Brain correlates and functional connectivity linking stress, autonomic dysregulation, and alcohol motivation

IF 4.3 2区 医学 Q1 NEUROSCIENCES Neurobiology of Stress Pub Date : 2024-05-21 DOI:10.1016/j.ynstr.2024.100645
Dongju Seo , Jorge S. Martins , Rajita Sinha
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Abstract

High stress is a key risk factor for alcohol use disorder (AUD) and often accompanied by physiological dysregulation including autonomic nervous system (ANS) disruptions. However, neural mechanisms underlying drinking behaviors associated with stress and ANS disruptions remain unclear. The current study aims to understand neural correlates of stress, ANS disruptions, and subsequent alcohol intake in social drinkers with risky drinking. Using functional magnetic resonance imaging (fMRI), we investigated brain and heart rate (HR) autonomic responses during brief exposure to stress, alcohol, and neutral cues utilizing a well-validated, individualized imagery paradigm in 48 social drinkers of which 26 reported high-risk drinking (HD) while 22 reported low-risk drinking (LD) patterns. Results indicated that HD individuals showed stress and ANS disruptions with increased basal HR, stress-induced craving, and decreased brain response to stress exposure in frontal-striatal regions including the ventromedial prefrontal cortex (VmPFC), anterior cingulate cortex, striatum, insula, and temporal gyrus. Furthermore, whole-brain correlation analysis indicated that greater basal HR was associated with hypoactive VmPFC, but hyperactive medulla oblongata (MOb) responses during stress, with an inverse association between activity in the VmPFC and Mob (whole-brain corrected (WBC), p < 0.05). Functional connectivity with the MOb as a seed to the whole brain indicated that HD versus LD had decreased functional connectivity between the VmPFC and MOb during stress (WBC, p < 0.05). In addition, those with more compromised functional connectivity between the VmPFC and MOb during stress consumed greater amount of alcohol beverage during an experimental alcohol taste test conducted on a separate day, as well as in their self-reported weekly alcohol intake. Together, these results indicate that stress-related, dysfunctional VmPFC control over brain regions of autonomic arousal contributes to greater alcohol motivation and may be a significant risk factor for hazardous alcohol use in non-dependent social drinkers. Findings also suggest that restoring VmPFC integrity in modulating autonomic arousal during stress may be critical for preventing the development of AUD.

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与压力、自律神经失调和酗酒动机有关的大脑相关性和功能连通性
高度压力是导致酒精使用障碍(AUD)的一个关键风险因素,通常伴随着生理失调,包括自律神经系统(ANS)紊乱。然而,与压力和自律神经系统紊乱相关的饮酒行为的神经机制仍不清楚。本研究旨在了解有饮酒风险的社交饮酒者的压力、自律神经系统紊乱和随后酒精摄入的神经相关性。我们采用功能磁共振成像(fMRI)技术,利用一种经过充分验证的个性化想象范式,对 48 名社交饮酒者(其中 26 人报告了高风险饮酒(HD),22 人报告了低风险饮酒(LD)模式)在短暂暴露于压力、酒精和中性线索时的大脑和心率(HR)自律神经反应进行了调查。结果表明,高危饮酒者表现出压力和自律神经系统紊乱,基础心率升高,压力诱发渴求,大脑对压力暴露的额叶-前额叶区域反应减弱,包括腹外侧前额叶皮层(VmPFC)、前扣带回皮层、纹状体、岛叶和颞回。此外,全脑相关性分析表明,在应激时,基础心率越大,VmPFC的反应越不活跃,而延髓(MOb)的反应却越活跃,VmPFC的活动与Mob之间存在反向关联(全脑校正(WBC),p <0.05)。以MOb作为全脑种子的功能连通性表明,在应激期间,HD与LD相比,VmPFC与MOb之间的功能连通性降低(WBC,p <0.05)。此外,应激时VmPFC和MOb之间的功能连通性受损更严重的人在单独一天进行的实验性酒精味觉测试中摄入了更多的酒精饮料,他们自我报告的每周酒精摄入量也更高。这些结果表明,与压力相关的、对自律神经唤醒脑区功能失调的VmPFC控制导致了更大的饮酒动机,并可能成为非依赖性社交饮酒者危险饮酒的一个重要风险因素。研究结果还表明,恢复 VmPFC 在应激时调节自律神经唤醒的完整性可能对预防 AUD 的发生至关重要。
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来源期刊
Neurobiology of Stress
Neurobiology of Stress Biochemistry, Genetics and Molecular Biology-Biochemistry
CiteScore
9.40
自引率
4.00%
发文量
74
审稿时长
48 days
期刊介绍: Neurobiology of Stress is a multidisciplinary journal for the publication of original research and review articles on basic, translational and clinical research into stress and related disorders. It will focus on the impact of stress on the brain from cellular to behavioral functions and stress-related neuropsychiatric disorders (such as depression, trauma and anxiety). The translation of basic research findings into real-world applications will be a key aim of the journal. Basic, translational and clinical research on the following topics as they relate to stress will be covered: Molecular substrates and cell signaling, Genetics and epigenetics, Stress circuitry, Structural and physiological plasticity, Developmental Aspects, Laboratory models of stress, Neuroinflammation and pathology, Memory and Cognition, Motivational Processes, Fear and Anxiety, Stress-related neuropsychiatric disorders (including depression, PTSD, substance abuse), Neuropsychopharmacology.
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