The effect of neural substrates of dual top-down control networks on modulating set-maintenance and rapid-adaptive performance

Abstract

Background Top-down control function is important for handling goal-directed actions. Two distinct top-down brain networks, cingulo-opercular network (CON) and fronto-parietal network (FPN), were identified for set-maintenance and rapid-adaptive control respectively. Emerging evidence showed that these two networks may interact with each other for handling tasks with higher top-down control demand. This study adopted transcranial magnetic stimulation (TMS) method to activate transiently representative brain substrates in the CON and FPN to enable better understanding the differential effect of substrates of two networks to handle different demand levels of set-maintenance and rapid-adaptive control. Objectives This two-phase study aimed to examine, under higher and lower demands of set-maintenance control and rapid-adaptive control, how the TMS-induced activation at the distinct substrates of the CON and the FPN may influence differentially on (1) the subsequent task performance; (2) the neural processes during task-set implementation and information processing; (3) the changes of effective connectivity during task-set implementation and information processing. Methods Younger adults (Phase 1: N = 13; mean age = 26.5 ± 4.1; Phase 2: N = 18, mean age=25 ± 4.9) were recruited to participate in a single task with Flanker task, and a dual task with Flanker and 2-back task was performed before and after iTBS stimulations that were applied at three selected sites corresponding to the substrates of the CON (i.e., ai/fO, dACC/msFC and aPFC), two substrates of the FPN (i.e., dlPFC and dFC) (Phase 2 only) and a control site (i.e., vertex). Reaction time and electroencephalogram data were recorded during the cognitive tasks. To achieve the objectives, repeated measure ANOVA was used to analyse the 1) behavioural performance of the Flanker task; 2) the mean amplitude difference between target stimulation and control stimulation of two event-related components, namely the stimulus-preceding negativity (SPN; -200 - 0ms) and N1 (150 - 300ms) component. The SPN and N1 results help to determine the time windows for later analysis of oscillation frequency. Then the isolated coherence analysis (ICoh) was used to examine the effect of stimulated substrates on the changes of effective connectivity in term of the theta- and alpha-band oscillations, which were verified by the time-frequency analysis (TFA) method. Results A shorter reaction time was found after iTBS stimulation at aI/fO of the CON and dlPFC of FPN under higher demand of set-maintenance and rapid-adaptive. ICoh analyses showed, during task-set implementation, iTBS-stimulated aI/fO altered the connectivity in which dlPFC received more theta-band oscillation from aI/fO, aPFC and dFC for handling higher set-maintenance and rapid-adaptive demand. During information processing, iTBS-stimulated dlPFC increased the flow of theta-band oscillation from dACC/msFC to dlPFC to handle higher rapid-adaptive demand while aI/fO and dACC/msFC decreased the flow of alpha-band oscillation to handle higher set-maintenance demand. Conclusion The findings of this study shed light on the mechanism for flexible cooperation between the dual top-down networks. This was shown in the influential effect of aI/fO of the CON and dlPFC of FPN on set-maintenance control and rapid-adaptive control, respectively. Furthermore, the results suggested that the changes of connectivity of the two top-down networks appear to be specific to different demands of set-maintenance and rapid-adaptive control for task-set implementation and information processing performances. There are significant implications of these results for training strategies to enhance the top-down control functions.