Systematic review of ERP and fMRI studies investigating inhibitory control and error processing in people with substance dependence and behavioural addictions

Abstract

Background: Several current theories emphasize the role of cognitive control in addiction. The present review evaluates neural deficits in the domains of inhibitory control and error processing in individuals with substance dependence and in those showing excessive addiction-like behaviours. The combined evaluation of event-related potential (ERP) and functional magnetic resonance imaging (fMRI) findings in the present review offers unique information on neural deficits in addicted individuals.

Methods: We selected 19 ERP and 22 fMRI studies using stop-signal, go/no-go or Flanker paradigms based on a search of PubMed and Embase.

Results: The most consistent findings in addicted individuals relative to healthy controls were lower N2, error-related negativity and error positivity amplitudes as well as hypoactivation in the anterior cingulate cortex (ACC), inferior frontal gyrus and dorsolateral prefrontal cortex. These neural deficits, however, were not always associated with impaired task performance. With regard to behavioural addictions, some evidence has been found for similar neural deficits; however, studies are scarce and results are not yet conclusive. Differences among the major classes of substances of abuse were identified and involve stronger neural responses to errors in individuals with alcohol dependence versus weaker neural responses to errors in other substance-dependent populations.

Limitations: Task design and analysis techniques vary across studies, thereby reducing comparability among studies and the potential of clinical use of these measures.

Conclusion: Current addiction theories were supported by identifying consistent abnormalities in prefrontal brain function in individuals with addiction. An integrative model is proposed, suggesting that neural deficits in the dorsal ACC may constitute a hallmark neurocognitive deficit under lying addictive behaviours, such as loss of control.

Figures

Fig. 1

Summary of anterior cingulate dysfunction in individuals with addictions for inhibitory control. Circles represent hypoactivation and squares hyperactivation for inhibitory control in individuals with addictions relative to controls. Of note, 6 studies included in this review reporting group differences are not displayed in this figure, as results did not indicate group differences in the anterior cingulate cortex for inhibitory control–related brain activation. Red: opioid dependence; green: cocaine dependence; dark blue: cannabis dependence; light blue: nicotine dependence; yellow: behavioural addictions. Locations are based on reported Talairach or Montreal Neurological Institute (MNI) coordinates in studies reporting group differences included in this review. Talairach coordinates were converted to MNI using the GingerALE toolbox. Foci of activation were projected onto the midline for ease of viewing.

Fig. 2

Summary of anterior cingulate dysfunction in individuals with addictions for error processing. Circles represent hypoactivation and squares hyperactivation for error processing in individuals with addictions relative to controls. Of note, 1 study included in this review that reports group differences is not displayed in this figure as results did not indicate group differences in the anterior cingulate cortex for error-related brain activation. Red: opioid dependence; green: cocaine dependence; purple: alcohol dependence; light blue: nicotine dependence; yellow: pathological gambling. Locations are based on reported Talairach or Montreal Neurological Institute (MNI) coordinates in studies reporting group differences included in this review. Talairach coordinates were converted to MNI using the GingerALE toolbox. Foci of activation were projected onto the midline for ease of viewing.

Fig. 3

Summary and integrative model of neural deficits in error processing and inhibitory control in individuals with addictive behaviours. The event-related potential components and brain regions listed in the boxes are those showing the most consistent neural deficits in individuals with addictions in error processing and inhibitory control. As the most consistent findings are related to dorsal anterior cingulate cortex (dACC) dysfunction, we suggest that problems with conflict monitoring, a critical function of the dACC, involved in both inhibitory control and error processing, may trigger the loss of control in individuals with addictions. The grey arrow indicates that the function of this highly interrelated system is decreased in individuals with addictions compared with healthy controls. It further illustrates the negative impact of this dysfunctional system over addiction-related behaviours. The arrows in the model symbolize the relationships between error-processing and inhibitory control with conflict monitoring. The dotted arrow represents the modulatory effect of error-related dACC activation on connected brain regions. DLPFC = dorsolateral prefrontal cortex; ERN = error-related negativity; IFG = inferior frontal gyrus; PG = parietal gyrus.