Cortico-subthalamic connection predicts individual differences in value-driven choice bias

Brain Structure and Function

Volumn 219, Issue 4, 2014, Pages 1239-1249

  Mulder, Martijn J ^a   Boekel, Wouter ^a   Ratcliff, Roger ^b   Forstmann, Birte U ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Choice bias; Perceptual decision making; Probabilistic tractography; STN; vmPFC

Indexed keywords

ADULT; ARTICLE; CHOICE BIAS; COGNITIVE BIAS; CONNECTOME; CONTROLLED STUDY; DECISION MAKING; DIFFUSION WEIGHTED IMAGING; DRIFT DIFFUSION MODEL; FEMALE; FORCED CHOICE METHOD; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HEAD ARRAY COIL; HUMAN; HUMAN EXPERIMENT; MALE; NEUROLOGICAL DIAGNOSTIC DEVICE; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE SCANNER; PERCEPTUAL DECISION MAKING; PREDICTION; PRIORITY JOURNAL; PSYCHOLOGICAL MODEL; SUBTHALAMIC NUCLEUS; TRACTOGRAPHY; VENTROMEDIAL PREFRONTAL CORTEX; YOUNG ADULT; BRAIN CORTEX; BRAIN MAPPING; DIFFUSION TENSOR IMAGING; INDIVIDUALITY; NERVE TRACT; PHYSIOLOGY; PROCEDURES; REACTION TIME;

ADULT; BRAIN MAPPING; CEREBRAL CORTEX; CHOICE BEHAVIOR; DIFFUSION TENSOR IMAGING; FEMALE; HUMANS; INDIVIDUALITY; MALE; NEURAL PATHWAYS; REACTION TIME; SUBTHALAMIC NUCLEUS; YOUNG ADULT;

EID: 84904334366     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-013-0561-3     Document Type: Article

References (84)

1. Aron AR, Poldrack RA (2006) Cortical and subcortical contributions to stop signal response inhibition: role of the subthalamic nucleus. J Neurosci 26(9):2424-2433. doi:10.1523/JNEUROSCI.4682-05.2006 (Pubitemid 44699002)
2. Aron AR, Behrens TE, Smith S, Frank MJ, Poldrack RA (2007) Triangulating a cognitive control network using diffusion-weighted magnetic resonance imaging (MRI) and functional MRI. J Neurosci 27(14):3743-3752. doi:10.1523/JNEUROSCI. 0519-07.2007 (Pubitemid 46557676)
3. Baunez C, Lardeux S (2011) Frontal cortex-like functions of the subthalamic nucleus. Front Syst Neurosci 5:83. doi:10.3389/fnsys.2011.00083
4. Baunez C, Amalric M, Robbins TW (2002) Enhanced food-related motivation after bilateral lesions of the subthalamic nucleus. J Neurosci 22(2):562-568. doi:22/2/562
5. Baunez C, Dias C, Cador M, Amalric M (2005) The subthalamic nucleus exerts opposite control on cocaine and 'natural' rewards. Nat Neurosci 8(4):484-489. doi:10.1038/nn1429 (Pubitemid 41007566)
6. Beckmann M, Johansen-Berg H, Rushworth MF (2009) Connectivity-based parcellation of human cingulate cortex and its relation to functional specialization. J Neurosci 29(4):1175-1190. doi:10.1523/JNEUROSCI.3328-08.2009
7. Behrens TE, Johansen-Berg H, Woolrich MW, Smith SM, Wheeler-Kingshott CA, Boulby PA, Barker GJ, Sillery EL, Sheehan K, Ciccarelli O, Thompson AJ, Brady JM, Matthews PM (2003a) Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci 6(7):750-757. doi:10.1038/nn1075 (Pubitemid 36792891)
8. Behrens TE, Woolrich MW, Jenkinson M, Johansen-Berg H, Nunes RG, Clare S, Matthews PM, Brady JM, Smith SM (2003b) Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn Reson Med: Off J Soc Mag Reson Med/Soc Magn Reson Med 50(5):1077-1088. doi:10.1002/mrm.10609 (Pubitemid 37356588)
9. Behrens TE, Berg HJ, Jbabdi S, Rushworth MF, Woolrich MW (2007) Probabilistic diffusion tractography with multiple fibre orientations: what can we gain? Neuroimage 34(1):144-155. doi:10.1016/j.neuroimage.2006.09.018 (Pubitemid 44765263)
10. Blair K, Marsh AA, Morton J, Vythilingam M, Jones M, Mondillo K, Pine DC, Drevets WC, Blair JR (2006) Choosing the lesser of two evils, the better of two goods: specifying the roles of ventromedial prefrontal cortex and dorsal anterior cingulate in object choice. J Neurosci 26(44):11379-11386. doi:10.1523/JNEUROSCI.1640-06.2006 (Pubitemid 44772167)
11. Bogacz R (2007) Optimal decision-making theories: linking neurobiology with behaviour. Trends Cogn Sci 11(3):118-125. doi:10.1016/j.tics.2006.12.006
12. Bogacz R, Gurney K (2007) The basal ganglia and cortex implement optimal decision making between alternative actions. Neural Comput 19(2):442-477. doi:10.1162/neco.2007.19.2.442
13. 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(4):700-765. doi:10.1037/0033-295X.113.4.700 (Pubitemid 44629916)
14. Bogacz R, Hu PT, Holmes P, Cohen JD (2010a) Do humans produce the speed-accuracy trade-off that maximizes reward rate? Q J Exp Psychol 63:863-891. doi:10.1080/17470210903091643
15. Bogacz R, Wagenmakers E-J, Forstmann B, Nieuwenhuis S (2010b) The neural basis of the speed-accuracy tradeoff. Trends Neurosci 33(1):10-16
16. Cavanagh JF, Wiecki TV, Cohen MX, Figueroa CM, Samanta J, Sherman SJ, Frank MJ (2011) Subthalamic nucleus stimulation reverses mediofrontal influence over decision threshold. Nat Neurosci 14(11):1462-1467. doi:10.1038/nn.2925
17. Darbaky Y, Baunez C, Arecchi P, Legallet E, Apicella P (2005) Reward-related neuronal activity in the subthalamic nucleus of the monkey. NeuroReport 16(11):1241-1244. doi:00001756-200508010-00022
18. Deichmann R, Good CD, Josephs O, Ashburner J, Turner R (2000) Optimization of 3-D MP-RAGE sequences for structural brain imaging. Neuroimage 12(1):112-127. doi:10.1006/nimg.2000.0601 (Pubitemid 30602069)
19. Diederich A, Busemeyer JR (2006) Modeling the effects of payoff on response bias in a perceptual discrimination task: bound-change, drift-rate-change, or two-stage-processing hypothesis. Percept Psychophys 68(2):194-207 (Pubitemid 44874398)
20. Edwards W (1965) Optimal strategies for seeking information: models for statistics, choice reaction times, and human information processing. J Math Psychol 2(2):312-329
21. 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(2):e1000284. doi:10.1371/journal.pcbi.1000284
22. Ferry AT, Ongur D, An X, Price JL (2000) Prefrontal cortical projections to the striatum in macaque monkeys: evidence for an organization related to prefrontal networks. J Comp Neurol 425(3):447-470. doi:10.1002/1096- 9861(20000925)425:3<447:AID-CNE9>3.0.CO;2-V (Pubitemid 30659209)
23. Fleming SM, Thomas CL, Dolan RJ (2010a) Overcoming status quo bias in the human brain. Proc Natl Acad Sci USA 107(13): 6005-6009. doi:10.1073/pnas. 0910380107
24. Fleming SM, Whiteley L, Hulme OJ, Sahani M, Dolan RJ (2010b) Effects of category-specific costs on neural systems for perceptual decision-making. J Neurophysiol 103(6):3238-3247. doi:10.1152/jn.01084.2009
25. Forstmann BU, Dutilh G, Brown S, Neumann J, von Cramon DY, Ridderinkhof KR, Wagenmakers E-J (2008) Striatum and pre-SMA facilitate decision-making under time pressure. Proc Natl Acad Sci USA 105(45):17538-17542. doi:10.1073/pnas. 0805903105
26. Forstmann BU, Anwander A, Schäfer A, Neumann J, Brown S, Wagenmakers E-J, Bogacz R, Turner R (2010a) Cortico-striatal connections predict control over speed and accuracy in perceptual decision making. Proc Natl Acad Sci USA 107(36): 15916-15920. doi:10.1073/pnas.1004932107
27. Forstmann BU, Brown S, Dutilh G, Neumann J, Wagenmakers E-J (2010b) The neural substrate of prior information in perceptual decision making: a model-based analysis. Front Hum Neurosci 4(40):1-11. doi:10.3389/fnhum.2010. 00040
28. Forstmann BU, Keuken MC, Jahfari S, Bazin PL, Neumann J, Schafer A, Anwander A, Turner R (2012) Cortico-subthalamic white matter tract strength predicts interindividual efficacy in stopping a motor response. Neuroimage 60(1):370-375. doi:10.1016/j.neuroimage.2011.12.044
29. Frank MJ (2006) Hold your horses: a dynamic computational role for the subthalamic nucleus in decision making. Neural Netw 19(8):1120-1136. doi:10.1016/j.neunet.2006.03.006
30. Frank MJ (2009) The basal ganglia in reward and decision making: computational models and empirical studies. In: Handbook of Reward and Decision Making. Academic Press, Oxford, pp 399-425
31. Gjedde A, Geday J (2009) Deep brain stimulation reveals emotional impact processing in ventromedial prefrontal cortex. PLoS ONE 4(12):e8120. doi:10.1371/journal.pone.0008120
32. Gläscher J, Hampton AN, O'Doherty JP (2009) Determining a role for ventromedial prefrontal cortex in encoding action-based value signals during reward-related decision making. Cereb Cortex 19(2):483-495. doi:10.1093/cercor/ bhn098
33. Gold JI, Shadlen MN (2007) The neural basis of decision making. Annu Rev Neurosci 30:535-574. doi:10.1146/annurev.neuro.29.051605.113038 (Pubitemid 47218767)
34. Gurney K, Prescott TJ, Redgrave P (2001) A computational model of action selection in the basal ganglia. I. A new functional anatomy. Biol Cybern 84(6):401-410 (Pubitemid 33605190)
35. Haber SN, Kim KS, Mailly P, Calzavara R (2006) Reward-related cortical inputs define a large striatal region in primates that interface with associative cortical connections, providing a substrate for incentive-based learning. J Neurosci 26(32):8368-8376. doi:10.1523/JNEUROSCI.0271-06.2006 (Pubitemid 44309851)
36. Hampton AN, Adolphs R, Tyszka MJ, O'Doherty JP (2007) Contributions of the amygdala to reward expectancy and choice signals in human prefrontal cortex. Neuron 55(4):545-555. doi:10.1016/j.neuron.2007.07.022 (Pubitemid 47225198)
37. Haynes WIA, Haber SN (2013) The organization of prefrontal-subthalamic inputs in primates provides an anatomical substrate for both functional specificity and integration: implications for basal ganglia models and deep brain stimulation. J Neurosci 33(11):4804-4814. doi:10.1523/jneurosci.4674-12. 2013
38. Heida T, Marani E, Usunoff KG (2008) The subthalamic nucleus part II: modelling and simulation of activity. Adv Anat Embryol Cell Biol 199:1-85, vii
39. Humphries MD, Stewart RD, Gurney KN (2006) A physiologically plausible model of action selection and oscillatory activity in the basal ganglia. J Neurosci 26(50):12921-12942. doi:10.1523/JNEUROSCI.3486-06.2006 (Pubitemid 44954612)
40. Jbabdi S, Lehman JF, Haber SN, Behrens TE (2013) Human and monkey ventral prefrontal fibers use the same organizational principles to reach their targets: tracing versus tractography. J Neurosci 33(7):3190-3201. doi:10.1523/JNEUROSCI.2457-12.2013
41. Jenkinson M, Smith S (2001) A global optimisation method for robust affine registration of brain images. Med Image Anal 5(2): 143-156 (Pubitemid 35282800)
42. Johansen-Berg H, Behrens TE (2009) Diffusion MRI: from quantitative measurement to in vivo neuroanatomy. Elsevier, London
43. Kable J, Glimcher PW (2007) The neural correlates of subjective value during intertemporal choice. Nat Neurosci 10(12):1625-1633. doi:10.1038/nn2007 (Pubitemid 350175876)
44. Kalbe E, Voges J, Weber T, Haarer M, Baudrexel S, Klein JC, Kessler J, Sturm V, Heiss WD, Hilker R (2009) Frontal FDG-PET activity correlates with cognitive outcome after STN-DBS in Parkinson disease. Neurology 72(1):42-49. doi:10.1212/01.wnl.0000338536.31388.f0
45. Kantak KM, Yager LM, Brisotti MF (2012) Impact of medial orbital cortex and medial subthalamic nucleus inactivation, individually and together, on the maintenance of cocaine self-administration behavior in rats. Behav Brain Res 238C:1-9. doi:10.1016/j.bbr.2012.10.021
46. Knutson B, Bjork JM, Fong GW, Hommer D, Mattay VS, Weinberger DR (2004) Amphetamine modulates human incentive processing. Neuron 43(2):261-269. doi:10.1016/j.neuron.2004.06.030 (Pubitemid 38942965)
47. Knutson B, Taylor J, Kaufman M, Peterson R, Glover G (2005) Distributed neural representation of expected value. J Neurosci 25(19):4806-4812. doi:10.1523/JNEUROSCI.0642-05.2005 (Pubitemid 40664129)
48. Knutson B, Rick S, Wimmer GE, Prelec D, Loewenstein G (2007) Neural predictors of purchases. Neuron 53(1):147-156. doi:10.1016/j.neuron.2006.11.010 (Pubitemid 44969483)
49. Lambert C, Zrinzo L, Nagy Z, Lutti A, Hariz M, Foltynie T, Draganski B, Ashburner J, Frackowiak R (2012) Confirmation of functional zones within the human subthalamic nucleus: patterns of connectivity and sub-parcellation using diffusion weighted imaging. Neuroimage 60(1):83-94. doi:10.1016/j.neuroimage. 2011.11.082
50. Laming D (1968) Information theory of choice reaction times. Academic Press, New York
51. Lardeux S, Baunez C (2008) Alcohol preference influences the subthalamic nucleus control on motivation for alcohol in rats. Neuropsychopharmacology 33(3):634-642. doi:10.1038/sj.npp.1301432
52. Lardeux S, Pernaud R, Paleressompoulle D, Baunez C (2009) Beyond the reward pathway: coding reward magnitude and error in the rat subthalamic nucleus. J Neurophysiol 102(4):2526-2537. doi:10.1152/jn.91009.2008
53. Lehman JF, Greenberg BD, McIntyre CC, Rasmussen SA, Haber SN (2011) Rules ventral prefrontal cortical axons use to reach their targets: implications for diffusion tensor imaging tractography and deep brain stimulation for psychiatric illness. J Neurosci: Off J Soc Neurosci 31(28):10392-10402. doi:10.1523/JNEUROSCI.0595-11.2011
54. Leite FP, Ratcliff R (2011) What cognitive processes drive response biases? A diffusion model analysis. Judgm Decis Mak 6(7): 651-687
55. Link S, Heath R (1975) A sequential theory of psychological discrimination. Psychometrika 40(1):77-105. doi:10.1007/bf02291481
56. Liu X, Powell DK, Wang H, Gold BT, Corbly CR, Joseph JE (2007) Functional dissociation in frontal and striatal areas for processing of positive and negative reward information. J Neurosci 27(17):4587-4597. doi:10.1523/JNEUROSCI. 5227-06.2007 (Pubitemid 46663580)
57. Marani E, Heida T, Lakke EA, Usunoff KG (2008) The subthalamic nucleus. Part I: development, cytology, topography and connections. Adv Anat Embryol Cell Biol 198:1-113, vii
58. Matsumura M, Kojima J, Gardiner TW, Hikosaka O (1992) Visual and oculomotor functions of monkey subthalamic nucleus. J Neurophysiol 67(6):1615-1632
59. Maurice N, Deniau JM, Glowinski J, Thierry AM (1998) Relationships between the prefrontal cortex and the basal ganglia in the rat: physiology of the corticosubthalamic circuits. J Neurosci 18(22):9539-9546 (Pubitemid 28512482)
60. Maurice N, Deniau JM, Glowinski J, Thierry AM (1999) Relationships between the prefrontal cortex and the basal ganglia in the rat: physiology of the cortico-nigral circuits. J Neurosci 19(11):4674-4681 (Pubitemid 29241115)
61. Mori Zhang (2006) Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 51(5):527-539
62. Mori S, van Zijl PC (2002) Fiber tracking: principles and strategies - a technical review. NMR Biomed 15(7-8):468-480. doi:10.1002/nbm.781 (Pubitemid 36054510)
63. Mulder MJ, Wagenmakers E-J, Ratcliff R, Boekel W, Forstmann BU (2012) Bias in the brain: a diffusion model analysis of prior probability and potential payoff. J Neurosci 32(7):2335-2343. doi:10.1523/JNEUROSCI.4156-11.2012
64. Nambu A, Tokuno H, Takada M (2002) Functional significance of the cortico-subthalamo-pallidal 'hyperdirect' pathway. Neurosci Res 43(2):111-117. doi:S0168010202000275
65. Philiastides MG, Biele G, Heekeren HR (2010) A mechanistic account of value computation in the human brain. Proc Natl Acad Sci USA 107(20):9430-9435. doi:10.1073/pnas.1001732107
66. Preuschhof C, Schubert T, Villringer A, Heekeren HR (2010) Prior information biases stimulus representations during vibrotactile decision making. J Cogn Neurosci 22(5):875-887. doi:10.1162/jocn.2009.21260
67. Ramnani N, Elliott R, Athwal BS, Passingham RE (2004) Prediction error for free monetary reward in the human prefrontal cortex. Neuroimage 23(3):777-786. doi:10.1016/j.neuroimage.2004.07.028 (Pubitemid 39446513)
68. Ratcliff R (1978) A theory of memory retrieval. Psychol Rev 85(2): 59-108
69. Ratcliff R (1985) Theoretical interpretations of the speed and accuracy of positive and negative responses. Psychol Rev 92(2):212-225
70. Ratcliff R, McKoon G (2008) The diffusion decision model: theory and data for two-choice decision tasks. Neural Comput 20(4): 873-922. doi:10.1162/neco.2008.12-06-420
71. Ratcliff R, Tuerlinckx F (2002) Estimating parameters of the diffusion model: approaches to dealing with contaminant reaction times and parameter variability. Psychon Bull Rev 9(3):438-481
72. Ratcliff R, Van Zandt T, McKoon G (1999) Connectionist and diffusion models of reaction time. Psychol Rev 106(2):261-300
73. Simen P, Cohen JD, Holmes P (2006) Rapid decision threshold modulation by reward rate in a neural network. Neural Netw 19(8):1013-1026. doi:10.1016/j.neunet.2006.05.038 (Pubitemid 44466344)
74. Simen P, Contreras D, Buck C, Hu P, Holmes P, Cohen JD (2009) Reward rate optimization in two-alternative decision making: empirical tests of theoretical predictions. J Exp Psychol Hum Percept Perform 35(6):1885-1897
75. Smith DV, Hayden BY, Truong TK, Song AW, Platt ML, Huettel SA (2010) Distinct value signals in anterior and posterior ventromedial prefrontal cortex. J Neurosci 30(7):2490-2495. doi:10.1523/JNEUROSCI.3319-09.2010
76. Teagarden MA, Rebec GV (2007) Subthalamic and striatal neurons concurrently process motor, limbic, and associative information in rats performing an operant task. J Neurophysiol 97(3): 2042-2058. doi:10.1152/jn.00368.2006 (Pubitemid 46411141)
77. Temel Y, Blokland A, Steinbusch HW, Visser-Vandewalle V (2005) The functional role of the subthalamic nucleus in cognitive and limbic circuits. Prog Neurobiol 76(6):393-413. doi:10.1016/j.pneurobio.2005.09.005 (Pubitemid 41636778)
78. van Maanen L, Brown SD, Eichele T, Wagenmakers E-J, Ho T, Serences J, Forstmann BU (2011) Neural correlates of trial-to-trial fluctuations in response caution. J Neurosci 31(48): 17488-17495. doi:10.1523/JNEUROSCI.2924-11.2011
79. van Ravenzwaaij D, Mulder MJ, Tuerlinckx F, Wagenmakers E-J (2012) Do the dynamics of prior information depend on task context? An analysis of optimal performance and an empirical test. Front Psychol 3:132. doi:10.3389/fpsyg.2012. 00132
80. van Wouwe NC, Ridderinkhof KR, van den Wildenberg WP, Band GP, Abisogun A, Elias WJ, Frysinger R, Wylie SA (2011) Deep brain stimulation of the subthalamic nucleus improves reward-based decision-learning in Parkinson's disease. Front Hum Neurosci 5:30. doi:10.3389/fnhum.2011.00030
81. Voss A, Rothermund K, Voss J (2004) Interpreting the parameters of the diffusion model: an empirical validation. Mem Cognit 32(7):1206-1220 (Pubitemid 40344330)
82. Wagenmakers E-J (2009) Methodological and empirical developments for the Ratcliff diffusion model of response times and accuracy. Eur J Cogn Psychol 21(5):641-671. doi:10.1080/09541440802205067
83. Witjas T, Baunez C, Henry JM, Delfini M, Regis J, Cherif AA, Peragut JC, Azulay JP (2005) Addiction in Parkinson's disease: impact of subthalamic nucleus deep brain stimulation. Mov Disord 20(8):1052-1055. doi:10.1002/mds.20501 (Pubitemid 41419526)
84. Zaghloul KA, Weidemann CT, Lega BC, Jaggi JL, Baltuch GH, Kahana MJ (2012) Neuronal activity in the human subthalamic nucleus encodes decision conflict during action selection. J Neurosci 32(7):2453-2460. doi:10.1523/JNEUROSCI.5815-11.2012