Multimodal Neuroimaging Dissociates Hemodynamic and Electrophysiological Correlates of Error Processing

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2011 Oct 5

PMID 21969565

Citations 54

Authors

Yigal Agam

Matti S Hamalainen

Adrian K C Lee

Kara A Dyckman

Jesse S Friedman

Marlisa Isom

Nikos Makris

Dara S Manoach

Affiliations

Soon will be listed here.

Abstract

Recognizing errors and adjusting responses are fundamental to adaptive behavior. The error-related negativity (ERN) and error-related functional MRI (fMRI) activation of the dorsal anterior cingulate cortex (dACC) index these processes and are thought to reflect the same neural mechanism. In the present study, we evaluated this hypothesis. Although errors elicited robust dACC activation using fMRI, combined electroencephalography and magnetoencephalography data localized the ERN to the posterior cingulate cortex (PCC). ERN amplitude correlated with fMRI activation in both the PCC and dACC, and these two regions showed coordinated activity based on functional connectivity MRI. Finally, increased microstructural integrity of the posterior cingulum bundle, as measured by diffusion tensor imaging, predicted faster error correction. These findings suggest that the PCC generates the ERN and communicates with the dACC to subserve error processing. They challenge current models that view fMRI activation of the dACC as the hemodynamic reflection of the ERN.

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References

McCoy A, Crowley J, Haghighian G, Dean H, Platt M . Saccade reward signals in posterior cingulate cortex. Neuron. 2003; 40(5):1031-40. DOI: 10.1016/s0896-6273(03)00719-0. View

Menon V, Adleman N, White C, Glover G, Reiss A . Error-related brain activation during a Go/NoGo response inhibition task. Hum Brain Mapp. 2001; 12(3):131-43. PMC: 6872006. DOI: 10.1002/1097-0193(200103)12:3<131::aid-hbm1010>3.0.co;2-c. View

Magno E, Foxe J, Molholm S, Robertson I, Garavan H . The anterior cingulate and error avoidance. J Neurosci. 2006; 26(18):4769-73. PMC: 6674160. DOI: 10.1523/JNEUROSCI.0369-06.2006. View

Lin F, Belliveau J, Dale A, Hamalainen M . Distributed current estimates using cortical orientation constraints. Hum Brain Mapp. 2005; 27(1):1-13. PMC: 6871274. DOI: 10.1002/hbm.20155. View

Ahlfors S, Han J, Lin F, Witzel T, Belliveau J, Hamalainen M . Cancellation of EEG and MEG signals generated by extended and distributed sources. Hum Brain Mapp. 2009; 31(1):140-9. PMC: 2797557. DOI: 10.1002/hbm.20851. View

Williams Z, Bush G, Rauch S, Cosgrove G, Eskandar E . Human anterior cingulate neurons and the integration of monetary reward with motor responses. Nat Neurosci. 2004; 7(12):1370-5. DOI: 10.1038/nn1354. View

Vogt B, Vogt L, Laureys S . Cytology and functionally correlated circuits of human posterior cingulate areas. Neuroimage. 2005; 29(2):452-66. PMC: 2649771. DOI: 10.1016/j.neuroimage.2005.07.048. View

Smith B, Mitchell D, Hardin M, Jazbec S, Fridberg D, Blair R . Neural substrates of reward magnitude, probability, and risk during a wheel of fortune decision-making task. Neuroimage. 2008; 44(2):600-9. PMC: 2695942. DOI: 10.1016/j.neuroimage.2008.08.016. View

Garavan H, Ross T, Murphy K, Roche R, Stein E . Dissociable executive functions in the dynamic control of behavior: inhibition, error detection, and correction. Neuroimage. 2002; 17(4):1820-9. DOI: 10.1006/nimg.2002.1326. View

10.

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

11.

Kerns J, Cohen J, MacDonald 3rd A, Cho R, Stenger V, Carter C . Anterior cingulate conflict monitoring and adjustments in control. Science. 2004; 303(5660):1023-6. DOI: 10.1126/science.1089910. View

12.

Ridderinkhof K, Ullsperger M, Crone E, Nieuwenhuis S . The role of the medial frontal cortex in cognitive control. Science. 2004; 306(5695):443-7. DOI: 10.1126/science.1100301. View

13.

Logothetis N . What we can do and what we cannot do with fMRI. Nature. 2008; 453(7197):869-78. DOI: 10.1038/nature06976. View

14.

Fitzgerald K, Perkins S, Angstadt M, Johnson T, Stern E, Welsh R . The development of performance-monitoring function in the posterior medial frontal cortex. Neuroimage. 2009; 49(4):3463-73. PMC: 2846421. DOI: 10.1016/j.neuroimage.2009.11.004. View

15.

Mathalon D, Whitfield S, Ford J . Anatomy of an error: ERP and fMRI. Biol Psychol. 2003; 64(1-2):119-41. DOI: 10.1016/s0301-0511(03)00105-4. View

16.

Fujiwara J, Tobler P, Taira M, Iijima T, Tsutsui K . Segregated and integrated coding of reward and punishment in the cingulate cortex. J Neurophysiol. 2009; 101(6):3284-93. DOI: 10.1152/jn.90909.2008. View

17.

Scheffers M, Coles M . Performance monitoring in a confusing world: error-related brain activity, judgments of response accuracy, and types of errors. J Exp Psychol Hum Percept Perform. 2000; 26(1):141-151. DOI: 10.1037//0096-1523.26.1.141. View

18.

Endrass T, Reuter B, Kathmann N . ERP correlates of conscious error recognition: aware and unaware errors in an antisaccade task. Eur J Neurosci. 2007; 26(6):1714-20. DOI: 10.1111/j.1460-9568.2007.05785.x. View

19.

Holroyd C, Larsen J, Cohen J . Context dependence of the event-related brain potential associated with reward and punishment. Psychophysiology. 2004; 41(2):245-53. DOI: 10.1111/j.1469-8986.2004.00152.x. View

20.

Polli F, Barton J, Cain M, Thakkar K, Rauch S, Manoach D . Rostral and dorsal anterior cingulate cortex make dissociable contributions during antisaccade error commission. Proc Natl Acad Sci U S A. 2005; 102(43):15700-5. PMC: 1255733. DOI: 10.1073/pnas.0503657102. View