Temporally and functionally distinct large-scale brain network dynamics supporting task switching

OBJECTIVE: Our daily activities require frequent switches among competing responses at the millisecond time scale. We determined the spatiotemporal characteristics and functional significance of rapid, large-scale brain network dynamics during task switching. METHODS: This cross-sectional study investigated patients with drug-resistant focal epilepsy who played a Lumosity cognitive flexibility training game during intracranial electroencephalography (iEEG) recording. According to a given task rule, unpredictably switching across trials, participants had to swipe the screen in the direction the stimulus was pointing or moving. Using this data, we described the spatiotemporal characteristics of iEEG high-gamma augmentation occurring more intensely during switch than repeat trials, unattributable to the effect of task rule (pointing or moving), within-stimulus congruence (the direction of stimulus pointing and moving was same or different in a given trial), or accuracy of an immediately preceding response. Diffusion-weighted imaging (DWI) tractography determined whether distant cortical regions showing enhanced activation during task switch trials were directly connected by white matter tracts. Trial-by-trial iEEG analysis deduced whether the intensity of task switch-related high-gamma augmentation was altered through practice and whether high-gamma amplitude predicted the accuracy of an upcoming response among switch trials. RESULTS: The average number of completed trials during five-minute gameplay was 221.4 per patient (range: 171–285). Task switch trials increased the response times, whereas later trials reduced them. Analysis of iEEG signals sampled from 860 brain sites effectively elucidated the distinct spatiotemporal characteristics of task switch, task rule, and post-error-specific high-gamma modulations. Post-cue, task switch-related high-gamma augmentation was initiated in the right calcarine cortex after 260 ms, right precuneus after 330 ms, right entorhinal after 420 ms, and bilateral anterior middle-frontal gyri after 450 ms. DWI tractography successfully showed the presence of direct white matter tracts connecting the right visual areas to the precuneus and anterior middle-frontal regions but not between the right precuneus and anterior middle-frontal regions. Task-related high-gamma amplitudes in later trials were reduced in the calcarine, entorhinal and anterior middle-frontal regions, but increased in the precuneus. Functionally, enhanced post-cue precuneus high-gamma augmentation improved the accuracy of subsequent responses among switch trials. CONCLUSIONS: Our multimodal analysis uncovered two temporally and functionally distinct network dynamics supporting task switching. High-gamma augmentation in the visual-precuneus pathway may reflect the neural process facilitating an attentional shift to a given updated task rule. High-gamma activity in the visual-dorsolateral prefrontal pathway, rapidly reduced through practice, may reflect the cost of executing appropriate stimulus-response translation.