Error Monitoring Using External Feedback: Specific Roles of the Habenular Complex, the Reward System, and the Cingulate Motor Area Revealed by Functional Magnetic Resonance Imaging

Overview

Journal J Neurosci

Specialty Neurology

Date 2003 May 24

PMID 12764119

Citations 172

Authors

Markus Ullsperger

D Yves von Cramon

Affiliations

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Abstract

The dopaminergic system has been shown to be involved in the processing of rewarding stimuli, specifically of errors in reward prediction, in animal studies as well as in recent neuroimaging studies in humans. Furthermore, a specific role of dopamine in the human homolog of the rostral cingulate motor area (rCMA) was proposed in a recent model of error detection. Negative feedback as well as self-detected errors elicit a negative event-related brain potential probably generated in the rCMA. We performed two experiments using functional magnetic resonance imaging to investigate the brain activity related to negative and positive feedback in a dynamically adaptive motion prediction task. Whereas positive feedback raised hemodynamic activity in the ventral striatum (nucleus accumbens), negative feedback activated the rCMA, the inferior anterior insula, and the epithalamus (habenular complex). These data demonstrate the role of the habenular complex in the control of the human reward system, a function previously hypothesized on the basis of animal research. The rCMA reacted only to errors with negative feedback but not to errors without feedback, which ruled out an influence of response conflict or uncertainty on its role in error detection by external signals.

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References

Wansapura J, Holland S, Dunn R, Ball Jr W . NMR relaxation times in the human brain at 3.0 tesla. J Magn Reson Imaging. 1999; 9(4):531-8. DOI: 10.1002/(sici)1522-2586(199904)9:4<531::aid-jmri4>3.0.co;2-l. View

Horvitz J . Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events. Neuroscience. 2000; 96(4):651-6. DOI: 10.1016/s0306-4522(00)00019-1. View

Schultz W, Dickinson A . Neuronal coding of prediction errors. Annu Rev Neurosci. 2000; 23:473-500. DOI: 10.1146/annurev.neuro.23.1.473. View

Miezin F, Maccotta L, Ollinger J, Petersen S, Buckner R . Characterizing the hemodynamic response: effects of presentation rate, sampling procedure, and the possibility of ordering brain activity based on relative timing. Neuroimage. 2000; 11(6 Pt 1):735-59. DOI: 10.1006/nimg.2000.0568. View

Elliott R, Friston K, Dolan R . Dissociable neural responses in human reward systems. J Neurosci. 2000; 20(16):6159-65. PMC: 6772605. View

Schultz W . Multiple reward signals in the brain. Nat Rev Neurosci. 2001; 1(3):199-207. DOI: 10.1038/35044563. View

Berns G, McClure S, Pagnoni G, Montague P . Predictability modulates human brain response to reward. J Neurosci. 2001; 21(8):2793-8. PMC: 6762527. View

Lohmann G, Muller K, Bosch V, Mentzel H, Hessler S, Chen L . LIPSIA--a new software system for the evaluation of functional magnetic resonance images of the human brain. Comput Med Imaging Graph. 2001; 25(6):449-57. DOI: 10.1016/s0895-6111(01)00008-8. View

Ullsperger M, von Cramon D . Subprocesses of performance monitoring: a dissociation of error processing and response competition revealed by event-related fMRI and ERPs. Neuroimage. 2001; 14(6):1387-401. DOI: 10.1006/nimg.2001.0935. View

10.

Bush G, Vogt B, Holmes J, Dale A, Greve D, Jenike M . Dorsal anterior cingulate cortex: a role in reward-based decision making. Proc Natl Acad Sci U S A. 2002; 99(1):523-8. PMC: 117593. DOI: 10.1073/pnas.012470999. View

11.

Pagnoni G, Zink C, Montague P, Berns G . Activity in human ventral striatum locked to errors of reward prediction. Nat Neurosci. 2002; 5(2):97-8. DOI: 10.1038/nn802. View

12.

Holroyd C, Coles M . The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity. Psychol Rev. 2002; 109(4):679-709. DOI: 10.1037/0033-295X.109.4.679. View

13.

Schultz W . Getting formal with dopamine and reward. Neuron. 2002; 36(2):241-63. DOI: 10.1016/s0896-6273(02)00967-4. View

14.

Luu P, Tucker D, Derryberry D, Reed M, Poulsen C . Electrophysiological responses to errors and feedback in the process of action regulation. Psychol Sci. 2003; 14(1):47-53. DOI: 10.1111/1467-9280.01417. View

15.

Volz K, Schubotz R, von Cramon D . Predicting events of varying probability: uncertainty investigated by fMRI. Neuroimage. 2003; 19(2 Pt 1):271-80. DOI: 10.1016/s1053-8119(03)00122-8. View

16.

Josephs O, Turner R, Friston K . Event-related f MRI. Hum Brain Mapp. 2010; 5(4):243-8. DOI: 10.1002/(SICI)1097-0193(1997)5:4<243::AID-HBM7>3.0.CO;2-3. View

17.

Miltner W, Braun C, Coles M . Event-related brain potentials following incorrect feedback in a time-estimation task: evidence for a "generic" neural system for error detection. J Cogn Neurosci. 2013; 9(6):788-98. DOI: 10.1162/jocn.1997.9.6.788. View

18.

Nishikawa T, Fage D, Scatton B . Evidence for, and nature of, the tonic inhibitory influence of habenulointerpeduncular pathways upon cerebral dopaminergic transmission in the rat. Brain Res. 1986; 373(1-2):324-36. DOI: 10.1016/0006-8993(86)90347-1. View

19.

Christoph G, Leonzio R, Wilcox K . Stimulation of the lateral habenula inhibits dopamine-containing neurons in the substantia nigra and ventral tegmental area of the rat. J Neurosci. 1986; 6(3):613-9. PMC: 6568453. View

20.

Rabbitt P . Errors and error correction in choice-response tasks. J Exp Psychol. 1966; 71(2):264-72. DOI: 10.1037/h0022853. View