title: Orchestrating Proactive and Reactive Mechanisms for Filtering Distracting Information: Brain-Behavior Relationships Revealed by a Mixed-Design fMRI Study.
abstract: Given the information overload often imparted to human cognitive-processing systems, suppression of irrelevant and distracting information is essential for successful behavior. Using a hybrid block/event-related fMRI design, we characterized proactive and reactive brain mechanisms for filtering distracting stimuli. Participants performed a flanker task, discriminating the direction of a target arrow in the presence versus absence of congruent or incongruent flanking distracting arrows during either Pure blocks (distracters always absent) or Mixed blocks (distracters on 80% of trials). Each Mixed block had either 20% or 60% incongruent trials. Activations in the dorsal frontoparietal attention network during Mixed versus Pure blocks evidenced proactive (blockwise) recruitment of a distraction-filtering mechanism. Sustained activations in right middle frontal gyrus during 60% Incongruent blocks correlated positively with behavioral indices of distraction-filtering (slowing when distracters might occur) and negatively with distraction-related behavioral costs (incongruent vs congruent trials), suggesting a role in coordinating proactive filtering of potential distracters. Event-related analyses showed that incongruent trials elicited greater reactive activations in 20% (vs 60%) Incongruent blocks for counteracting distraction and conflict, including in the insula and anterior cingulate. Context-related effects in occipitoparietal cortex consisted of greater target-evoked activations for distracter-absent trials (central-target-only) in Mixed versus Pure blocks, suggesting enhanced attentional engagement. Functional-localizer analyses in V1/V2/V3 revealed less distracter-processing activity in 60% (vs 20%) Incongruent blocks, presumably reflecting tonic suppression by proactive filtering mechanisms. These results delineate brain mechanisms underlying proactive and reactive filtering of distraction and conflict, and how they are orchestrated depending on distraction probability, thereby aiding task performance. Significance statement: Irrelevant stimuli distract people and impair their attentional performance. Here, we studied how the brain deals with distracting stimuli using a hybrid block/event-related fMRI design and a task that varied the probability of the occurrence of such distracting stimuli. The results suggest that when distraction is likely, a region in right frontal cortex proactively implements attentional control mechanisms to help filter out any distracting stimuli that might occur. In contrast, when distracting input occurs infrequently, this region is more reactively engaged to help limit the negative consequences of the distracters on behavioral performance. Our results thus help illuminate how the brain flexibly responds under differing attentional demands to engender effective behavior.
authors.affiliation: Center for Cognitive Neuroscience, Department of Psychology, University of Milano-Bicocca, Milan 20126, Italy, Department of Psychology, University of California, San Diego, California 92093.
authors.forename: Francesco
authors.identifier: http://orcid.org/0000-0002-4071-4783
authors.initials: F
authors.lastname: Marini
authors.affiliation: Center for Cognitive Neuroscience.
authors.forename: Elise
authors.identifier: http://orcid.org/0000-0001-5993-1692
authors.initials: E
authors.lastname: Demeter
authors.affiliation: Center for Cognitive Neuroscience.
authors.forename: Kenneth C
authors.initials: KC
authors.lastname: Roberts
authors.affiliation: Department of Neurological, Biomedical and Movement Science, University of Verona, Verona 37134, Italy, and Italian Institute of Neuroscience, Verona 37134, Italy.
authors.forename: Leonardo
authors.identifier: http://orcid.org/0000-0001-8566-0611
authors.initials: L
authors.lastname: Chelazzi
authors.affiliation: Center for Cognitive Neuroscience, Departments of Psychiatry and Psychology and Neuroscience, Duke University, Durham, North Carolina 27708, woldorff@duke.edu.
authors.forename: Marty G
authors.initials: MG
authors.lastname: Woldorff
mesh_terms: D000293:Adolescent; D000328:Adult; D001288:Attention / Q000502:physiology*; D001921:Brain / Q000502:physiology*; D001931:Brain Mapping / Q000379:methods; D003220:Conflict, Psychological; D005260:Female; D006801:Humans; D008279:Magnetic Resonance Imaging / Q000379:methods*; D008297:Male; D010775:Photic Stimulation / Q000379:methods; D011597:Psychomotor Performance / Q000502:physiology*; D011930:Reaction Time / Q000502:physiology*; D055815:Young Adult
keywords: attention; cognitive control; distraction filtering; flanker task; mixed-design fMRI