The role of neural oscillations in coordinating competing cognitive processes

人类大脑是如何灵活地采样和优先处理传入的感官信息的？想象一下新年前夜纽约时代广场上繁忙的景象：高耸的摩天大楼、闪烁的灯光、刺耳的音乐、纷乱的交通、形形色色的人群、多种对话的嘈杂声，而你却在努力听朋友用手机和你交谈。由于我们的大脑感官处理资源有限，我们根本无法完全处理所有涌入这个场景的感官信息。因此，我们选择性地将注意力集中在对行为最重要的信息和事件上。大脑使用注意力过滤器来决定什么应该优先考虑，这些过滤器可以增强相关信息。例如，注意力可以选择性地促进对朋友声音的听觉处理，并增强视觉处理，集中在你们约定见面的街角。虽然以前的研究有时将特定位置（例如，在特定的街角）的视觉注意力描述为一个持续的聚光灯，照亮了行为上重要的信息，但最近的其他研究表明，这种注意力聚光灯每秒闪烁约四次。也就是说，注意力聚光灯的强度随着时间有节奏地增加和减少。聚光灯的这种有节奏的闪烁表明，大脑正在“签到”或“更新”大约每秒四次，以确保注意力聚光灯当前的焦点仍然是观察者最重要和最相关的焦点。这种有节奏的检查过程创造了时间窗口，当注意力更容易转移到一个新的位置时，潜在地在采样和转移行为之间创造了一个关键的平衡。注意力聚光灯有节奏的闪烁可能已经发展成为一种生存机制，帮助我们的祖先（和其他动物），例如，灵活地寻找食物，同时仍然注意捕食者。该项目研究了正常人类受试者的这种有节奏的注意力闪烁的神经起源和行为后果。这项研究还可能为与异常有限的注意力灵活性相关的脑部疾病提供新的线索，比如注意缺陷多动障碍（ADHD），在这种情况下，个体可能会陷入与高度注意力分散（即行为转移）或过度集中（即抽样行为）相关的行为状态。为了研究视觉注意力聚光灯的强度是如何以及为什么每秒有节奏地增加和减少大约四次，这项研究使用了眼动追踪（一种对眼睛位置的行为测量）和脑电图（EEG，一种非侵入性的，全面测量大脑电活动的方法）。首先，这项研究探讨了注意力较弱的时间段是否也与注意力分散的增加有关。这些实验的结果将检验一个假设，即大脑会周期性地分散注意力，以增强选择性注意力的更新。虽然这对于完成需要集中注意力和为突发事件做好准备的日常任务至关重要，比如在繁忙的交通高峰时段开车时可能遇到的意外事件，但在我们日益分散注意力的现代环境中（例如，笔记本电脑在我们面前打开，智能手机在我们附近），这可能是一个潜在的问题。其次，该项目调查了注意力聚光灯强度的节奏变化是否反映了大脑用来调节竞争功能的基本机制。先前的研究表明，在视觉处理过程中，控制注意力相关刺激的大脑区域（如大脑皮层的额眼区）也会将眼球运动导向行为上重要的信息。这个项目的实验测试了这些大脑区域是否会在一段时间内交替执行这些潜在的视觉和运动（即眼球运动）功能，例如，与较弱的视觉注意力聚光灯相关的时间段也与更多的眼球运动相关。最后，这个项目调查大脑是否使用这种竞争功能的节奏协调，不仅在感觉处理中，而且作为一种更普遍的机制来解决可能的认知冲突的来源，这种冲突可能发生在受试者被要求在短时间内同时记住几个相似的项目的任务中。这些实验测试了这些被记住的事物的表征强度是否随时间有节奏地波动（即，类似于注意力视觉感官聚光灯的闪烁强度）。这项研究将增加对大脑如何从环境中动态采样视觉信息以及大脑如何不断更新以保持关键认知灵活性的理解。该奖项反映了美国国家科学基金会的法定使命，并通过使用基金会的知识价值和更广泛的影响审查标准进行评估，被认为值得支持。

How does the human brain flexibly sample and prioritize incoming sensory information? Imagine a busy scene in Times Square in New York City on New Year’s Eve: towering skyscrapers, flashing lights, blaring music, swirling traffic, a colorful crowd of mingling people, the hubbub of multiple conversations, all while you are trying to listen to a friend talking with you on your cell phone. Since our brain has limited sensory processing resources, we simply cannot fully process all of the surging flood of incoming sensory information arriving in this scene. So instead, we selectively focus our attention on the most behaviorally important information and events. The brain uses attentional filters to determine what should be prioritized, and these filters can boost relevant information. For example, attention can selectively boost auditory processing of your friend’s voice, and enhance visual processing, focused on the street corner where you agreed to meet. Whereas previous research has sometimes described visual attention at a specific location (e.g., at a specific street corner) as a sustained spotlight that illuminates behaviorally important information, other recent investigations have instead shown that this attentional spotlight flickers at about four times per second. That is, the strength of the attentional spotlight rhythmically increases and decreases over time. This rhythmic flickering of the spotlight suggests that the brain is “checking-in” or “updating” about four times per second to ensure that the present focus of the attentional spotlight is still the most important and relevant focus for the observer. This rhythmic checking-in process creates time windows when it is easier to shift the attentional spotlight to a new location, potentially creating a critical balance between sampling and shifting behaviors. Rhythmic flickering of the attentional spotlight may have developed as a survival mechanism to help our ancestors (and other animals), for example, flexibly look for food while still keeping an eye out for predators. This project investigates the neural origins and behavioral consequences of this rhythmic flickering of attention in normal human subjects. This research may also shed new light on brain disorders associated with abnormally limited attentional flexibility, such as attention deficit hyperactivity disorder (ADHD), in which individuals can become fixed in behavioral states associated with either high distractibility (i.e., shifting behaviors) or hyper-focus (i.e., sampling behaviors).In order to investigate how and why the strength of the visual attentional spotlight rhythmically waxes and wanes about four times per second, this research uses eye tracking (a behavioral measure of eye position), and electroencephalography (EEG, a non-invasive, global measure of electrical activity in the brain) in humans. First, this research explores whether time periods associated with a weaker attentional spotlight are also associated with increased distractibility. The results of these experiments will test the hypothesis that the brain is wired to be periodically distractible to enhance updating of selective attention. While this may be critical to performing everyday tasks that require both focus and preparedness for unexpected events, such as one may encounter while driving a car in busy rush-hour traffic, it is potentially problematic in our increasingly distracting modern environments (e.g., with a laptop open in front of us and a smart phone nearby). Second, this project investigates whether rhythmic change in the strength of the attentional spotlight reflects a fundamental mechanism that the brain uses to mediate competing functions. Previous research has shown that the very same brain regions (such as the frontal eye fields in the cerebral cortex) that direct attention-related boosts in visual processing, also direct eye movements toward behaviorally important information. This projects' experiments test whether these brain regions perform these potentially competing visual and motor (i.e., eye movements) functions by alternating between them over time, such that time periods associated with a weaker visual attentional spotlight are also associated with more eye movements. Finally, this project investigates whether the brain uses such rhythmic coordination of competing functions, not only in sensory processing, but as a more general mechanism for resolving sources of possible cognitive conflict, that might occur in a task where subjects are asked to simultaneously remember several similar items for a short period of time. These experiments test whether the strength of representations for these to-be-remembered items rhythmically fluctuates over time (i.e., similar to the flickering strength of the attentional visual sensory spotlight). This research will increase understanding both of how the brain dynamically samples visual information from the environment and also how the brain continuously updates to maintain critical cognitive flexibility.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.