Rule-Guided Executive Control of Response Inhibition: Functional Topography of the Inferior Frontal Cortex

BackgroundThe human inferior frontal cortex (IFC) is a large heterogeneous structure with distinct cytoarchitectonic subdivisions and fiber connections. It has been found involved in a wide range of executive control processes from target detection, rule retrieval to response control. Since these processes are often being studied separately, the functional organization of executive control processes within the IFC remains unclear.
Methodology/Principal FindingsWe conducted an fMRI study to examine the activities of the subdivisions of IFC during the presentation of a task cue (rule retrieval) and during the performance of a stop-signal task (requiring response generation and inhibition) in comparison to a not-stop task (requiring response generation but not inhibition). We utilized a mixed event-related and block design to separate brain activity in correspondence to transient control processes from rule-related and sustained control processes. We found differentiation in control processes within the IFC. Our findings reveal that the bilateral ventral-posterior IFC/anterior insula are more active on both successful and unsuccessful stop trials relative to not-stop trials, suggesting their potential role in the early stage of stopping such as triggering the stop process. Direct countermanding seems to be outside of the IFC. In contrast, the dorsal-posterior IFC/inferior frontal junction (IFJ) showed transient activity in correspondence to the infrequent presentation of the stop signal in both tasks and the left anterior IFC showed differential activity in response to the task cues. The IFC subdivisions also exhibited similar but distinct patterns of functional connectivity during response control.
Conclusions/SignificanceOur findings suggest that executive control processes are distributed across the IFC and that the different subdivisions of IFC may support different control operations through parallel cortico-cortical and cortico-striatal circuits.

【研究背景】人类额下回（inferior frontal cortex, IFC）是一类高度异质性的大脑结构，拥有明确的细胞构筑亚区与纤维连接通路。既往研究证实，该结构参与从目标检测、规则提取到反应控制的一系列执行控制过程。由于上述过程通常被独立研究，额下回内执行控制过程的功能组织模式至今仍未明确。

【方法与主要结果】本研究采用功能性磁共振成像（fMRI）技术，对比分析被试在任务线索呈现（对应规则提取过程）、停止信号任务（需完成反应产生与抑制）与非停止任务（仅需反应产生，无需抑制）中，额下回各亚区的神经活动模式。我们结合事件相关设计与区组设计，将与瞬时控制过程相关的脑活动，与规则相关及持续控制过程的脑活动进行分离。研究发现额下回内的控制过程存在显著分化：结果显示，相较于非停止试次，双侧腹侧后额下回/前脑岛在成功与失败的停止试次中均表现出更高激活水平，提示其可能参与停止过程的早期阶段（如触发停止程序）。直接反应撤销过程似乎并不涉及额下回区域。与之相对，背侧后额下回/额下回联络区（inferior frontal junction, IFJ）在两项任务中，仅在停止信号罕见呈现时表现出瞬时激活；而左侧前额下回则在响应任务线索时呈现差异化激活。此外，额下回各亚区在反应控制过程中，还展现出相似但彼此区分的功能连接模式。

【结论与意义】本研究结果表明，执行控制过程广泛分布于额下回内，且额下回的不同亚区可通过并行的皮层-皮层与皮层-纹状体通路，分别支撑不同的控制操作。