPTION; PREFRONTAL CORTEX; PRIORITY JOURNAL; REACTION TIME; REWARD; SIGNAL TRANSDUCTION; TASK PERFORMANCE;

ADULT; ANTICIPATION, PSYCHOLOGICAL; BRAIN MAPPING; DECISION MAKING; DOPAMINE; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; REWARD; TYROSINE; VISUAL PERCEPTION; YOUNG ADULT;

EID: 84864008609     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00592.2011     Document Type: Article

References (92)

1. Abler B, Walter H, Erk S, Kammerer H, Spitzer M. Prediction error as a linear function of reward probability is coded in human nucleus accumbens. Neuroimage 31: 790-795, 2006.
2. Andersen RA, Cui H. Intention, action planning, and decision making in parietal-frontal circuits. Neuron 63: 568-583, 2009.
3. Antal A, Baudewig J, Paulus W, Dechent P. The posterior cingulate cortex and planum temporale/parietal operculum are activated by coherent visual motion. Vis Neurosci 25: 17-26, 2008.
4. Apicella P. Leading tonically active neurons of the striatum from reward detection to context recognition. Trends Neurosci 30: 299-306, 2007.
5. Baleydier C, Mauguiere F. The duality of the cingulate gyrus in monkey. Neuroanatomical study and functional hypothesis. Brain 103: 525-554, 1980.
6. Bardgett ME, Depenbrock M, Downs N, Points M, Green L. Dopamine modulates effort-based decision making in rats. Behav Neurosci 123: 242-251, 2009.
7. Bisley JW, Goldberg ME. Neuronal activity in the lateral intraparietal area and spatial attention. Science 299: 81-86, 2003.
8. Bogacz R, Gurney K. The basal ganglia and cortex implement optimal decision making between alternative actions. Neural Comput 19: 442-477, 2007.
9. Buchel C, Josephs O, Rees G, Turner R, Frith CD, Friston KJ. The functional anatomy of attention to visual motion. A functional MRI study. Brain 121: 1281-1294, 1998.
10. Carpenter RH, Williams ML. Neural computation of log likelihood in control of saccadic eye movements. Nature 377: 59-62, 1995.
11. Chance FS, Abbott LF, Reyes AD. Gain modulation from background synaptic input. Neuron 35: 773-782, 2002.
12. Cisek P. Cortical mechanisms of action selection: the affordance competition hypothesis. Philos Trans R Soc Lond B Biol Sci 362: 1585-1599, 2007.
13. Cisek P, Puskas G, El-Murr S. Decisions in changing conditions: the urgency-gating model. J Neurosci 29: 11560-11571, 2009.
14. Coe B, Tomihara K, Matsuzawa M, Hikosaka O. Visual and anticipatory bias in three cortical eye fields of the monkey during an adaptive decisionmaking task. J Neurosci 22: 5081-5090, 2002.
15. Collins DL, Neelin P, Peters TM, Evans AC. Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J Comput Assist Tomogr 18: 192-205, 1994.
16. Delgado MR, Nystrom LE, Fissell C, Noll DC, Fiez JA. Tracking the hemodynamic responses to reward and punishment in the striatum. J Neurophysiol 84: 3072-3077, 2000.
17. Ding L, Gold JI. Caudate encodes multiple computations for perceptual decisions. J Neurosci 30: 15747-15759, 2010.
18. Domenech P, Dreher JC. Decision threshold modulation in the human brain. J Neurosci 30: 14305-14317, 2010.
19. Dreher JC, Kohn P, Berman KF. Neural coding of distinct statistical properties of reward information in humans. Cereb Cortex 16: 561-573, 2006.
20. Ezzati A, Khadjevand F, Zandvakili A, Abbassian A. Higher-level motion detection deficit in Parkinson's disease. Brain Res 1320: 143-151, 2010.
21. Trick GL, Kaskie B, Steinman SB. Visual impairment in Parkinson's disease: deficits in orientation and motion discrimination. Optom Vis Sci 71: 242-245, 1994.
22. Forman S, Cohen J, Fitzgerald M, Eddy W, Mintun M, Noll D. Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn Reson Med 33: 636-647, 1995.
23. Forstmann B, Dutilh G, Brown S, Neumann J, von Cramon DY, Ridderinkhof KR, Wagenmakers EJ. Striatum and pre-SMA facilitate decision-making under time pressure. Proc Natl Acad Sci USA 105: 17538-17542, 2008.
24. Forstmann BU, Brown S, Dutilh G, Neumann J, Wagenmakers EJ. The neural substrate of prior information in perceptual decision making: a model-based analysis. Front Hum Neurosci 4: 40, 2010.
25. Frank MJ. Hold your horses: a dynamic computational role for the subthalamic nucleus in decision making. Neural Netw 19: 1120-1136, 2006.
26. Frank MJ, Seeberger LC, O'Reilly RC. By carrot or by stick: cognitive reinforcement learning in parkinsonism. Science 306: 1940-1943, 2004.
27. Genovese CR, Lazar NA, Nichols T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15: 870-878, 2002.
28. Glover GH. Deconvolution of impulse response in event-related BOLD fMRI. Neuroimage 9: 416-429, 1999.
29. Goto Y, Grace AA. Dopaminergic modulation of limbic and cortical drive of nucleus accumbens in goal-directed behavior. Nat Neurosci 8: 805-812, 2005.
30. Haber SN, Fudge JL, McFarland NR. Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. J Neurosci 20: 2369-2382, 2000.
31. Hesselmann G, Kell C, Kleinschmidt A. Ongoing activity fluctuations in hMT+ bias the perception of coherent visual motion. J Neurosci 28: 14481-14485, 2008.
32. Ipata AE, Gee AL, Gottlieb J, Bisley JW, Goldberg ME. LIP responses to a popout stimulus are reduced if it is overtly ignored. Nat Neurosci 9: 1071-1076, 2006.
33. Kawagoe R, Takikawa Y, Hikosaka O. Expectation of reward modulates cognitive signals in the basal ganglia. Nat Neurosci 1: 411-416, 1998.
34. Knutson B, Adams CM, Fong GW, Hommer D, Taylor J, Kaufman M, Peterson R, Glover G. Anticipation of increasing monetary reward selectively recruits nucleus accumbens distributed neural representation of expected value. J Neurosci 21: RC159, 2001.
35. Kobayashi Y, Amaral DG. Macaque monkey retrosplenial cortex: II. Cortical afferents. J Comp Neurol 466: 48-79, 2003.
36. Kobayashi Y, Amaral DG. Macaque monkey retrosplenial cortex: III. Cortical efferents. J Comp Neurol 502: 810-833, 2007.
37. Kouneiher F, Charron S, Koechlin E. Motivation and cognitive control in the human prefrontal cortex. Nat Neurosci 12: 939-945, 2009.
38. Krawczyk DC, Gazzaley A, D'Esposito M. Reward modulation of prefrontal and visual association cortex during an incentive working memory task. Brain Res 1141: 168-177, 2007.
39. Lau B, Glimcher PW. Value representations in the primate striatum during matching behavior. Neuron 58: 451-463, 2008.
40. Lauwereyns J, Watanabe K, Coe B, Hikosaka O. A neural correlate of response bias in monkey caudate nucleus. Nature 418: 413-417, 2002.
41. Leyton M, aan het Rot M, Booij L, Baker GB, Young SN, Benkelfat C. Mood-elevating effects of d-amphetamine and incentive salience: the effect of acute dopamine precursor depletion. J Psychiatry Neurosci 32:.129-136, 2007.
42. 11C]raclopride study in healthy men. Neuropsychopharmacology 29: 427-432, 2004.
43. Leyton M, Young SN, Pihl RO, Etezadi S, Lauze C, Blier P, Baker GB, Benkelfat C. Effects on mood of acute phenylalanine/tyrosine depletion in healthy women. Neuropsychopharmacology 22: 52-63, 2000.
44. Llinas RR. I of the Vortex: From Neurons to Self. Cambridge, MA: MIT Press, 2002.
45. Lo CC, Wang XJ. Cortico-basal ganglia circuit mechanism for a decision threshold in reaction time tasks. Nat Neurosci 9: 956-963, 2006.
46. Logothetis NK, Wandell BA. Interpreting the BOLD signal. Annu Rev Physiol 66: 735-769, 2004.
47. Lorr M, McNair DM, Fisher SU. Evidence for bipolar mood states. J Pers Assess 46: 432-436, 1982.
48. McClure SM, Berns GS, Montague PR. Temporal prediction errors in a passive learning task activate human striatum. Neuron 38: 339-346, 2003.
49. McTavish SF, Callado L, Cowen PJ, Sharp T. Comparison of the effects of α-methyl-p-tyrosine and a tyrosine-free amino acid load on extracellular noradrenaline in the rat hippocampus in vivo. J Psychopharmacol 13: 379-384, 1999a.
50. McTavish SF, Cowen PJ, Sharp T. Effect of a tyrosine-free amino acid mixture on regional brain catecholamine synthesis and release. Psychopharmacology (Berl) 141: 182-188, 1999b.
51. Mogenson GJ, Jones DL, Yim CY. From motivation to action: functional interface between the limbic system and the motor system. Prog Neurobiol 14: 69-97, 1980.
52. Moja EA, Lucini V, Benedetti F, Lucca A. Decrease in plasma phenylalanine and tyrosine after phenylalanine-tyrosine free amino acid solutions in man. Life Sci 58: 2389-2395, 1996.
53. Monosov IE, Trageser JC, Thompson KG. Measurements of simultaneously recorded spiking activity and local field potentials suggest that spatial selection emerges in the frontal eye field. Neuron 57: 614-625, 2008.
54. 11C]raclopride PET study. Am J Psychiatry 160: 1887-1889, 2003.
55. Morris G, Nevet A, Arkadir D, Vaadia E, Bergman H. Midbrain dopamine neurons encode decisions for future action. Nat Neurosci 9: 1057-1063, 2006.
56. Mufson EJ, Pandya DN. Some observations on the course and composition of the cingulum bundle in the rhesus monkey. J Comp Neurol 225: 31-43, 1984.
57. Nagano-Saito A, Leyton M, Monchi O, Goldberg YK, He Y, Dagher A. Dopamine depletion impairs frontostriatal functional connectivity during a set-shifting task. J Neurosci 28: 3697-3706, 2008.
58. Nicola SM, Taha SA, Kim SW, Fields HL. Nucleus accumbens dopamine release is necessary and sufficient to promote the behavioral response to reward-predictive cues. Neuroscience 135: 1025-1033, 2005.
59. Niv Y, Daw ND, Joel D, Dayan P. Tonic dopamine: opportunity costs and the control of response vigor. Psychopharmacology (Berl) 191: 507-520, 2007.
60. Noorani I, Gao MJ, Pearson BC, Carpenter RH. Predicting the timing of wrong decisions with LATER. Exp Brain Res 209: 587-598, 2011.
61. Pesaran B, Nelson MJ, Andersen RA. Free choice activates a decision circuit between frontal and parietal cortex. Nature 453: 406-409, 2008.
62. Pessiglione M, Seymour B, Flandin G, Dolan RJ, Frith CD. Dopaminedependent prediction errors underpin reward-seeking behaviour in humans. Nature 442: 1042-1045, 2006.
63. Phillips PE, Stuber GD, Heien ML, Wightman RM, Carelli RM. Subsecond dopamine release promotes cocaine seeking. Nature 422: 614-618, 2003.
64. Platt ML, Glimcher PW. Neural correlates of decision variables in parietal cortex. Nature 400: 233-238, 1999.
65. Pleger B, Ruff CC, Blankenburg F, Kloppel S, Driver J, Dolan RJ. Influence of dopaminergically mediated reward on somatosensory decisionmaking. PLoS Biol 7: e1000164, 2009.
66. Ratcliff R. A theory of memory retrieval. Psychol Rev 85: 59-108, 1978.
67. Reddi BA, Asrress KN, Carpenter RH. Accuracy, information, and response time in a saccadic decision task. J Neurophysiol 90: 3538-3546, 2003.
68. Roitman JD, Shadlen MN. Response of neurons in the lateral intraparietal area during a combined visual discrimination reaction time task. J Neurosci 22: 9475-9489, 2002.
69. Rowe JB, Eckstein D, Braver T, Owen AM. How does reward expectation influence cognition in the human brain? J Cogn Neurosci 20: 1980-1992, 2008.
70. Saint-Cyr JA, Ungerleider LG, Desimone R. Organization of visual cortical inputs to the striatum and subsequent outputs to the pallido-nigral complex in the monkey. J Comp Neurol 298: 129-156, 1990.
71. Salamone JD, Correa M, Farrar A, Mingote SM. Effort-related functions of nucleus accumbens dopamine and associated forebrain circuits. Psychopharmacology (Berl) 191: 461-482, 2007.
72. Samejima K, Ueda Y, Doya K, Kimura M. Representation of action-specific reward values in the striatum. Science 310: 1337-1340, 2005.
73. Satoh T, Nakai S, Sato T, Kimura M. Correlated coding of motivation and outcome of decision by dopamine neurons. J Neurosci 23: 9913-9923, 2003.
74. Schultz W. Predictive reward signal of dopamine neurons. J Neurophysiol 80: 1-27, 1998.
75. Seamans JK, Yang CR. The principal features and mechanisms of dopamine modulation in the prefrontal cortex. Prog Neurobiol 74: 1-58, 2004.
76. Shadlen MN, Britten KH, Newsome WT, Movshon JA. A computational analysis of the relationship between neuronal and behavioral responses to visual motion. J Neurosci 16: 1486-1510, 1996.
77. Shadlen MN, Newsome WT. Motion perception: seeing and deciding. Proc Natl Acad Sci USA 93: 628-633, 1996.
78. Shadlen MN, Newsome WT. Neural basis of a perceptual decision in the parietal cortex (area LIP) of the rhesus monkey. J Neurophysiol 86: 1916-1936, 2001.
79. Shimo Y, Hikosaka O. Role of tonically active neurons in primate caudate in reward-oriented saccadic eye movement. J Neurosci 21: 7804-7814, 2001.
80. Summerfield C, Koechlin E. Economic value biases uncertain perceptual choices in the parietal and prefrontal cortices. Front Hum Neurosci 4: 208, 2010.
81. Takikawa Y, Kawagoe R, Hikosaka O. Reward-dependent spatial selectivity of anticipatory activity in monkey caudate neurons. J Neurophysiol 87: 508-515, 2002.
82. Tobler PN, Fiorillo CD, Schultz W. Adaptive coding of reward value by dopamine neurons. Science 307: 1642-1645, 2005.
83. Trick GL, Kaskie B, Steinman SB. Visual impairment in Parkinson's disease: deficits in orientation and motion discrimination. Optom Vis Sci 71: 242-245, 1994.
84. Usher M, McClelland JL. The time course of perceptual choice: the leaky, competing accumulator model. Psychol Rev 108: 550-592, 2001.
85. Vogt BA, Pandya DN. Cingulate cortex of the rhesus monkey: II. Cortical afferents. J Comp Neurol 262: 271-289, 1987.
86. Watanabe M, Cromwell HC, Tremblay L, Hollerman JR, Hikosaka K, Schultz W. Behavioral reactions reflecting differential reward expectations in monkeys. Exp Brain Res 140: 511-518, 2001.
87. Watson JD, Myers R, Frackowiak RS, Hajnal JV, Woods RP, Mazziotta JC, Shipp S, Zeki S. Area V5 of the human brain: evidence from a combined study using positron emission tomography and magnetic resonance imaging. Cereb Cortex 3: 79-94, 1993.
88. Wittmann BC, Schott BH, Guderian S, Frey JU, Heinze HJ, Duzel E. Reward-related FMRI activation of dopaminergic midbrain is associated with enhanced hippocampus-dependent long-term memory formation. Neuron 45: 459-467, 2005.
89. Worsley KJ. Spatial smoothing of autocorrelations to control the degrees of freedom in fMRI analysis. Neuroimage 26: 635-641, 2005.
90. Worsley KJ, Liao CH, Aston J, Petre V, Duncan GH, Morales F, Evans AC. A general statistical analysis for fMRI data. Neuroimage 15: 1-15, 2002.
91. Yang T, Shadlen MN. Probabilistic reasoning by neurons. Nature 447: 1075-1080, 2007.
92. Zijdenbos AP, Forghani R, Evans AC. Automatic "pipeline" analysis of 3-D MRI data for clinical trials: application to multiple sclerosis. IEEE Trans Med Imaging 21: 1280-1291, 2002.