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When your error becomes my error: anterior insula activation in response to observed errors is modulated by agency.

ABSTRACT: Research on error observation has focused predominantly on situations in which individuals are passive observers of errors. In daily life, however, we are often jointly responsible for the mistakes of others. In the current study, we examined how information on agency is integrated in the error observation network. It was found that activation in the anterior insula but not in the posterior medial frontal cortex or lateral prefrontal cortex differentiates between observed errors for which we are partly responsible or not. Interestingly, the activation pattern of the AI was mirrored by feelings of guilt and shame. These results suggest that the anterior insula is crucially involved in evaluating the consequences of our actions for other persons. Consequently, this region may be thought of as critical in guiding social behavior.

SUBMITTER: Cracco E

PROVIDER: S-EPMC4769623 | biostudies-literature | 2016 Mar

REPOSITORIES: biostudies-literature

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When your error becomes my error: anterior insula activation in response to observed errors is modulated by agency.

Cracco Emiel E Desmet Charlotte C Brass Marcel M

Social cognitive and affective neuroscience 20150923 3

Research on error observation has focused predominantly on situations in which individuals are passive observers of errors. In daily life, however, we are often jointly responsible for the mistakes of others. In the current study, we examined how information on agency is integrated in the error observation network. It was found that activation in the anterior insula but not in the posterior medial frontal cortex or lateral prefrontal cortex differentiates between observed errors for which we are ...[more]

PMID: 26400856

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Project description:Introduction:Smoking is associated with significant morbidity and mortality. Understanding the neurobiology of the rewarding effects of nicotine promises to aid treatment development for nicotine dependence. Through its actions on mesolimbic dopaminergic systems, nicotine engenders enhanced responses to drug-related cues signaling rewards, a mechanism hypothesized to underlie the development and maintenance of nicotine addiction. Methods:We evaluated the effects of acute nicotine on neural responses to anticipatory cues signaling (nondrug) monetary reward or loss among 11 nonsmokers who had no prior history of tobacco smoking. In a double-blind, crossover design, participants completed study procedures while wearing nicotine or placebo patches at least 1 week apart. In each drug condition, participants underwent functional magnetic resonance imaging while performing the monetary incentive delay task and performed a probabilistic monetary reward task, probing reward responsiveness as measured by response bias toward a more frequently rewarded stimulus. Results:Nicotine administration was associated with enhanced activation, compared with placebo, of right fronto-anterior insular cortex and striatal regions in response to cues predicting possible rewards or losses and to dorsal anterior cingulate for rewards. Response bias toward rewarded stimuli correlated positively with insular activation to anticipatory cues. Conclusion:Nicotinic enhancement of monetary reward-related brain activation in the insula and striatum in nonsmokers dissociated acute effects of nicotine from effects on reward processing due to chronic smoking. Reward responsiveness predicted a greater nicotinic effect on insular activation to salient stimuli. Implications:Previous research demonstrates that nicotine enhances anticipatory responses to rewards in regions targeted by midbrain dopaminergic systems. The current study provides evidence that nicotine also enhances responses to rewards and losses in the anterior insula. A previous study found enhanced insular activation to rewards and losses in smokers and ex-smokers, a finding that could be due to nicotine sensitization or factors related to current or past smoking. Our finding of enhanced anterior insula response after acute administration of nicotine in nonsmokers provides support for nicotine-induced sensitization of insular response to rewards and losses.

Project description:Attenuated activity in performance-monitoring brain regions following erroneous actions may contribute to the repetition of maladaptive behaviors such as continued drug use. Externalizing is a broad personality construct characterized by deficient impulse control, vulnerability to addiction and reduced neurobiological indices of error processing. The insula and dorsal anterior cingulate cortex (dACC) are regions critically linked with error processing as well as the perpetuation of cigarette smoking. As such, we examined the interrelations between externalizing tendencies, erroneous task performance, and error-related insula and dACC activity in overnight-deprived smokers (n?=?24) and non-smokers (n?=?20). Participants completed a self-report measure assessing externalizing tendencies (Externalizing Spectrum Inventory) and a speeded Flanker task during functional magnetic resonance imaging scanning. We observed that higher externalizing tendencies correlated with the occurrence of more performance errors among smokers but not non-smokers. Suggesting a neurobiological contribution to such suboptimal performance among smokers, higher externalizing also predicted less recruitment of the right insula and dACC following error commission. Critically, this error-related activity fully mediated the relationship between externalizing traits and error rates. That is, higher externalizing scores predicted less error-related right insula and dACC activity and, in turn, less error-related activity predicted more errors. Relating such regional activity with a clinically relevant construct, less error-related right insula and dACC responses correlated with higher tobacco craving during abstinence. Given that inadequate error-related neuronal responses may contribute to continued drug use despite negative consequences, these results suggest that externalizing tendencies and/or compromised error processing among subsets of smokers may be relevant factors for smoking cessation success.

Dataset Information

When your error becomes my error: anterior insula activation in response to observed errors is modulated by agency.

Publications

When your error becomes my error: anterior insula activation in response to observed errors is modulated by agency.

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