Nentwig Todd B, Obray J Daniel, Kruyer Anna, Wilkes Erik T, Vaughan Dylan T, Scofield Michael D, Chandler L Judson
Department of Neuroscience, Medical University of South Carolina, Charleston SC 29425, United States.
Current affiliation: Department of Neuroscience, University of Cincinnati, Cincinnati, OH, USA.
bioRxiv. 2024 Jun 11:2024.06.11.598470. doi: 10.1101/2024.06.11.598470.
Dependence is a hallmark of alcohol use disorder characterized by excessive alcohol intake and withdrawal symptoms. The central nucleus of the amygdala (CeA) is a key brain structure underlying the synaptic and behavioral consequences of ethanol dependence. While accumulating evidence suggests that astrocytes regulate synaptic transmission and behavior, there is a limited understanding of the role astrocytes play in ethanol dependence. The present study used a combination of viral labeling, super resolution confocal microscopy, 3D image analysis, and slice electrophysiology to determine the effects of chronic intermittent ethanol (CIE) exposure on astrocyte plasticity in the CeA. During withdrawal from CIE exposure, we observed increased GABA transmission, an upregulation in astrocytic GAT3 levels, and an increased proximity of astrocyte processes near CeA synapses. Furthermore, GAT3 levels and synaptic proximity were positively associated with voluntary ethanol drinking in dependent rats. Slice electrophysiology confirmed that the upregulation in astrocytic GAT3 levels was functional, as CIE exposure unmasked a GAT3-sensitive tonic GABA current in the CeA. A causal role for astrocytic GAT3 in ethanol dependence was assessed using viral-mediated GAT3 overexpression and knockdown approaches. However, GAT3 knockdown or overexpression had no effect on somatic withdrawal symptoms, dependence-escalated ethanol intake, aversion-resistant drinking, or post-dependent ethanol drinking in male or female rats. Moreover, intra-CeA pharmacological inhibition of GAT3 also did not alter dependent ethanol drinking. Together, these findings indicate that ethanol dependence induces GABAergic dysregulation and astrocyte plasticity in the CeA. However, astrocytic GAT3 does not appear necessary for the drinking related phenotypes associated with dependence.
依赖是酒精使用障碍的一个标志,其特征为酒精摄入过量和戒断症状。杏仁核中央核(CeA)是乙醇依赖的突触和行为后果背后的关键脑结构。虽然越来越多的证据表明星形胶质细胞调节突触传递和行为,但对于星形胶质细胞在乙醇依赖中所起的作用了解有限。本研究结合病毒标记、超分辨率共聚焦显微镜、3D图像分析和脑片电生理学,以确定慢性间歇性乙醇(CIE)暴露对CeA中星形胶质细胞可塑性的影响。在从CIE暴露中戒断期间,我们观察到GABA传递增加、星形胶质细胞GAT3水平上调以及CeA突触附近星形胶质细胞突起的接近度增加。此外,GAT3水平和突触接近度与依赖大鼠的自愿乙醇饮用量呈正相关。脑片电生理学证实,星形胶质细胞GAT3水平的上调是有功能的,因为CIE暴露揭示了CeA中一种对GAT3敏感的紧张性GABA电流。使用病毒介导的GAT3过表达和敲低方法评估了星形胶质细胞GAT3在乙醇依赖中的因果作用。然而,GAT3敲低或过表达对雄性或雌性大鼠的躯体戒断症状、依赖升级的乙醇摄入量、抗厌恶饮用量或依赖后乙醇饮用量均无影响。此外,CeA内对GAT3的药理学抑制也未改变依赖的乙醇饮用量。总之,这些发现表明乙醇依赖会诱导CeA中的GABA能失调和星形胶质细胞可塑性。然而,星形胶质细胞GAT3对于与依赖相关的饮酒相关表型似乎并非必需。