Albert J Arias1,2, Liangsuo Ma1,2, James M Bjork1,2, Christopher J Hammond3, Yi Zhou2, Andrew Snyder1,2, Frederick Gerard Moeller1,2,4,5. 1. Institute for Drug and Alcohol Studies, Virginia Commonwealth University (VCU), Richmond, VA, USA. 2. Department of Psychiatry, Virginia Commonwealth University (VCU), Richmond, VA, USA. 3. Department of Psychiatry, Johns Hopkins University, Baltimore, MD, USA. 4. Department of Pharmacology and Toxicology, Virginia Commonwealth University (VCU), Richmond, VA, USA. 5. Department of Neurology, Virginia Commonwealth University (VCU), Richmond, VA, USA.
Abstract
BACKGROUND: Abnormalities of reward sensitivity and impulsivity are known to be correlated with each other and alcohol use disorder (AUD) risk, but the underlying aberrant neural circuitry involved is not clearly defined. We sought to extend the current knowledge of AUD pathophysiology by studying incentive processing in persons with AUD using functional neuroimaging data. METHODS: We utilized functional MRI data from the Human Connectome Project Database obtained during performance of a number-guessing incentive-processing task with win, loss, and neutral feedback conditions in 78 participants with either DSM-IV alcohol abuse or dependence (combined as the AUD group) and 78 age- and sex-matched control (CON) participants. Within a network consisting of anterior cingulate cortex (ACC), dorsolateral prefrontal cortex (DLPFC), insula, ventral striatum, and dorsal striatum (DS) in the right hemisphere, we performed dynamic causal modeling analysis to test group-level differences (AUD vs. CON) in effective directional connectivity (EC) as modulated by "win" and "loss" conditions. We used linear regression analyses to characterize the relations between each EC outcome and measures of cumulative alcohol exposure and impulsivity. RESULTS: During wins, AUD participants had lower ECs from ACC to the other four nodes, greater ECs from insula to the other four nodes, greater ECs from DLPFC to the other four nodes, and greater DS to DS self-connection EC than CON participants. In the total sample, EC from the insula to the DLPFC (insula → DLPFC) during wins was positively correlated with both impulsivity (as measured by the delay-discounting task) and cumulative alcohol exposure. The DS to DS self-connection EC during wins was positively correlated with impulsivity. Many of the altered ECs from the ACC and insula to other nodes were correlated with cumulative alcohol exposure. CONCLUSIONS: Individuals with AUD have disrupted EC in both instrumentally driven and automatized corticostriatal reward circuits during non-alcohol reward feedback. These results point to disrupted corticostriatal EC in both "top-down" and "bottom-up" pathways among individuals with AUD.
BACKGROUND: Abnormalities of reward sensitivity and impulsivity are known to be correlated with each other and alcohol use disorder (AUD) risk, but the underlying aberrant neural circuitry involved is not clearly defined. We sought to extend the current knowledge of AUD pathophysiology by studying incentive processing in persons with AUD using functional neuroimaging data. METHODS: We utilized functional MRI data from the Human Connectome Project Database obtained during performance of a number-guessing incentive-processing task with win, loss, and neutral feedback conditions in 78 participants with either DSM-IV alcohol abuse or dependence (combined as the AUD group) and 78 age- and sex-matched control (CON) participants. Within a network consisting of anterior cingulate cortex (ACC), dorsolateral prefrontal cortex (DLPFC), insula, ventral striatum, and dorsal striatum (DS) in the right hemisphere, we performed dynamic causal modeling analysis to test group-level differences (AUD vs. CON) in effective directional connectivity (EC) as modulated by "win" and "loss" conditions. We used linear regression analyses to characterize the relations between each EC outcome and measures of cumulative alcohol exposure and impulsivity. RESULTS: During wins, AUD participants had lower ECs from ACC to the other four nodes, greater ECs from insula to the other four nodes, greater ECs from DLPFC to the other four nodes, and greater DS to DS self-connection EC than CON participants. In the total sample, EC from the insula to the DLPFC (insula → DLPFC) during wins was positively correlated with both impulsivity (as measured by the delay-discounting task) and cumulative alcohol exposure. The DS to DS self-connection EC during wins was positively correlated with impulsivity. Many of the altered ECs from the ACC and insula to other nodes were correlated with cumulative alcohol exposure. CONCLUSIONS: Individuals with AUD have disrupted EC in both instrumentally driven and automatized corticostriatal reward circuits during non-alcohol reward feedback. These results point to disrupted corticostriatal EC in both "top-down" and "bottom-up" pathways among individuals with AUD.
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