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Decreased Alertness Reconfigures Cognitive Control Networks
Journal of Neuroscience ( IF 5.3 ) Pub Date : 2020-09-09 , DOI: 10.1523/jneurosci.0343-20.2020
Andrés Canales-Johnson , Lola Beerendonk , Salome Blain , Shin Kitaoka , Alejandro Ezquerro-Nassar , Stijn Nuiten , Johannes Fahrenfort , Simon van Gaal , Tristan A. Bekinschtein

Humans' remarkable capacity to flexibly adapt their behavior based on rapid situational changes is termed cognitive control. Intuitively, cognitive control is thought to be affected by the state of alertness; for example, when drowsy, we feel less capable of adequately implementing effortful cognitive tasks. Although scientific investigations have focused on the effects of sleep deprivation and circadian time, little is known about how natural daily fluctuations in alertness in the regular awake state affect cognitive control. Here we combined a conflict task in the auditory domain with EEG neurodynamics to test how neural and behavioral markers of conflict processing are affected by fluctuations in alertness. Using a novel computational method, we segregated alert and drowsy trials from two testing sessions and observed that, although participants (both sexes) were generally sluggish, the typical conflict effect reflected in slower responses to conflicting information compared with nonconflicting information, as well as the moderating effect of previous conflict (conflict adaptation), were still intact. However, the typical neural markers of cognitive control—local midfrontal theta-band power changes—that participants show during full alertness were no longer noticeable when alertness decreased. Instead, when drowsy, we found an increase in long-range information sharing (connectivity) between brain regions in the same frequency band. These results show the resilience of the human cognitive control system when affected by internal fluctuations of alertness and suggest that there are neural compensatory mechanisms at play in response to physiological pressure during diminished alertness.

SIGNIFICANCE STATEMENT The normal variability in alertness we experience in daily tasks is rarely taken into account in cognitive neuroscience. Here we studied neurobehavioral dynamics of cognitive control with decreasing alertness. We used the classic Simon task where participants hear the word "left" or "right" in the right or left ear, eliciting slower responses when the word and the side are incongruent—the conflict effect. Participants performed the task both while fully awake and while getting drowsy, allowing for the characterization of alertness modulating cognitive control. The changes in the neural signatures of conflict from local theta oscillations to a long-distance distributed theta network suggest a reconfiguration of the underlying neural processes subserving cognitive control when affected by alertness fluctuations.



中文翻译:

警觉性下降会重新配置认知控制网络

人们根据快速的情境变化灵活地适应其行为的非凡能力被称为认知控制。直觉上,认知控制被认为受警觉状态的影响。例如,在昏昏欲睡时,我们感觉无法充分执行艰巨的认知任务。尽管科学研究主要集中在睡眠剥夺和昼夜节律的影响上,但人们对于正常的清醒状态下每天自然的机敏波动如何影响认知控制知之甚少。在这里,我们将听觉域中的冲突任务与EEG神经动力学相结合,以测试冲突处理的神经和行为标记如何受到警觉性波动的影响。使用一种新颖的计算方法,我们将警报和困倦试验与两个测试阶段隔离开来,并观察到,尽管参与者(男女)通常都比较迟钝,但是与非冲突信息相比,对冲突信息的反应较慢所反映的典型冲突效果以及先前冲突的调解效果(冲突适应)仍然完好无损。但是,参与者在完全警觉期间显示的认知控制的典型神经标志物(局部中额θ带功率变化)在警觉降低时不再明显。相反,当困倦时,我们发现同一频段内大脑区域之间的远程信息共享(连接性)增加了。

重要性声明认知神经科学很少考虑我们在日常工作中遇到的正常警觉性差异。在这里,我们研究了认知控制的神经行为动力学随着警觉性的降低。我们使用经典的Simon任务,即参与者在右耳或左耳中听到“左”或“右”一词,当单词和侧面不一致时会引起较慢的响应,即冲突效果。参与者在完全清醒和昏昏欲睡时都执行了任务,从而可以表征调节认知控制的机敏性。从局部theta振荡到长距离分布式theta网络的冲突神经特征的变化表明,当受到警觉性波动的影响时,基础神经过程将重新配置,从而有助于认知控制。

更新日期:2020-09-10
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