A neural mechanism underlying failure of optimal choice with multiple alternatives

Nature Neuroscience

Volumn 17, Issue 3, 2014, Pages 463-470

  Chau, Bolton K H ^a   Kolling, Nils ^a   Hunt, Laurence T ^b   Walton, Mark E ^a   Rushworth, Matthew F S ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BIOPHYSICAL MODEL; BOLD SIGNAL; CONTROLLED STUDY; DECISION MAKING; EFFECT SIZE; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; HUMAN EXPERIMENT; INHIBITION (PSYCHOLOGY); INTRAPARIETAL SULCUS; MACACA; MALE; NONHUMAN; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE SCANNER; OPTIMAL DECISION MAKING; PARIETAL CORTEX; PHYSICAL MODEL; PREDICTION; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; VENTROMEDIAL PREFRONTAL CORTEX; YOUNG ADULT;

ADULT; ATTENTION; DECISION MAKING; FEMALE; FUNCTIONAL NEUROIMAGING; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NEURAL NETWORKS (COMPUTER); PREFRONTAL CORTEX; PSYCHOMOTOR PERFORMANCE; YOUNG ADULT;

EID: 84896696352     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3649     Document Type: Article

References (60)

1. Vickery, T.J., Chun, M.M. & Lee, D. Ubiquity and Specificity of Reinforcement Signals throughout the Human Brain. Neuron 72, 166-177 (2011).
2. Noonan, M.P. et al. Separate value comparison and learning mechanisms in macaque medial and lateral orbitofrontal cortex. Proc. Natl. Acad. Sci. USA 107, 20547-20552 (2010).
3. Hunt, L.T. et al. Mechanisms underlying cortical activity during value-guided choice. Nat. Neurosci. 15, 470-476 (2012).
4. Wang, X.J. Neural dynamics and circuit mechanisms of decision-making. Curr. Opin. Neurobiol. 22, 1039-1046 (2012).
5. Boorman, E.D., Behrens, T.E., Woolrich, M.W. & Rushworth, M.F. How green is the grass on the other side? Frontopolar cortex and the evidence in favor of alternative courses of action. Neuron 62, 733-743 (2009).
6. Camille, N., Griffiths, C.A., Vo, K., Fellows, L.K. & Kable, J.W. Ventromedial frontal lobe damage disrupts value maximization in humans. J. Neurosci. 31, 7527-7532 (2011).
7. Rangel, A., Camerer, C. & Montague, P.R. A framework for studying the neurobiology of value-based decision making. Nat. Rev. Neurosci. 9, 545-556 (2008). (Pubitemid 351873461)
8. Kable, J.W. & Glimcher, P.W. The neurobiology of decision: consensus and controversy. Neuron 63, 733-745 (2009).
9. Rushworth, M.F., Noonan, M.P., Boorman, E.D., Walton, M.E. & Behrens, T.E. Frontal cortex and reward-guided learning and decision-making. Neuron 70, 1054-1069 (2011).
10. Bouret, S. & Richmond, B.J. Ventromedial and orbital prefrontal neurons differentially encode internally and externally driven motivational values in monkeys. J. Neurosci. 30, 8591-8601 (2010).
11. Monosov, I.E. & Hikosaka, O. Regionally distinct processing of rewards and punishments by the primate ventromedial prefrontal cortex. J. Neurosci. 32, 10318-10330 (2012).
12. Lebreton, M., Jorge, S., Michel, V., Thirion, B. & Pessiglione, M. An automatic valuation system in the human brain: evidence from functional neuroimaging. Neuron 64, 431-439 (2009).
13. Kable, J.W. & Glimcher, P.W. The neural correlates of subjective value during intertemporal choice. Nat. Neurosci. 10, 1625-1633 (2007). (Pubitemid 350175876)
14. Platt, M.L. & Glimcher, P.W. Neural correlates of decision variables in parietal cortex. Nature 400, 233-238 (1999). (Pubitemid 29334132)
15. Louie, K. & Glimcher, P.W. Separating value from choice: delay discounting activity in the lateral intraparietal area. J. Neurosci. 30, 5498-5507 (2010).
16. FitzGerald, T.H., Seymour, B. & Dolan, R.J. The role of human orbitofrontal cortex in value comparison for incommensurable objects. J. Neurosci. 29, 8388-8395 (2009).
17. Philiastides, M.G., Biele, G. & Heekeren, H.R. A mechanistic account of value computation in the human brain. Proc. Natl. Acad. Sci. USA 107, 9430-9435 (2010).
18. Kolling, N., Behrens, T.E., Mars, R.B. & Rushworth, M.F. Neural mechanisms of foraging. Science 336, 95-98 (2012).
19. De Martino, B., Fleming, S.M., Garrett, N. & Dolan, R.J. Confidence in value-based choice. Nat. Neurosci. 16, 105-110 (2013).
20. Hare, T.A., Schultz, W., Camerer, C.F., O'Doherty, J.P. & Rangel, A. Transformation of stimulus value signals into motor commands during simple choice. Proc. Natl. Acad. Sci. USA 108, 18120-18125 (2011).
21. Summerfield, C. & Tsetsos, K. Building bridges between perceptual and economic decision-making: neural and computational mechanisms. Front. Neurosci. 6, 70 (2012).
22. Churchland, A.K., Kiani, R. & Shadlen, M.N. Decision-making with multiple alternatives. Nat. Neurosci. 11, 693-702 (2008). (Pubitemid 351748120)
23. Usher, M. & McClelland, J.L. The time course of perceptual choice: the leaky, competing accumulator model. Psychol. Rev. 108, 550-592 (2001). (Pubitemid 33604137)
24. Wang, X.J. Probabilistic decision making by slow reverberation in cortical circuits. Neuron 36, 955-968 (2002).
25. Mars, R.B. et al. Diffusion-weighted imaging tractography-based parcellation of the human parietal cortex and comparison with human and macaque resting-state functional connectivity. J. Neurosci. 31, 4087-4100 (2011).
26. Gould, I.C., Nobre, A.C., Wyart, V. & Rushworth, M.F. Effects of decision variables and intraparietal stimulation on sensorimotor oscillatory activity in the human brain. J. Neurosci. 32, 13805-13818 (2012).
27. Louie, K., Grattan, L.E. & Glimcher, P.W. Reward value-based gain control: divisive normalization in parietal cortex. J. Neurosci. 31, 10627-10639 (2011).
28. Jocham, G., Hunt, L.T., Near, J. & Behrens, T.E. A mechanism for value-guided choice based on the excitation-inhibition balance in prefrontal cortex. Nat. Neurosci. 15, 960-961 (2012).
29. Wunderlich, K., Dayan, P. & Dolan, R.J. Mapping value based planning and extensively trained choice in the human brain. Nat. Neurosci. 15, 786-791 (2012).
30. Lim, S.L., O'Doherty, J.P. & Rangel, A. The decision value computations in the vmPFC and striatum use a relative value code that is guided by visual attention. J. Neurosci. 31, 13214-13223 (2011).
31. Rudebeck, P.H. & Murray, E.A. Dissociable effects of subtotal lesions within the macaque orbital prefrontal cortex on reward-guided behavior. J. Neurosci. 31, 10569-10578 (2011).
32. Walton, M.E., Behrens, T.E., Buckley, M.J., Rudebeck, P.H. & Rushworth, M.F. Separable learning systems in the macaque brain and the role of orbitofrontal cortex in contingent learning. Neuron 65, 927-939 (2010).
33. Noonan, M.P., Mars, R.B. & Rushworth, M.F. Distinct roles of three frontal cortical areas in reward-guided behavior. J. Neurosci. 31, 14399-14412 (2011).
34. Fellows, L.K. Deciding how to decide: ventromedial frontal lobe damage affects information acquisition in multi-attribute decision making. Brain 129, 944-952 (2006).
35. Lee, J. & Maunsell, J.H. A normalization model of attentional modulation of single unit responses. PLoS ONE 4, e4651 (2009).
36. Lee, J. & Maunsell, J.H. Attentional modulation of MT neurons with single or multiple stimuli in their receptive fields. J. Neurosci. 30, 3058-3066 (2010).
37. Sugrue, L.P., Corrado, G.S. & Newsome, W.T. Choosing the greater of two goods: neural currencies for valuation and decision making. Nat. Rev. Neurosci. 6, 363-375 (2005). (Pubitemid 40593482)
38. Padoa-Schioppa, C. Range-adapting representation of economic value in the orbitofrontal cortex. J. Neurosci. 29, 14004-14014 (2009).
39. Palminteri, S., Boraud, T., Lafargue, G., Dubois, B. & Pessiglione, M. Brain hemispheres selectively track the expected value of contralateral options. J. Neurosci. 29, 13465-13472 (2009).
40. Louie, K., Khaw, M.W. & Glimcher, P.W. Normalization is a general neural mechanism for context-dependent decision making. Proc. Natl. Acad. Sci. USA 110, 6139-6144 (2013).
41. Wallis, J.D. & Kennerley, S.W. Heterogeneous reward signals in prefrontal cortex. Curr. Opin. Neurobiol. 20, 191-198 (2010).
42. Soltani, A. & Wang, X.J. A biophysically based neural model of matching law behavior: melioration by stochastic synapses. J. Neurosci. 26, 3731-3744 (2006).
43. Ashbridge, E., Walsh, V. & Cowey, A. Temporal aspects of visual search studied by transcranial magnetic stimulation. Neuropsychologia 35, 1121-1131 (1997). (Pubitemid 27342964)
44. Sereno, A.B. & Maunsell, J.H.R. Shape selectivity in primate lateral intraparietal cortex. Nature 395, 500-503 (1998). (Pubitemid 28462444)
45. Grol, M.J., de Lange, F.P., Verstraten, F.A., Passingham, R.E. & Toni, I. Cerebral changes during performance of overlearned arbitrary visuomotor associations. J. Neurosci. 26, 117-125 (2006). (Pubitemid 43089524)
46. Noonan, M.P., Kolling, N., Walton, M.E. & Rushworth, M.F. Re-evaluating the role of the orbitofrontal cortex in reward and reinforcement. Eur. J. Neurosci. 35, 997-1010 (2012).
47. Wallis, J.D. Cross-species studies of orbitofrontal cortex and value-based decision-making. Nat. Neurosci. 15, 13-19 (2012).
48. Kaping, D., Vinck, M., Hutchison, R.M., Everling, S. & Womelsdorf, T. Specific contributions of ventromedial, anterior cingulate, and lateral prefrontal cortex for attentional selection and stimulus valuation. PLoS Biol. 9, e1001224 (2011).
49. Seo, H., Barraclough, D.J. & Lee, D. Lateral intraparietal cortex and reinforcement learning during a mixed-strategy game. J. Neurosci. 29, 7278-7289 (2009).
50. Simon, H.A. Rational choice and the structure of the environment. Psychol. Rev. 63, 129-138 (1956).
51. Deichmann, R., Gottfried, J.A., Hutton, C. & Turner, R. Optimized EPI for fMRI studies of the orbitofrontal cortex. Neuroimage 19, 430-441 (2003). (Pubitemid 39665693)
52. Smith, S.M. et al. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23 (suppl. 1): S208-S219 (2004). (Pubitemid 39421720)
53. Jenkinson, M., Bannister, P., Brady, M. & Smith, S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17, 825-841 (2002). (Pubitemid 35317016)
54. Jenkinson, M. Fast, automated, N-dimensional phase-unwrapping algorithm. Magn. Reson. Med. 49, 193-197 (2003). (Pubitemid 36042352)
55. Jenkinson, M. & Smith, S. A global optimisation method for robust affine registration of brain images. Med. Image Anal. 5, 143-156 (2001). (Pubitemid 35282800)
56. Beckmann, C.F., Jenkinson, M. & Smith, S.M. General multilevel linear modeling for group analysis in FMRI. Neuroimage 20, 1052-1063 (2003). (Pubitemid 37268124)
57. Woolrich, M.W., Behrens, T.E., Beckmann, C.F., Jenkinson, M. & Smith, S.M. Multilevel linear modelling for FMRI group analysis using Bayesian inference. Neuroimage 21, 1732-1747 (2004). (Pubitemid 38446594)
58. Woolrich, M. Robust group analysis using outlier inference. Neuroimage 41, 286-301 (2008).
59. Worsley, K.J., Evans, A.C., Marrett, S. & Neelin, P. A three-dimensional statistical analysis for CBF activation studies in human brain. J. Cereb. Blood Flow Metab. 12, 900-918 (1992).
60. Friston, K.J. et al. Psychophysiological and modulatory interactions in neuroimaging. Neuroimage 6, 218-229 (1997). (Pubitemid 27488453)