Orbitofrontal cortex biases attention to emotional events

Abstract

We examined the role of orbitofrontal (OF) cortex in regulating emotion–attention interaction and the balance between involuntary and voluntary attention allocation. We studied patients with OF lesion applying reaction time (RT) and event-related potential (ERP) measures in a lateralized visual discrimination task with novel task-irrelevant affective pictures (unpleasant, pleasant, or neutral) preceding a neutral target. This allowed for comparing the effects of automatic attention allocation to emotional versus neutral stimuli on subsequent voluntary attention allocation to target stimuli. N2–P3a and N2–P3b ERP components served as measures of involuntary and voluntary attention allocation correspondingly. Enhanced N2–P3a amplitudes to emotional distractors and reduced N2–P3b amplitudes to targets preceded by emotional distractors were observed in healthy subjects, suggesting automatic emotional orienting interfered with subsequent voluntary orienting. OF patients showed an opposite pattern with tendency towards reduced N2–P3a responses to emotional distractors, suggesting impaired automatic orienting to emotional stimuli due to orbitofrontal damage. Enhanced N2–P3b responses to targets preceded by any affective distractor were observed in OF patients, suggesting bias towards voluntary target-related attention allocation due to orbitofrontal lesion. Behavioral evidence indicated that left visual field (LVF) attention performance was modulated by emotional stimuli. Specifically, OF patients responded faster to LVF targets subsequent to pleasant emotional distractors. We suggest that damage to the orbitofrontal circuitry leads to dysbalance between voluntary and involuntary attention allocation in the context of affective distractors with predisposition to posterior target-related processing over frontal novelty and affect-related processing. Furthermore, we suggest that orbitofrontal influence on emotion–attention interaction is valence and hemisphere dependent.

Keywords:

• Novelty
• Affective
• Event-related potential
• P300
• Frontal
• Lesion
• Attention
• Reaction time
• Behavior
• Electrophysiology

Acknowledgments

Supported by the Academy of Finland, Competitive Research Funding of the Pirkanmaa Hospital District, and a National Institute of Neurological Disorders and Stroke (NINDS) Grant NS 21135.