Synchrony of Corticostriatal-Midbrain Activation Enables Normal Inhibitory Control and Conflict Processing in Recovering Alcoholic Men

Abstract

Background Alcohol dependence is associated with inhibitory control deficits, possibly related to abnormalities in frontoparietal cortical and midbrain function and connectivity. Methods We examined functional connectivity and microstructural fiber integrity between frontoparietal and midbrain structures using a Stroop Match-to-Sample task with functional MRI and diffusion tensor imaging in 18 alcoholics and 17 controls. Manipulation of color cues and response repetition sequences modulated cognitive demands during Stroop conflict. Results Despite similar lateral frontoparietal activity and functional connectivity in alcoholics and controls when processing conflict, controls deactivated the posterior cingulate cortex (PCC), whereas alcoholics did not. Posterior cingulum fiber integrity predicted the degree of PCC deactivation in controls but not alcoholics. Also, PCC activity was modulated by executive control demands: activated during response switching and deactivated during response repetition. Alcoholics showed the opposite pattern: activation during repetition and deactivation during switching. Here, in alcoholics, greater deviations from the normal PCC activity correlated with higher amounts of lifetime alcohol consumption. A functional dissociation of brain network connectivity between the groups further showed that controls exhibited greater corticocortical connectivity between middle cingulate, posterior cingulate, and medial prefrontal cortices than alcoholics. By contrast, alcoholics exhibited greater midbrain-orbitofrontal cortical network connectivity than controls. Degree of microstructural fiber integrity predicted robustness of functional connectivity. Conclusion Thus, even subtle compromise of microstructural connectivity in alcoholism can influence modulation of functional connectivity and underlie alcohol-related cognitive impairment.

Resting-state regional homogeneity as a biological marker for patients with Internet gaming disorder: A comparison with patients with alcohol use disorder and healthy controls

“…As the PCC is part of DMN, which is synchronized with low-frequency oscillations in some brain regions during the resting-state, it is important for attention and self-monitoring as it involves cognitive functions associated with the coupling of executive control and the ability to disengage from the DMN (Fox and Raichle, 2007). Several studies reported functional abnormality IGD or AUD in the PCC, including increased ReHo (Liu et al, 2010) and failing to exhibit task-induced deactivation (Schulte et al, 2012). Chanraud et al (2011Chanraud et al ( , 2012 supported that difference in brain activity and in the functional synchrony between brain regions may be compensatory and bestow resources for task processing in alcoholism during the resting-state.…”

Imaging the Addicted Brain

“…During a task engaging executive functions (ie, Stroop task), Schulte, M€ uller-Oehring, Sullivan, and Pfefferbaum (2012) observed that connectivity of the middle cingulate cortex (MCC) was modified in alcoholics compared to controls. For this experiment, the Stroop effect was defined as the difference in RT between incongruent and congruent stimuli.…”

Human Imaging Studies of Brain Circuitry Disrupted by Alcoholism

“…These findings show a double dissociation of anterior and posterior cortical systems engaging in different types of control for perceptually driven and action-driven conflict resolution and showed that appropriate engagement of topdown control was disrupted in the healthy elderly (Schulte et al, 2009). This paradigm was also successful in identifying disruption of top-down regulation of inhibition used by controls and evidenced as medial prefrontal-posterior cingulate activation synchrony in contrast with recovering alcoholics who invoked a bottom-up strategy marked by greater midbrain-orbitofrontal connectivity than controls (Schulte et al, 2012).…”

“…A common finding in task-activated paradigms tapping response inhibition has been weaker connectivity in frontostriatal networks in alcoholics compared with controls (Courtney, Ghahremani, & Ray, 2013). In some instances, weaker connectivity was associated with a composite measure of alcoholism severity (Courtney et al, 2013), greater amounts of alcohol consumed over a lifetime (Schulte, Müller-Oehring, Sullivan, & Pfefferbaum, 2012), and length of sobriety (Dresler et al, 2011).…”

“…An objective of merging structural and functional data is to identify white matter pathways that connect functional nodes or, when anatomically remote from each other, fibers that are included in parts of the known circuitry connecting brain regions (e.g., Greicius, Supekar, Menon, & Dougherty, 2009). Currently, the only such study in alcoholism used a task-activated fMRI paradigm involving a Stroop Match-to-Sample task to assess inhibitory control and conflict processing (Schulte et al, 2012). Despite similar levels of performance, the alcoholics and controls invoked different constellations of regions to conduct the different component processes demanded by the complex task.…”