Task-related dissociation in ERN amplitude as a function of obsessive-compulsive symptoms

Max Planck Institute for Neurological Research, Cologne, Germany.
Neuropsychologia (Impact Factor: 3.3). 08/2009; 47(8-9):1978-87. DOI: 10.1016/j.neuropsychologia.2009.03.010
Source: PubMed


Hyperactive cortico-striatal circuits including the anterior cingulate cortex (ACC) have been implicated to underlie obtrusive thoughts and repetitive behaviors in obsessive-compulsive disorder (OCD). Larger error-related negativities (ERNs) in OCD patients during simple flanker tasks have been proposed to reflect an amplified error signal in these hyperactive circuits. Such amplified error signals typically are associated with an adaptive change in response, yet in OCD these same repetitive responses persist to the point of distress and impairment. In contrast to this repetitive character of OC behavior, larger ERN amplitudes have been linked to better avoidance learning in reinforcement learning tasks. Study I thus investigated if OC symptomatology in non-patients predicted an enhanced ERN after suboptimal choices in a probabilistic learning task. Absent any behavioral differences, higher OC symptoms predicted smaller ERNs. Study II replicated this effect in an independent sample while also replicating findings of a larger ERN in a flanker task. There were no relevant behavioral differences in reinforcement learning or error monitoring as a function of symptom score. These findings implicate different, yet overlapping neural mechanisms underlying the negative deflection in the ERP following the execution of an erroneous motor response and the one following a suboptimal choice in a reinforcement learning paradigm. OC symptomatology may be dissociated in these neural systems, with hypoactivity in a system that enables learning to avoid maladaptive choices, and hyperactivity in another system that enables the same behavior to be repeated when it was assessed as not quite good enough the first time.

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Available from: James F Cavanagh
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    • "More specifically, the Ne has been proposed to reflect the activity of a generic prefrontal performance monitoring system and to track learning-related changes in the evaluation and utilization of information about performance outcomes (Holroyd and Coles, 2002). Consistent with this notion, previous findings suggested a link between the Ne and error-induced behavioral adaptation during reinforcement learning (e.g., Frank et al., 2005; Gründler et al., 2009; Unger et al., 2012). Moreover, there is substantial evidence for motivational and affective influences on the Ne in adults (for a review, see Gehring et al., 2012). "
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    ABSTRACT: Developmental researchers have suggested that adolescents are characterized by stronger reward sensitivity than both children and younger adults. However, at this point, little is known about the extent to which developmental differences in incentive processing influence feedback-based learning. In this study, we applied an incentivized reinforcement learning task, in which errors resulted in losing money (loss condition), failure to gain money (gain condition), or neither (no-incentive condition). Children (10-11 years), mid-adolescents (13-14 years), and late adolescents (15-17 years) performed this task while event-related potentials (ERPs) were recorded. We focused our analyses on two ERP correlates of error processing, the error-negativity (Ne) and the error positivity (Pe) that are thought to reflect a rapid preconscious performance monitoring mechanism (Ne) and conscious detection and/or evaluation of response errors (Pe). Participants in all age groups responded more quickly and accurately in gain and loss conditions than in the no-incentive condition. The performance data thus did not support the idea that incentives generally have a greater behavioral impact in adolescents than in children. While the Ne was not modulated by the incentive manipulation, both children and adolescents showed a larger Pe to errors in the gain condition compared to loss and no-incentive conditions. This is in contrast to results from adult studies, in which the Ne but not the Pe was enhanced for high-value errors, raising the possibility that motivational influences on performance monitoring might be reflected in the activity of separable neural systems in children and adolescents vs. adults. In contrast to the idea of higher reward/incentive sensitivity in adolescents, our findings suggest that incentives have similar effects on feedback-based learning from late childhood into late adolescence with no changes in preferences for “trick over treat".
    Full-text · Article · Sep 2014 · Frontiers in Psychology
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    • "Previously, it has been demonstrated that the ERN is greater for unexpected error outcomes in OC groups than healthy individuals [12], [27], [69]. However, the ERN findings differed from the results of FRN amplitudes in subclinical populations with OC symptoms and OCD, in which reduced FRN has been discovered [30]–[32], [70]. The explanation of these results may relate to the bias for overestimation of possible negative outcomes in OC populations [71], [72], but such an explanation does not rule out the influence of anxiety. "
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    ABSTRACT: Feedback-related negativity (FRN) is believed to be an important electrophysiology index of "external" negative feedback processing. Previous studies on FRN in obsessive-compulsive (OC) individuals are scarce and controversial. In these studies, anxiety symptoms were not evaluated in detail. However, OC disorders have a number of radical differences from anxiety disorders. It is necessary to study FRN and its neuroanatomical correlates in OC individuals without anxious symptoms. A total of 628 undergraduate students completed an OC questionnaire. We chose 14 students who scored in the upper 10% and 14 students who scored in the lowest 10% without anxiety symptoms as a subclinical OC group (SOC) and a low obsessive-compulsive group (LOC). The students all performed the revised Iowa Gambling Task. We used the event-related potentials (ERP) and standardized low-resolution brain electromagnetic tomography (sLORETA) to track external negative feedback processing and its substrate in the brain. Our study revealed poorer decision-making ability and greater FRN amplitudes in SOC subjects compared with LOC controls. The SOC subjects displayed anterior prefrontal cortex (aPFC) hyperactivation during the loss feedback condition. Specifically, we found an intercorrelation of current source density during the loss condition between the dorsal anterior cingulate cortex (dACC) and aPFC in the LOC subjects but not in the SOC group. Our results support the notion that overactive external feedback error processing may reflect a candidate endophenotype of OC. We also provide important information on the dysfunction in the interaction between aPFC and dACC in populations with OC. Nevertheless, the findings support that OC may be distinguished from other anxiety disorders using a new electrophysiology perspective.
    Full-text · Article · Mar 2014 · PLoS ONE
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    • "To our knowledge, such an anatomical dissociation of encoding different types of errors has only rarely been reported (Quilodran et al. 2008; Kennerley et al. 2011). In human Electroencephalogram (EEG) studies, slightly different scalp EEG topographies and source locations of error-related negativity amplitudes have been reported for errors of different origins (erroneous motor executions vs. suboptimal choices) (Grundler et al. 2009; Cavanagh et al. 2010; see also Holroyd et al. 2009). "
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    ABSTRACT: Errors indicate the need to adjust attention for improved future performance. Detecting errors is thus a fundamental step to adjust and control attention. These functions have been associated with the dorsal anterior cingulate cortex (dACC), predicting that dACC cells should track the specific processing states giving rise to errors in order to identify which processing aspects need readjustment. Here, we tested this prediction by recording cells in the dACC and lateral prefrontal cortex (latPFC) of macaques performing an attention task that dissociated 3 processing stages. We found that, across prefrontal subareas, the dACC contained the largest cell populations encoding errors indicating (1) failures of inhibitory control of the attentional focus, (2) failures to prevent bottom-up distraction, and (3) lapses when implementing a choice. Error-locked firing in the dACC showed the earliest latencies across the PFC, emerged earlier than reward omission signals, and involved a significant proportion of putative inhibitory interneurons. Moreover, early onset error-locked response enhancement in the dACC was followed by transient prefrontal-cingulate inhibition, possibly reflecting active disengagement from task processing. These results suggest a functional specialization of the dACC to track and identify the actual processes that give rise to erroneous task outcomes, emphasizing its role to control attentional performance.
    Full-text · Article · Mar 2014 · Cerebral Cortex
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