Event‐related potential activity in the basal ganglia differentiates rewards from nonrewards: Response to commentary

Foti, Dan; Weinberg, Anna; Dien, Joseph; Hajcak, Greg

doi:10.1002/hbm.21357

Cited by 52 publications

(35 citation statements)

References 14 publications

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“…The ACC and a second potential source in the basal ganglia appear to contribute to the FN in distinct ways, such that the former is associated with increased activity to monetary loss and the latter with increased activity to monetary gain; this interpretation is also consistent with the extant neuroimaging literature (Liu et al, 2011). As with any application of source analysis to ERP data, however, this result should be interpreted with some caution (Cohen et al, 2011a; Foti et al, 2011c) and further substantiated with complementary evidence from depth electrodes and lesion studies. For example, gain-related delta may reflect coordinated frontostriatal activation to rewards rather than a direct contribution of the striatum to the scalp-recorded signal per se.…”

Section: Discussionmentioning

confidence: 61%

Anterior cingulate activity to monetary loss and basal ganglia activity to monetary gain uniquely contribute to the feedback negativity

Foti¹,

Weinberg²,

Bernat³

et al. 2015

Clinical Neurophysiology

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Objective The feedback negativity (FN) is an event-related potential that differentiates unfavorable versus favorable outcomes. Although thought to reflect error-related activity within the anterior cingulate cortex, recent work indicates the FN may also reflect reward-related activity that has been linked to the basal ganglia. To date, it remains unclear how to reconcile these conflicting perspectives. Methods We decomposed the FN by applying time-frequency analysis to isolate activity unique to monetary losses and gains. The FN was recorded from 84 individuals during a laboratory gambling task. Results Two signals contributed to the FN elicited by unpredictable outcomes: theta activity (4-7 Hz) was increased following monetary loss, and delta activity (< 3 Hz) was increased following monetary gain. Predictable outcomes elicited delta but not theta activity. Source analysis revealed distinct generators, with loss-related theta localized to the anterior cingulate cortex and gain-related delta to a possible source in the striatum. Symptoms of depression, anxiety, and stress reactivity were specifically associated with blunted gain-related delta. Conclusions The FN may be a composite of loss- and gain-related neural activity, reflecting distinct facets of reward processing. Significance Gain-related delta activity may provide unique information about reward dysfunction in major depression and other internalizing psychopathology.

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Section: Discussionmentioning

confidence: 61%

Anterior cingulate activity to monetary loss and basal ganglia activity to monetary gain uniquely contribute to the feedback negativity

Foti¹,

Weinberg²,

Bernat³

et al. 2015

Clinical Neurophysiology

Self Cite

149

164

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“…Several studies localized its origin along the anterior cingulate cortex (Bellebaum and Daum, 2008;Gruendler et al, 2011;Hewig et al, 2007;Mathewson et al, 2008;Miltner et al, 1997;Potts et al, 2006;Zhou et al, 2010). Others found the source rather in the posterior cingulate cortex (Badgaiyan and Posner, 1998;Cohen and Ranganath, 2007;Hewig et al, 2007;Müller et al, 2005;Nieuwenhuis et al, 2005b) or even in the basal ganglia (Carlson et al, 2011;Foti et al, 2011aFoti et al, , 2011bMartin et al, 2009;Nieuwenhuis et al, 2005b). Besides the inconsistent localizations, the methods used in these studies face several limitations when trying to overcome the unsolvable inverse problem (Helmholtz, 1853).…”

Section: Discussionmentioning

confidence: 99%

“…Although many source estimation studies localized the FRN in the large area of the ACC (for review cf Walsh and Anderson, 2012), several studies also located the origin of the FRN in the posterior cingulate cortex (Badgaiyan and Posner, 1998;Cohen and Ranganath, 2007;Hewig et al, 2007;Müller et al, 2005;Nieuwenhuis et al, 2005b). Others (Carlson et al, 2011;Foti et al, 2011aFoti et al, , 2011bMartin et al, 2009;Nieuwenhuis et al, 2005b) found the source within the basal ganglia, which is also known to crucially process RPEs. All source localization studies so far face the unsolvable inverse problem, which states that the same topographical maps measured at the scalp surface can be caused by several different sources and/or source configurations (Helmholtz, 1853).…”

Section: Introductionmentioning

confidence: 99%

The feedback-related negativity (FRN) revisited: New insights into the localization, meaning and network organization

et al. 2014

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Changes in response contingencies require adjusting ones assumptions about outcomes of behaviors. Such adaptation processes are driven by reward prediction error (RPE) signals which reflect the inadequacy of expectations. Signals resembling RPEs are known to be encoded by mesencephalic dopamine neurons projecting to the striatum and frontal regions. Although regions that process RPEs, such as the dorsal anterior cingulate cortex (dACC), have been identified, only indirect evidence links timing and network organization of RPE processing in humans. In electroencephalography (EEG), which is well known for its high temporal resolution, the feedback-related negativity (FRN) has been suggested to reflect RPE processing. Recent studies, however, suggested that the FRN might reflect surprise, which would correspond to the absolute, rather than the signed RPE signals. Furthermore, the localization of the FRN remains a matter of debate. In this simultaneous EEG-functional magnetic resonance imaging (fMRI) study, we localized the FRN directly using the superior spatial resolution of fMRI without relying on any spatial constraint or other assumption. Using two different single-trial approaches, we consistently found a cluster within the dACC. One analysis revealed additional activations of the salience network. Furthermore, we evaluated the effect of signed RPEs and surprise signals on the FRN amplitude. We considered that both signals are usually correlated and found that only surprise signals modulate the FRN amplitude. Last, we explored the pathway of RPE signals using dynamic causal modeling (DCM). We found that the surprise signals are directly projected to the source region of the FRN. This finding contradicts earlier theories about the network organization of the FRN, but is in line with a recent theory stating that dopamine neurons also encode surprise-like saliency signals. Our findings crucially advance the understanding of the FRN. We found compelling evidence that the FRN originates from the dACC. Furthermore, we clarified the functional role of the FRN, and determined the role of the dACC within the RPE network. These findings should enable us to study the processing of surprise and adjustment signals in the dACC in healthy and also in psychiatric patients.

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“…Accordingly, while several studies identified the dorsal ACC as the major generator of the FN (Bellebaum & Daum, ; Gehring & Willoughby, ; Holroyd et al., ; Miltner et al., ), several other cortical sources close or more distant to the dorsal ACC have also been reported, including, for example, the rostral ACC and the posterior cingulate (Nieuwenhuis, Slagter et al., ), lateral frontal cortex and temporal sites (Bellebaum & Daum, ), as well as the presupplementary and supplementary motor area (Holroyd, Nieuwenhuis et al., ). Others have even identified subcortical regions (i.e., the striatum) as the main FN source (Foti et al., ), although these findings are not unquestioned (Cohen, Cavanagh, & Slagter, ; also see Foti, Weinberg, Dien, & Hajcak, ). Moreover, single unit recordings in monkeys suggest that there are several functional subpopulations of neurons in the MFC that can code distinct kinds of reward information like outcome favorableness (e.g., Matsumoto, Matsumoto, Abe, & Tanaka, ), recent reward history (e.g., Seo & Lee, ), or unexpectedness of a particular reward (Hayden et al., ).…”

Section: Discussionmentioning

confidence: 99%

Feedback‐related potentials are sensitive to sequential order of decision outcomes in a gambling task

2012

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The feedback negativity (FN) has been repeatedly linked to expectancies about decision outcomes. Sequential outcome order is likely to influence such expectancies but has been widely disregarded. We therefore investigated whether the three-trial order of decision outcomes in a gambling task influences the FN as well as the P200 and P300. All three deflections were not only influenced by the outcome valence of the current trial but also by the outcomes of the two preceding trials. In detail, the FN and P300 to any current trial outcome were largest when the outcomes in the two preceding trials had an opposite valence. The P200 was highest in the context of two directly preceding wins, indicating that it may reflect representations of local outcome history. Our findings demonstrate that neural systems involved in decision outcome processing dynamically and continuously integrate the local outcome history for the evaluation of present outcomes.

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Event‐related potential activity in the basal ganglia differentiates rewards from nonrewards: Response to commentary

Cited by 52 publications

References 14 publications

Anterior cingulate activity to monetary loss and basal ganglia activity to monetary gain uniquely contribute to the feedback negativity

Anterior cingulate activity to monetary loss and basal ganglia activity to monetary gain uniquely contribute to the feedback negativity

The feedback-related negativity (FRN) revisited: New insights into the localization, meaning and network organization

Feedback‐related potentials are sensitive to sequential order of decision outcomes in a gambling task

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