Is Decreased Prefrontal Cortical Sensitivity to Monetary Reward Associated With Impaired Motivation and Self-Control in Cocaine Addiction?

Goldstein, Rita Z.; Alia‐Klein, Nelly; Tomasi, Dardo; Zhang, Lei; Cottone, Lisa A.; Maloney, Thomas; Telang, Frank; Caparelli, Elisabeth C.; Chang, Linda; Ernst, Thomas; Samaras, Dimitris; Squires, Nancy K.; Volkow, Nora D.

doi:10.1176/ajp.2007.164.1.43

Cited by 199 publications

(198 citation statements)

References 41 publications

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“…In drug dependency, the dorsal caudate is implicated in compulsive drug seeking and habit formation (Everitt et al, 2008;Koob and Volkow, 2010). Our finding is consistent with studies reporting decreased neural sensitivity in drug-dependent patients for nondrug-related rewarding stimuli (Buhler et al, 2010;Diekhof et al, 2008;Goldstein et al, 2007;Peters et al, 2011;Wrase et al, 2007) and with a hypothesis of nondrug rewards being undervalued in drug dependency (Hyman et al, 2006).…”

Section: Discussionsupporting

confidence: 90%

“…Fewer studies have investigated neural responses to nondrug-related rewards in dependent individuals. Decreased neural responses to nondrug-related rewards have been reported with cocaine (Garavan et al, 2000;Goldstein et al, 2007), alcohol (Wrase et al, 2007), nicotine, (Buhler et al, 2010;Peters et al, 2011) and opiate (Martin-Soelch et al, 2001) misuse. Investigation of neural responses to aversive stimuli in addiction is rare.…”

Section: Introductionmentioning

confidence: 98%

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Abnormal Brain Activity During a Reward and Loss Task in Opiate-Dependent Patients Receiving Methadone Maintenance Therapy

Gradin

Baldacchino

Balfour

et al. 2013

Neuropsychopharmacol

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A core feature of human drug dependency is persistence in seeking and using drugs at the expense of other life goals. It has been hypothesized that addiction is associated with overvaluation of drug-related rewards and undervaluation of natural, nondrug-related rewards. Humans additionally tend to persist in using drugs despite adverse consequences. This suggests that the processing of both rewarding and aversive information may be abnormal in addictions. We used fMRI to examine neural responses to reward and loss events in opiate-dependent patients receiving methadone maintenance treatment (MMT, n ¼ 30) and healthy controls (n ¼ 23) using nondrug-related stimuli. Half of the patients were scanned after/before daily methadone intake (ADM/BDM patient groups). During reward trials, patients as a whole exhibited decreased neural discrimination between rewarding and nonrewarding outcomes in the dorsal caudate. Patients also showed reduced neural discrimination in the ventral striatum with regard to aversive and nonaversive outcomes and failed to encode successful loss avoidance as a reward signal in the ventral striatum. Patients also showed decreased insula activation during the anticipation/decision phase of loss events. ADM patients exhibited increased loss signals in the midbrain/ parahippocampal gyrus, possibly related to a disinhibition of dopamine neurons. This study suggests that patients with opiate dependency on MMT exhibit abnormal brain activations to nondrug-related rewarding and loss events. Our findings add support to proposals that treatments for opiate addiction should aim to increase the reward value of nondrug-related rewarding events and highlight the importance of potential abnormalities in aversive information processing.

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Section: Discussionsupporting

confidence: 90%

Section: Introductionmentioning

confidence: 98%

Abnormal Brain Activity During a Reward and Loss Task in Opiate-Dependent Patients Receiving Methadone Maintenance Therapy

Gradin

Baldacchino

Balfour

et al. 2013

Neuropsychopharmacol

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“…Providing validity to this underlying hypothesis, our current study is the first to document that, compared with healthy control subjects and even in the absence of behavioral differences between the groups, the ACC is hypoactive as measured with BOLD-fMRI during an emotionally salient task. These findings extend previous fMRI results where ACC hypoactivations were documented in CUD as compared with controls in response to emotionally neutral cognitive tasks (9), or where performance differed on similar cognitive (5-8) or other emotionally salient tasks (27). Our current results indicate that such ACC hypoactivations cannot be fully attributed to task difficulty.…”

Section: Discussionsupporting

confidence: 89%

Anterior cingulate cortex hypoactivations to an emotionally salient task in cocaine addiction

Goldstein

Alia‐Klein²,

Tomasi³

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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167

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Anterior cingulate cortex (ACC) hypoactivations during cognitive processing characterize drug addicted individuals as compared with healthy controls. However, impaired behavioral performance or task disengagement may be crucial factors. We hypothesized that ACC hypoactivations would be documented in groups matched for performance on an emotionally salient task. Seventeen individuals with current cocaine use disorders (CUD) and 17 demographically matched healthy controls underwent functional magnetic resonance imaging during performance of a rewarded drug cue-reactivity task previously shown to engage the ACC. Despite lack of group differences in objective or subjective taskrelated performance, CUD showed more ACC hypoactivations throughout this emotionally salient task. Nevertheless, intensity of emotional salience contributed to results: (i) CUD with the largest rostroventral ACC [Brodmann Area (BA) 10, 11, implicated in default brain function] hypoactivations to the most salient task condition (drug words during the highest available monetary reward), had the least task-induced cocaine craving; (ii) CUD with the largest caudal-dorsal ACC (BA 32) hypoactivations especially to the least salient task condition (neutral words with no reward) had the most frequent current cocaine use; and (iii) responses to the most salient task condition in both these ACC major subdivisions were positively intercorrelated in the controls only. In conclusion, ACC hypoactivations in drug users cannot be attributed to task difficulty or disengagement. Nevertheless, emotional salience modulates ACC responses in proportion to drug use severity. Interventions to strengthen ACC reactivity or interconnectivity may be beneficial in enhancing top-down monitoring and emotion regulation as a strategy to reduce impulsive and compulsive behavior in addiction.blood-oxygen-level-dependent fMRI ͉ salience ͉ brain-behavior dissociation ͉ craving ͉ cocaine use I n the impaired response inhibition and salience attribution (I-RISA) model we have emphasized the role of the anterior cingulate (ACC) and orbitofrontal cortices (OFC) in core clinical symptoms of drug addiction that encompass attribution of enhanced salience to drug cues at the expense of the salience attributed to nondrug-related stimuli (1). Supporting this core I-RISA hypothesis, neuroimaging studies in drug addicted individuals demonstrate ACC and OFC hyperactivations during drug-related cue reactivity (2), including craving (3, 4) and hypoactivations during performance of neutrally valenced cognitive tasks (5-9). Because these hypoactivations in addicted individuals could reflect impaired performance (5-8) or decreased engagement (9), in the current study we set out to determine whether ACC hypoactivations in addiction can still be observed in groups matched for overt performance on an emotionally salient task. This is a crucial question because the clinical implications for such hypoactivations even in the absence of overt behavioral group differences may be pronounced. For example, t...

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“…However, we did not expect to find similar correlations between these measures of performance with the BOLD signal. Prior studies from our laboratory, using a different fMRI blocked-design task, showed lack of an association between these performance measures in the cocaine addicted but not control subjects; we attributed these results to impaired perception of inner motivation in drug addiction (Goldstein et al, 2007).…”

Section: Methodsmentioning

confidence: 65%

Role of the anterior cingulate and medial orbitofrontal cortex in processing drug cues in cocaine addiction

et al. 2007

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Our goal in the current report was to design a new fMRI task to probe the role of the anterior cingulate cortex (ACC) and orbitofrontal cortex (OFC) in processing of salient symptom-related cues during the simultaneous performance of an unrelated task in drug addicted individuals. We used a novel functional magnetic resonance imaging color-word drug Stroop task in 14 individuals with cocaine use disorders; subjects had to press for color of drug vs. matched neutral words. Although there were no accuracy or speed differences between the drug and neutral conditions in the current sample of subjects, drug words were more negatively valenced than the matched neutral words. Further, consistent with prior reports in individuals with other psychopathologies using different Stroop fMRI paradigms, our more classical color-word Stroop design revealed bilateral activations in the caudaldorsal ACC (cdACC) and hypoactivations in the rostro-ventral ACC/medial OFC (rACC/mOFC). A trend for larger rACC/mOFC hypoactivations to the drug than neutral words did not survive wholebrain corrections. Nevertheless, correlation analyses indicated that (1) the more the cdACC drugrelated activation, the more negative the valence attributed to the drug words (r=-0.86, p < 0.0001) but not neutral words; and (2) the more the rACC/mOFC hypoactivation to drug minus neutral words, the more the errors committed specifically to the drug minus neutral words (r=0.85, p < 0.0001). Taken together, results suggest that this newly developed drug Stroop fMRI task may be a sensitive biobehavioral assay of the functions recruited for the regulation of responses to salient symptomrelated stimuli in drug addicted individuals.

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Is Decreased Prefrontal Cortical Sensitivity to Monetary Reward Associated With Impaired Motivation and Self-Control in Cocaine Addiction?

Cited by 199 publications

References 41 publications

Abnormal Brain Activity During a Reward and Loss Task in Opiate-Dependent Patients Receiving Methadone Maintenance Therapy

Abnormal Brain Activity During a Reward and Loss Task in Opiate-Dependent Patients Receiving Methadone Maintenance Therapy

Anterior cingulate cortex hypoactivations to an emotionally salient task in cocaine addiction

Role of the anterior cingulate and medial orbitofrontal cortex in processing drug cues in cocaine addiction

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