Department of Psychiatry, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA, USA; Penn PROMOTES Research on Sex and Gender in Health, University of Pennsylvania, Philadelphia, PA, USA.
Department of Psychiatry, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA, USA.
Psychoneuroendocrinology. 2020 Sep;119:104710. doi: 10.1016/j.psyneuen.2020.104710. Epub 2020 May 19.
Many women with no history of cognitive difficulties experience executive dysfunction during menopause. Significant adversity during childhood negatively impacts executive function into adulthood and may be an indicator of women at risk of a mid-life cognitive decline. Previous studies have indicated that alterations in functional network connectivity underlie these negative effects of childhood adversity. There is growing evidence that functional brain networks are not static during executive tasks; instead, such networks reconfigure over time. Optimal dynamics are necessary for efficient executive function; while too little reconfiguration is insufficient for peak performance, too much reconfiguration (supra-optimal reconfiguration) is also maladaptive and associated with poorer performance. Here we examined the impact of adverse childhood experiences (ACEs) on network flexibility, a measure of dynamic reconfiguration, during a letter n-back task within three networks that support executive function: frontoparietal, salience, and default mode networks. Several animal and human subject studies have suggested that childhood adversity exerts lasting effects on executive function via serotonergic mechanisms. Tryptophan depletion (TD) was used to examine whether serotonin function drives ACE effects on network flexibility. We hypothesized that ACE would be associated with higher flexibility (supra-optimal flexibility) and that TD would further increase this measure. Forty women underwent functional imaging at two time points in this double-blind, placebo controlled, crossover study. Participants also completed the Penn Conditional Exclusion Test, a task assessing abstraction and mental flexibility. The effects of ACE and TD were evaluated using generalized estimating equations. ACE was associated with higher flexibility across networks (frontoparietal β = 0.00748, D = 2.79, p = 0.005; salience β = 0.00679, D = 3.02, p = 0.003; and default mode β = 0.00910, D = 3.53, p = 0.0004). While there was no interaction between ACE and TD, active TD increased network flexibility in both ACE groups in comparison to sham depletion (frontoparietal β = 0.00489, D = 2.15, p = 0.03; salience β = 0.00393, D = 1.91, p = 0.06; default mode β = 0.00334, D = 1.73, p = 0.08). These results suggest that childhood adversity has lasting impacts on dynamic reconfiguration of functional brain networks supporting executive function and that decreasing serotonin levels may exacerbate these effects.
许多没有认知障碍史的女性在更年期会经历执行功能障碍。童年时的重大逆境会对成年后的执行功能产生负面影响,可能是女性处于中年认知衰退风险的指标。先前的研究表明,童年逆境的负面影响是基于功能网络连接的改变。越来越多的证据表明,在执行任务期间,功能性大脑网络并不是静态的;相反,这些网络会随着时间的推移重新配置。有效的执行功能需要最佳的动态;而配置不足则不足以达到最佳表现,配置过多(超优配置)也不适应,表现也会较差。在这里,我们研究了在三个支持执行功能的网络(额顶网络、突显网络和默认模式网络)内进行字母 n 回任务时,童年逆境经历(ACE)对网络灵活性(动态重新配置的度量)的影响。一些动物和人类研究表明,童年逆境通过 5-羟色胺能机制对执行功能产生持久影响。色氨酸耗竭(TD)用于检查 5-羟色胺功能是否会驱动 ACE 对网络灵活性的影响。我们假设 ACE 将与更高的灵活性(超优灵活性)相关,而 TD 将进一步增加该度量。在这项双盲、安慰剂对照、交叉研究中,40 名女性在两个时间点接受了功能成像。参与者还完成了宾夕法尼亚条件排除测试,这是一项评估抽象和心理灵活性的任务。使用广义估计方程评估 ACE 和 TD 的影响。ACE 与网络之间的灵活性呈正相关(额顶网络β=0.00748,D=2.79,p=0.005;突显网络β=0.00679,D=3.02,p=0.003;默认模式β=0.00910,D=3.53,p=0.0004)。尽管 ACE 和 TD 之间没有相互作用,但与假耗竭相比,活性 TD 增加了 ACE 组中两个网络的网络灵活性(额顶网络β=0.00489,D=2.15,p=0.03;突显网络β=0.00393,D=1.91,p=0.06;默认模式β=0.00334,D=1.73,p=0.08)。这些结果表明,童年逆境对支持执行功能的功能性大脑网络的动态重新配置具有持久影响,而降低 5-羟色胺水平可能会加剧这些影响。