Frontal theta overrides Pavlovian learning biases

Journal of Neuroscience

Volumn 33, Issue 19, 2013, Pages 8541-8548

  Cavanagh, James F ^a   Eisenberg, Ian ^a   Guitart Masip, Marc ^b   Huys, Quentin ^c,d   Frank, Michael J ^a  

^a BROWN UNIVERSITY   (United States)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d UNIVERSITY HOSPITAL OF PSYCHIATRY ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BEHAVIOR; COMPUTER MODEL; DECISION MAKING; ELECTROENCEPHALOGRAPHY; FEMALE; HUMAN; HUMAN EXPERIMENT; LEARNING; MALE; NORMAL HUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; REWARD; TASK PERFORMANCE; THETA RHYTHM;

ADOLESCENT; ADULT; BIAS (EPIDEMIOLOGY); BRAIN MAPPING; COMPUTER SIMULATION; CONDITIONING, CLASSICAL; DECISION MAKING; ELECTROENCEPHALOGRAPHY; FEMALE; FRONTAL LOBE; HUMANS; MALE; MODELS, NEUROLOGICAL; REINFORCEMENT (PSYCHOLOGY); THETA RHYTHM; YOUNG ADULT;

EID: 84877292766     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5754-12.2013     Document Type: Article

References (36)

1. Beeler JA, Frank MJ, McDaid J, Alexander E, Turkson S, Sol Bernandez MS, McGehee DS, Zhuang X (2012) Arolefordopamine-mediatedlearning in the pathophysiology and treatment of Parkinson's disease. Cell Rep 2:1747-1761.CrossRefMedline
2. Cardinal RN, Parkinson JA, Hall J, Everitt BJ (2002) Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobehav Rev 26:321-352CrossRefMedline
3. Cavanagh JF, Cohen MX, Allen JJ (2009) Prelude to and resolution of an error: EEG phase synchrony reveals cognitive control dynamics during action monitoring. J Neurosci 29:98-105.CrossRef Medline
4. Cavanagh JF, Frank MJ, Klein TJ, Allen JJ (2010) Frontal theta links prediction errors to behavioral adaptation in reinforcement learning. Neuroimage 49:3198-3209.CrossRefMedline
5. 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 14:1462-1467.CrossRef Medline
6. Cavanagh JF, Figueroa CM, Cohen MX, Frank MJ (2012) Frontal theta reflects uncertainty and unexpectedness during exploration and exploitation. Cereb Cortex 22:2575-2586.CrossRefMedline
7. Cavanagh JF, Zambrano-Vazquez L, Allen JJ (2012) Theta lingua franca: a common mid-frontal substrate for action monitoring processes. Psychophysiology 49:220-238.CrossRefMedline
8. Cohen MX, Ranganath C (2007) Reinforcement learning signals predict future decisions. J Neurosci 27:371-378.CrossRefMedline
9. Cohen MX, van Gaal S, Ridderinkhof KR, Lamme VA (2009) Unconscious errors enhance prefrontal-occipital oscillatory synchrony. Front Hum Neurosci 3:54.CrossRefMedline
10. Dayan P, Balleine BW (2002) Reward, motivation, and reinforcement learning. Neuron 36:285-298. rossRefMedline
11. Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. JNeurosci Methods 134:9-21. CrossRefMedline
12. Frank MJ (2005) Dynamic dopamine modulation in the basal ganglia: a neurocomputational account of cognitive deficits in medicated and nonmedicated Parkinsonism. J Cogn Neurosci 17:51-72. CrossRefMedline
13. Frank MJ (2006) Hold your horses: a dynamic computational role for the subthalamic nucleus in decision making. Neural Netw 19:1120-1136.CrossRef Medline
14. Frank MJ, Seeberger LC, O'Reilly RC (2004) By carrot or by stick: cognitive reinforcement learning in parkinsonism. Science 306:1940-1943.CrossRef Medline
15. Gerfen CR, Surmeier DJ (2011) Modulation of striatal projection systems by dopamine. Annual review of neuroscience 34:441-466.CrossRef Medline
16. Guitart-Masip M, Fuentemilla L, Bach DR, Huys QJ, Dayan P, Dolan RJ, Duzel E (2011) Action dominates valence in anticipatory representations in the human striatum and dopaminergic midbrain. J Neurosci 31:7867-7875.CrossRefMedline
17. Guitart-Masip M, Chowdhury R, Sharot T, Dayan P, Duzel E, Dolan RJ (2012) Action controls dopaminergic enhancement of reward representations. Proc Natl Acad Sci USA 109:7511-7516.CrossRefMedline
18. Guitart-Masip M, Huys QJ, Fuentemilla L, Dayan P, Duzel E, Dolan RJ (2012) Go and no-go learning in reward and punishment: interactions between affect and effect. Neuroimage 62:154-166.CrossRefMedline
19. Hajihosseini A, Holroyd CB (2013) Frontal midline theta and N200 amplitude reflect complementary information about expectancy and outcome evaluation. Psychophysiology. Advance online publication. doi:10.1111/ psyp.12040. Retrieved: Feb. 27,2013.CrossRefMedline
20. Hampton AN, Bossaerts P, O'Doherty JP (2006) The role of the ventromedial prefrontal cortex in abstract state-based inference during decision making in humans. J Neurosci 26:8360-8367.CrossRefMedline
21. Hanslmayr S, Pastotter B, Bäuml KH, Gruber S, Wimber M, Klimesch W (2008) The electrophysiological dynamics of interference during the Stroop task. J Cogn Neurosci 20:215-225.CrossRefMedline
22. Hershberger WA (1986) An approach through the looking-glass. Animal Learning and Behavior 14:443-451. CrossRef
23. Holland PC (1979) Differential effects of omission contingencies on various components of Pavlovian appetitive conditioned responding in rats. J Exp Psychol Anim Behav Process 5:178-193.CrossRef Medline
24. Holroyd CB, Krigolson OE, Lee S (2011) Reward positivity elicited by predictive cues. Neuroreport 22:249-252.CrossRefMedline
25. Huys QJ, Cools R, Golzer M, Friedel E, Heinz A, Dolan RJ, Dayan P (2011) Disentangling the roles ofapproach, activation and valence in instrumental and Pavlovian responding. PLoS Comput Biol 7:e1002028.CrossRef Medline
26. Kass RE, Raftery AE (1995) Bayes factors. J Am Stat Assoc 90:773-795.CrossRef
27. Kayser J, Tenke CE (2006) Principal components analysis of Laplacian waveforms as a generic method for identifying ERP generator patterns: I. Evaluation with auditory oddball tasks. Clin Neurophysiol 117:348-368.CrossRef Medline
28. Kravitz AV, Tye LD, Kreitzer AC (2012) Distinct roles for direct and indirect pathway striatal neurons in reinforcement. Nat Neurosci 15:816-818.CrossRef Medline
29. Oliveira FT, McDonald JJ, Goodman D (2007) Performance monitoring in the anterior cingulate is not all error related: expectancy deviation and the representation of action-outcome associations. J Cogn Neurosci 19:1994-2004.CrossRefMedline
30. Prévost C, Liljeholm M, Tyszka JM, O'Doherty JP (2012) Neural correlates of specific and general Pavlovian-to-instrumental transfer within human amygdalar subregions: a high-resolution fMRI study. J Neurosci 32:8383-8390.CrossRefMedline
31. Ratcliff R, Frank MJ (2012) Reinforcement-based decision making in corti- costriatal circuits: mutual constraints by neurocomputational and diffusion models. Neural Comput 24:1186-1229.CrossRefMedline
32. Talmi D, Seymour B, Dayan P, Dolan RJ (2008) Human Pavlovian- instrumental transfer. J Neurosci 28:360-368.CrossRefMedline
33. van de Vijver I, Ridderinkhof KR, Cohen MX (2011) Frontal oscillatory dynamics predict feedback learning and action adjustment. J Cogn Neurosci 23:4106-4121.CrossRefMedline
34. Van Veen V, Carter CS (2002) Thetimingofaction-monitoringprocessesin the anterior cingulate cortex. J Cogn Neurosci 14:593-602.CrossRef Medline
35. Yeung N, Botvinick MM, Cohen JD (2004) The neural basis of error detection: conflict monitoring and the error-related negativity. Psychol Rev 111:931-959.CrossRefMedline
36. 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 32:2453-2460.CrossRef Medline