Functional dissociation of the inferior frontal junction from the dorsal attention network in top-down attentional control

Abstract

The posterior lateral prefrontal cortex—specifically, the inferior frontal junction (IFJ)—is thought to exert a key role in the control of attention. However, the precise nature of that role remains elusive. During the voluntary deployment and maintenance of visuospatial attention, the IFJ is typically coactivated with a core dorsal network consisting of the frontal eye field and superior parietal cortex. During stimulus-driven attention, IFJ instead couples with a ventrolateral network, suggesting that IFJ plays a role in attention distinct from the dorsal network. Because IFJ rapidly switches activation patterns to accommodate conditions of goal-directed and stimulus-driven attention (Asplund CL, Todd JJ, Snyder AP, Marois R. Nat Neurosci 13: 507–512, 2010), we hypothesized that IFJ’s primary role is to dynamically reconfigure attention rather than to maintain attention under steady-state conditions. This hypothesis predicts that in a goal-directed visuospatial cuing paradigm IFJ would transiently deploy attention toward the cued location, whereas the dorsal attention network would maintain attentional weights during the delay between cue and target presentation. Here we tested this hypothesis with functional magnetic resonance imaging while subjects were engaged in a Posner cuing task with variable cue-target delays. Both IFJ and dorsal network regions were involved in transient processes, but sustained activity was far more evident in the dorsal network than in IFJ. These results support the account that IFJ primarily acts to shift attention whereas the dorsal network is the main locus for the maintenance of stable attentional states. NEW & NOTEWORTHY Goal-directed visuospatial attention is controlled by a dorsal fronto-parietal network and lateral prefrontal cortex. However, the relative roles of these regions in goal-directed attention are unknown. Here we present evidence for their dissociable roles in the transient reconfiguration and sustained maintenance of attentional settings: while maintenance of attentional settings is confined to the dorsal network, the configuration of these settings at the beginning of an attentional episode is a function of lateral prefrontal cortex.