Dissociable effects of surprise and model update in parietal and anterior cingulate cortex

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 38, 2013, Pages

  O'Reilly, Jill X ^a   Schüffelgen, Urs ^b   Cuell, Steven F ^b   Behrens, Timothy E J ^a,c   Mars, Rogier B ^a,b   Rushworth, Matthew F S ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Attention; Bayes; Eye movement; Learning; Prediction

Indexed keywords

ANTERIOR CINGULATE; ARTICLE; BEHAVIOR; BRAIN REGION; HUMAN; LATERAL INTRAPARIETAL AREA; MODEL; PARIETAL CORTEX; POSTERIOR PARIETAL CORTEX; PRIORITY JOURNAL; PUPIL; PUPILLOMETRY; REACTION TIME; SACCADIC EYE MOVEMENT; ADULT; BAYES THEOREM; BIOLOGICAL MODEL; BRAIN MAPPING; CINGULATE GYRUS; CULTURAL ANTHROPOLOGY; FEMALE; KNOWLEDGE; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; PARIETAL LOBE; PHYSIOLOGY;

ADULT; BAYES THEOREM; BRAIN MAPPING; CULTURE; FEMALE; GYRUS CINGULI; HUMANS; KNOWLEDGE; MAGNETIC RESONANCE IMAGING; MALE; MODELS, NEUROLOGICAL; PARIETAL LOBE; PUPIL; REACTION TIME; SACCADES;

EID: 84884345145     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1305373110     Document Type: Article

References (63)

1. Friston K (2010) The free-energy principle: A unified brain theory? Nat Rev Neurosci 11(2):127-138.
2. Friston K, Kiebel S (2009) Predictive coding under the free-energy principle. Philos Trans R Soc Lond B Biol Sci 364(1521):1211-1221.
3. Posner MI, Snyder CRR, Davidson BJ (1980) Attention and the detection of signals. J Exp Psychol 109(2):160-174.
4. Posner MI, Walker JA, Friedrich FJ, Rafal RD (1984) Effects of parietal injury on covert orienting of attention. J Neurosci 4(7):1863-1874.
5. Sutton RS, Barto AG (1998) Reinforcement Learning: An Introduction (MIT Press, Cambridge, MA).
6. Baldi P, Itti L (2010) Of bits and wows: A Bayesian theory of surprise with applications to attention. Neural Netw 23(5):649-666.
7. Rescorla RA, Wagner AR (1972) A theory of Pavlovian conditioning: Variations in the effectiveness of reinforcement and nonreinforcement. Classical Conditioning II: Current Research and Theory, eds Black AH, Prokasy WF (Appleton-Century Crofts, New York), pp 64-99.
8. Knight FH (1921) Risk, Uncertainty and Profit (Hart, Schaffner & Marx, Boston, MA).
9. Courville AC, Daw ND, Touretzky DS (2006) Bayesian theories of conditioning in a changing world. Trends Cogn Sci 10(7):294-300.
10. Behrens TE, Woolrich MW, Walton ME, Rushworth MF (2007) Learning the value of information in an uncertain world. Nat Neurosci 10(9):1214-1221.
11. Dayan P (2012) Twenty-five lessons from computational neuromodulation. Neuron 76(1):240-256.
12. Colby CL, Duhamel JR, Goldberg ME (1996) Visual, presaccadic, and cognitive activation of single neurons in monkey lateral intraparietal area. J Neurophysiol 76(5):2841-2852.
13. Gold JI, Shadlen MN (2000) Representation of a perceptual decision in developing oculomotor commands. Nature 404(6776):390-394.
14. Platt ML, Glimcher PW (1999) Neural correlates of decision variables in parietal cortex. Nature 400(6741):233-238.
15. Yang T, Shadlen MN (2007) Probabilistic reasoning by neurons. Nature 447(7148): 1075-1080.
16. Milner A (1996) Neglect, extinction and the cortical streams of visual processing. Parietal Lobe Contributions to Orientation in 3D Space, Experimental Brain Research Series, eds Thier P, Karnath H-O (Springer, Berlin), Vol 25.
17. Milner A, Goodale M (1995) The Visual Brain in Action (Oxford Univ Press, Oxford).
18. Pierrot-Deseilligny C, Muri R (1996) Posterior parietal cortex control of saccades in man. Parietal Lobe Contributions to Orientation in 3D Space, Experimental Brain Research Series, eds Thier P, Karnath H-O (Springer, Berlin), Vol 25.
19. Mort DJ, et al. (2003) The anatomy of visual neglect. Brain 126(Pt 9):1986-1997.
20. Cox RT (1946) Probability, frequency and reasonable expectation. American Journal of Physics 14:1-13.
21. Vossel S, et al. (2013) Spatial Attention, Precision, and Bayesian Inference: A Study of Saccadic Response Speed. Cereb Cortex, 10.1093/cercor/bhs418.
22. Nassar MR, et al. (2012) Rational regulation of learning dynamics by pupil-linked arousal systems. Nat Neurosci 15(7):1040-1046.
23. Preuschoff K, 't Hart BM, Einhäuser W (2011) Pupil Dilation Signals Surprise: Evidence for Noradrenaline's Role in Decision Making. Front Neurosci 5:115.
24. Aston-Jones G, Cohen JD (2005) An integrative theory of locus coeruleus-norepinephrine function: Adaptive gain and optimal performance. Annu Rev Neurosci 28:403-450.
25. Bouret S, Sara SJ (2005) Network reset: A simplified overarching theory of locus coeruleus noradrenaline function. Trends Neurosci 28(11):574-582.
26. Yu AJ, Dayan P (2005) Uncertainty, neuromodulation, and attention. Neuron 46(4): 681-692.
27. Sara SJ (2009) The locus coeruleus and noradrenergic modulation of cognition. Nat Rev Neurosci 10(3):211-223.
28. Smith SM, et al. (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23(Suppl 1):S208-S219.
29. Jocham G, Neumann J, Klein TA, Danielmeier C, Ullsperger M (2009) Adaptive coding of action values in the human rostral cingulate zone. J Neurosci 29(23):7489-7496.
30. Kennerley SW, Walton ME, Behrens TE, Buckley MJ, Rushworth MF (2006) Optimal decision making and the anterior cingulate cortex. Nat Neurosci 9(7):940-947.
31. Mesulam MM, Nobre AC, Kim YH, Parrish TB, Gitelman DR (2001) Heterogeneity of cingulate contributions to spatial attention. Neuroimage 13(6 Pt 1):1065-1072.
32. 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.
33. Mars RB, et al. (2011) Diffusion-weighted imaging tractography-based parcellation of the human parietal cortex and comparison with human and macaque resting-state functional connectivity. J Neurosci 31(11):4087-4100.
34. Rushworth MF, Behrens TE, Johansen-Berg H (2006) Connection patterns distinguish 3 regions of human parietal cortex. Cereb Cortex 16(10):1418-1430.
35. Swisher JD, Halko MA, Merabet LB, McMains SA, Somers DC (2007) Visual topography of human intraparietal sulcus. J Neurosci 27(20):5326-5337.
36. Sereno MI, Pitzalis S, Martinez A (2001) Mapping of contralateral space in retinotopic coordinates by a parietal cortical area in humans. Science 294(5545):1350-1354.
37. Gottlieb J, Snyder LH (2010) Spatial and non-spatial functions of the parietal cortex. Curr Opin Neurobiol 20(6):731-740.
38. Cavada C, Goldman-Rakic PS (1989) Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe. J Comp Neurol 287(4):422-445.
39. Cavada C, Goldman-Rakic PS (1989) Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections. J Comp Neurol 287(4):393-421.
40. Caspers S, et al. (2008) The human inferior parietal lobule in stereotaxic space. Brain Struct Funct 212(6):481-495.
41. Molenberghs P, Mesulam MM, Peeters R, Vandenberghe RR (2007) Remapping attentional priorities: Differential contribution of superior parietal lobule and intraparietal sulcus. Cereb Cortex 17(11):2703-2712.
42. Vandenberghe R, Gitelman DR, Parrish TB, Mesulam MM (2001) Functional specificity of superior parietal mediation of spatial shifting. Neuroimage 14(3):661-673.
43. Molenberghs P, Gillebert CR, Peeters R, Vandenberghe R (2008) Convergence between lesion-symptom mapping and functional magnetic resonance imaging of spatially selective attention in the intact brain. J Neurosci 28(13):3359-3373.
44. Vandenberghe R, Molenberghs P, Gillebert CR (2012) Spatial attention deficits in humans: The critical role of superior compared to inferior parietal lesions. Neuropsychologia 50(6): 1092-1103.
45. Debener S, et al. (2005) Trial-by-trial coupling of concurrent electroencephalogram and functional magnetic resonance imaging identifies the dynamics of performance monitoring. J Neurosci 25(50):11730-11737.
46. Holroyd CB, et al. (2004) Dorsal anterior cingulate cortex shows fMRI response to internal and external error signals. Nat Neurosci 7(5):497-498.
47. Thiel CM, Zilles K, Fink GR (2004) Cerebral correlates of alerting, orienting and reorienting of visuospatial attention: An event-related fMRI study. Neuroimage 21(1): 318-328.
48. Mort DJ, et al. (2003) Differential cortical activation during voluntary and reflexive saccades in man. Neuroimage 18(2):231-246.
49. Hartwigsen G, et al. (2012) Left dorsal premotor cortex and supramarginal gyrus complement each other during rapid action reprogramming. J Neurosci 32(46): 16162-71a.
50. Mars RB, Piekema C, Coles MG, Hulstijn W, Toni I (2007) On the programming and reprogramming of actions. Cereb Cortex 17(12):2972-2979.
51. Rushworth MF, Ellison A, Walsh V (2001) Complementary localization and lateralization of orienting and motor attention. Nat Neurosci 4(6):656-661.
52. Rushworth MF, Paus T, Sipila PK (2001) Attention systems and the organization of the human parietal cortex. J Neurosci 21(14):5262-5271.
53. Gillebert CR, Mantini D, Peeters R, Dupont P, Vandenberghe R (2013) Cytoarchitectonic mapping of attentional selection and reorienting in parietal cortex. Neuroimage 67: 257-272.
54. Rushworth MF, Mars RB, Summerfield C (2009) General mechanisms for making decisions? Curr Opin Neurobiol 19(1):75-83.
55. Rushworth MF, Behrens TE (2008) Choice, uncertainty and value in prefrontal and cingulate cortex. Nat Neurosci 11(4):389-397.
56. Matsumoto M, Matsumoto K, Abe H, Tanaka K (2007) Medial prefrontal cell activity signaling prediction errors of action values. Nat Neurosci 10(5):647-656.
57. Cohen MX, Ranganath C (2007) Reinforcement learning signals predict future decisions. J Neurosci 27(2):371-378.
58. Quilodran R, Rothé M, Procyk E (2008) Behavioral shifts and action valuation in the anterior cingulate cortex. Neuron 57(2):314-325.
59. Karlsson MP, Tervo DG, Karpova AY (2012) Network resets in medial prefrontal cortex mark the onset of behavioral uncertainty. Science 338(6103):135-139.
60. Kolling N, Behrens TE, Mars RB, Rushworth MF (2012) Neural mechanisms of foraging. Science 336(6077):95-98.
61. Noonan MP, Mars RB, Rushworth MF (2011) Distinct roles of three frontal cortical areas in reward-guided behavior. J Neurosci 31(40):14399-14412.
62. Nobre AC, Coull JT, Frith CD, Mesulam MM (1999) Orbitofrontal cortex is activated during breaches of expectation in tasks of visual attention. Nat Neurosci 2(1):11-12.
63. Dayan P, Kakade S, Montague PR (2000) Learning and selective attention. Nat Neurosci 3(11, Suppl):1218-1223.