Acute Stress Alters Auditory Selective Attention in Humans Independent of HPA: A Study of Evoked Potentials

BackgroundAcute stress is a stereotypical, but multimodal response to a present or imminent challenge overcharging an organism. Among the different branches of this multimodal response, the consequences of glucocorticoid secretion have been extensively investigated, mostly in connection with long-term memory (LTM). However, stress responses comprise other endocrine signaling and altered neuronal activity wholly independent of pituitary regulation. To date, knowledge of the impact of such “paracorticoidal” stress responses on higher cognitive functions is scarce. We investigated the impact of an ecological stressor on the ability to direct selective attention using event-related potentials in humans. Based on research in rodents, we assumed that a stress-induced imbalance of catecholaminergic transmission would impair this ability. Methodology/Principal FindingsThe stressor consisted of a single cold pressor test. Auditory negative difference (Nd) and mismatch negativity (MMN) were recorded in a tonal dichotic listening task. A time series of such tasks confirmed an increased distractibility occuring 4–7 minutes after onset of the stressor as reflected by an attenuated Nd. Salivary cortisol began to rise 8–11 minutes after onset when no further modulations in the event-related potentials (ERP) occurred, thus precluding a causal relationship. This effect may be attributed to a stress-induced activation of mesofrontal dopaminergic projections. It may also be attributed to an activation of noradrenergic projections. Known characteristics of the modulation of ERP by different stress-related ligands were used for further disambiguation of causality. The conjuncture of an attenuated Nd and an increased MMN might be interpreted as indicating a dopaminergic influence. The selective effect on the late portion of the Nd provides another tentative clue for this. Conclusions/SignificancePrior studies have deliberately tracked the adrenocortical influence on cognition, as it has proven most influential with respect to LTM. However, current cortisol-optimized study designs would have failed to detect the present findings regarding attention.

背景：急性应激（Acute stress）是机体遭遇当前或即将到来的超负荷挑战时，所产生的一类刻板但具有多模态特征的应答反应。在这类多模态应答的不同分支中，糖皮质激素（glucocorticoid）分泌所引发的效应已得到广泛研究，且大多围绕长时记忆（long-term memory, LTM）展开。然而，应激应答还涵盖了完全不依赖垂体调控的其他内分泌信号传导与神经元活动改变。迄今为止，针对此类“皮质旁”（paracorticoidal）应激应答对高级认知功能影响的研究仍较为匮乏。本研究借助人类事件相关电位（event-related potentials, ERP）技术，探究了生态型应激源对选择性注意定向能力的影响。基于啮齿类动物（rodents）的相关研究基础，我们推测应激诱导的儿茶酚胺能传递失衡会损伤该定向能力。
方法与主要发现：本实验采用单次冷压试验（cold pressor test）作为应激源。在音调双耳分听任务中，同步记录了听觉负差异波（auditory negative difference, Nd）与失匹配负波（mismatch negativity, MMN）。对该任务的时序性测试结果显示，应激启动后4~7分钟时，被试的分心程度显著升高，这一现象可通过Nd波幅的衰减得到直观反映。应激启动后8~11分钟，唾液皮质醇（salivary cortisol）水平开始升高，但此时事件相关电位（ERP）未出现进一步调制，因此排除了二者存在直接因果关联的可能性。该效应可能源于应激诱导的中脑前额叶多巴胺能投射激活，也可能与去甲肾上腺素能投射激活相关。研究团队借助不同应激相关配体对ERP的调制特性，进一步厘清了该效应的因果关联。Nd波幅衰减与MMN波幅升高同时出现这一联合特征，可被解读为多巴胺能系统参与了调控。对Nd晚期成分的选择性调控效应，为此提供了另一项初步佐证。
结论与意义：既往研究多刻意聚焦于肾上腺皮质对认知的调控作用，因为该通路已被证实对长时记忆的影响最为显著。然而，当前以皮质醇为优化目标的实验设计，无法探测到本研究中关于注意调控的相关发现。