Alcohol effects on globus pallidus connectivity: Role of impulsivity and binge drinking.
- Authors
- Fede, Samantha J; Abrahao, Karina P; Cortes, Carlos R; Grodin, Erica N; Schwandt, Melanie L; George, David T; Diazgranados, Nancy; Ramchandani, Vijay A; Lovinger, David M; Momenan, Reza
- Year
- 2020
- Journal
- PloS one
- PMID
- 32214339
- DOI
- 10.1371/journal.pone.0224906
- PMCID
- PMC7098584
Despite the harm caused by binge drinking, the neural mechanisms leading to risky and disinhibited intoxication-related behaviors are not well understood. Evidence suggests that the globus pallidus externus (GPe), a substructure within the basal ganglia, participates in inhibitory control processes, as examined in stop-signaling tasks. In fact, studies in rodents have revealed that alcohol can change GPe activity by decreasing neuronal firing rates, suggesting that the GPe may have a central role in explaining impulsive behaviors and failures of inhibition that occur during binge drinking. In this study, twenty-five healthy volunteers underwent intravenous alcohol infusion to achieve a blood alcohol level of 0.08 g/dl, which is equivalent to a binge drinking episode. A resting state functional magnetic resonance imaging scan was collected prior to the infusion and at binge-level exposure. Functional connectivity analysis was used to investigate the association between alcohol-induced changes in GPe connectivity, drinking behaviors, and impulsivity traits. We found that individuals with greater number of drinks or heavy drinking days in the recent past had greater alcohol-induced deficits in GPe connectivity, particularly to the striatum. Our data also indicated an association between impulsivity and alcohol-induced deficits in GPe-frontal/precentral connectivity. Moreover, alcohol induced changes in GPe-amygdala circuitry suggested greater vulnerabilities to stress-related drinking in some individuals. Taken together, these findings suggest that alcohol may interact with impulsive personality traits and drinking patterns to drive alterations in GPe circuitry associated with behavioral inhibition, possibly indicating a neural mechanism by which binge drinking could lead to impulsive behaviors.
Timeline of intravenous alcohol infusion study.The timeline depiction of the two-session intravenous alcohol infusion study; sessions were separated at least three days from each other. The session 2 timeline indicates timepoints of resting state and BAC measurement alongside IV infusion; the first resting state scan occurred before the IV infusion at blood alcohol level of 0.0 g/dl and the second one was collected when the blood alcohol level reached the binge levels (0.08 g/dl).
LLM interpretation
This figure consists of two line graphs depicting the timeline of an intravenous alcohol infusion study across two sessions separated by a 3-day interval. Both graphs plot Breath Alcohol Concentration (mg%) against Experimental Time (min), showing a baseline of 0 mg% followed by a linear increase during the "1st Phase IV Infusion" and a plateau at 80 mg% during the "2nd Phase IV Clamp." The second graph specifically labels the timing of imaging acquisitions, including a pre-infusion Rs-fMRI scan at 0 mg% and a post-infusion Rs-fMRI scan during the 80 mg% plateau.
Association between past 30 day drinking and alcohol induced changes in GPe connectivity.(As measured by the Alcohol Timeline Followback). Scatter plots correspond to individual connectivity at baseline in teal (estimated BAC: 0.0) and after infusion in salmon (BAC: 0.08); linear fit lines are also displayed for each timepoint. Connectivity coefficient is the r (correlation value) between the signal in the GPe seed and the coordinate indicated. Brain images represent whole effects of drinks in past 30 days on alcohol induced change in functional connectivity (post-infusion connectivity > pre-infusion connectivity). Warm colors indicate intoxication related increases in connectivity; cool colors indicated intoxication related decreases in connectivity. Images shown at p < 0.005. Clusters with significant interaction effects are reported in Fig 3. Reported clusters of connectivity with GPe area correspond to the following regions: A.i.—Superior Frontal Gyrus extending into dorsal anterior cingulate; A.ii.—Hippocampus/amygdala; B.i.—Heschl’s Gyrus extending into the insula/putamen; B.ii.—Heschl’s Gyrus extending into the insula/putamen.
LLM interpretation
This figure consists of four scatter plots and two brain imaging maps showing the association between alcohol consumption in the past 30 days and GPe functional connectivity. The scatter plots compare connectivity coefficients at baseline (BAC: 0.00, teal) and after alcohol infusion (BAC: 0.08, salmon) across different brain regions, with linear fit lines indicating divergent trends between the two conditions. The brain images use a heat map (warm for increases, cool for decreases) to visualize the whole effects of past drinking on alcohol-induced connectivity changes at $p < 0.005$.
Effect of alcohol induced changes in GPe connectivity on the association between drinking and impulsivity.(As measured by the Alcohol Timeline Followback and UPPS-P, respectively). Cluster of Drinking Effect column: Brain images represent whole brain effects of drinks in past 30 days on alcohol induced change in functional connectivity (post-infusion connectivity > post-infusion connectivity). Warm colors indicate intoxication related increases in connectivity. Images shown at p < 0.005. Plots of Connectivity are scatter plots corresponding to individual connectivity at baseline in teal (estimated BAC: 0.0) and after infusion in salmon (BAC: 0.08); linear fit lines are also displayed for each timepoint. The y-axis for both plots is the same; the x-axis reflects the number of drinks in the last 30 days (center plot) and the number of drinks in the last 30 days multiplied by impulsivity score on the UPPS Negative Urgency scale (right plot). Abbreviations as follows: L. GPe- Left Globus Pallidus externus; Hipp./Amyg- Hippocampus/Amygdala cluster.
LLM interpretation
This figure consists of a brain map and two scatter plots analyzing the connectivity between the left Globus Pallidus externus (L. GPe) and the Hippocampus/Amygdala. The brain image highlights regions of intoxication-related connectivity changes, while the scatter plots show connectivity coefficients at baseline (BAC: 0.00, teal) and after infusion (BAC: 0.08, salmon). The center plot shows a negative linear trend between connectivity and drinks in the past 30 days for the BAC 0.08 group, and the right plot shows a negative trend for the interaction of drinking and impulsivity (UPPS Neg Urgency) for the same group.
Association between heavy drinking days and alcohol induced changes in GPe connectivity.(As measured by the Alcohol Timeline Followback). Scatter plots correspond to individual connectivity at baseline in teal (estimated BAC: 0.0) and after infusion in salmon (BAC: 0.08); linear fit lines are also displayed for each timepoint. Connectivity coefficient is the r (correlation value) between the signal in the right GPe seed and the coordinate indicated. Brain images represent whole effects of drinks in past 30 days on alcohol induced change in functional connectivity (post-infusion connectivity > pre-infusion connectivity). Warm colors indicate intoxication related increases in connectivity; cool colors indicated intoxication related decreases in connectivity. Images shown at p < 0.005. Heavy Drinking Days as measured by the Alcohol Timeline Followback in the last 90 days. Abbreviations: R.GPe- Right Globus Pallidus Externus.
LLM interpretation
This figure consists of a brain map and a scatter plot showing the association between heavy drinking days and functional connectivity between the right Globus Pallidus Externus (R.GPe) and the insula. The brain image uses warm colors to indicate intoxication-related increases in connectivity and cool colors for decreases (p < 0.005). The scatter plot displays connectivity coefficients across heavy drinking days for two conditions: baseline (BAC: 0.00, teal) and post-infusion (BAC: 0.08, salmon), with a downward linear trend visible for the post-infusion group.
Association between impulsivity measures and alcohol induced changes in GPe connectivity.Scatter plots correspond to individual connectivity at baseline in teal (estimated BAC: 0.0) and after infusion in salmon (BAC: 0.08); linear fit lines are also displayed for each timepoint. Connectivity coefficient is the r (correlation value) between the signal in the GPe seed and the coordinate indicated. Brain images represent whole brain effects of drinks in past 30 days on alcohol induced change in functional connectivity (post-infusion connectivity > pre-infusion connectivity). Warm colors indicate intoxication related increases in connectivity. Images shown at p < 0.005. (left) Changes in connectivity plotted by total scores on the BIS (Barratt Impulsiveness Scale). (right) Changes in connectivity plotted scores on the UPPS-P negative urgency subscale. Reported clusters of connectivity with GPe area correspond to the following regions: (left) Precentral gyrus / SMA (supplementary motor area). Abbreviations: GPe- Globus Pallidus Externus; L.-Left; R.-Right.
LLM interpretation
This figure consists of two brain maps and two corresponding scatter plots analyzing the association between impulsivity and alcohol-induced changes in GPe connectivity. The brain images highlight regions of increased connectivity (warm colors) following alcohol infusion (BAC 0.08) compared to baseline (BAC 0.00) for the right and left GPe seeds. The scatter plots show connectivity coefficients plotted against BIS Total scores (left) and UPPS-P Negative Urgency scores (right), with linear fit lines indicating that alcohol infusion (salmon) generally increases connectivity relative to baseline (teal) as impulsivity scores increase.
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