Interaction of Stimulus-Driven Reorienting and Expectation in Ventral and Dorsal Frontoparietal and Basal Ganglia-Cortical Networks

Abstract

Shifts of attention to unattended stimuli (stimulus-driven reorienting) are often studied by measuring responses to unexpected stimuli, confounding reorienting and expectation. We separately measured the blood-oxygenation-level-dependent signal for both factors by manipulating the probability of salient visual cues that either shifted attention away from or maintained attention on a stream of visual stimuli. The results distinguished three networks recruited by reorienting. Right temporoparietal junction (TPJ), the posterior core of a ventral frontoparietal network, was activated more by cues for shifting than maintaining attention independently of cue location and probability, acting as a switch. TPJ was separately modulated by low probability cues, which signaled a breach of spatial expectation, independently of whether they shifted attention. Under resting conditions, TPJ activity was correlated [resting-state functional connectivity magnetic resonance imaging, (rs-fcMRI)] with right inferior frontal gyrus (IFG), an anterior component of the ventral network. Nevertheless, IFG was activated only by unexpected shifts of attention, dissociating its function from TPJ. Basal ganglia and frontal/insula regions also were activated only when reorienting was unexpected but showed strong rs-fcMRI among themselves, not with TPJ/IFG, defining a distinct network that may retrieve/activate commands for shifting attention. Within dorsal frontoparietal regions, shifting attention produced sustained spatially selective modulations in intraparietal sulcus (IPS) and frontal-eye field (FEF), and transient less selective modulations in precuneus and FEF. Modulations were observed even when reorienting was likely, but increased when reorienting was unexpected. The latter result may partly reflect interactions with lateral prefrontal components of the basal-ganglia/frontal/insula network that showed significant rs-fcMRI with the dorsal network.