Spontaneous Fluctuations in the Flexible Control of Covert Attention

Spontaneous fluctuations in cognitive flexibility are characterized by moment-to-moment changes in the efficacy of control over attentional shifts. We used fMRI to investigate the neural correlates in humans of spontaneous fluctuations in readiness to covertly shift attention between two peripheral rapid serial visual presentation streams. Target detection response time (RT) after a shift or hold of covert spatial attention served as a behavioral index of fluctuations in attentional flexibility. In particular, the cost associated with shifting attention compared with holding attention varied as a function of pretrial brain activity in key regions of the default mode network (DMN), but not the dorsal attention network. High pretrial activity within the DMN was associated with a greater increase in shift trial RT relative to hold trial RT, revealing that these areas are associated with a state of attentional stability. Conversely, high pretrial activity within bilateral anterior insula and the presupplementary motor area/supplementary motor area was associated with a greater decrease in shift trial RT relative to hold trial RT, reflecting increased flexibility. Our results importantly clarify the roles of the precuneus, medial prefrontal cortex, and lateral parietal cortex, indicating that reduced activity may not simply indicate greater task engagement, but also, specifically, a readiness to update the focus of attention. Investigation of the neural correlates of spontaneous changes in attentional flexibility may contribute to our understanding of disorders of cognitive control as well as healthy variability in the control of spatial attention.

Individuals regularly experience fluctuations in preparatory cognitive control that affect performance in everyday life. For example, individuals are able to more quickly initiate a spatial shift of attention at some moments than at others. The current study revealed that pretrial brain activity in specific cortical regions predicted trial-by-trial changes in participants' abilities to flexibly shift the focus of attention. Intrinsically generated fluctuations in brain activity within several key default mode network regions, as well as within the anterior insula and presupplementary/supplementary motor areas, carried behavioral consequences for preparatory attentional control beyond lapses of attentional engagement. Our results are the first to link intrinsic variation in pretrial brain activity to moment-by-moment changes in preparatory attentional control over spatial selection.