A Dynamic Interplay within the Frontoparietal Network Underlies Rhythmic Spatial Attention

• Published in: Neuron (Cambridge, Mass.) Mass.), 2018-08, Vol.99 (4), p.842-853.e8
• Main Authors: Fiebelkorn, Ian C., Pinsk, Mark A., Kastner, Sabine
• Format: Article
• Language: English
• Subjects: Action Potentials - physiology; Animals; attention; Attention - physiology; Eye movements; FEF; Fourier transforms; Frontal Lobe - physiology; frontoparietal network; Information processing; LIP; Macaca fascicularis; Male; Monkeys & apes; Nerve Net - physiology; Oscillations; Parietal Lobe - physiology; phase-dependent behavior; Photic Stimulation - methods; Psychomotor Performance - physiology; Rhythm; Software; theta; Theta Rhythm - physiology; vision; Visual task performance
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2018.07.038

Classic studies of spatial attention assumed that its neural and behavioral effects were continuous over time. Recent behavioral studies have instead revealed that spatial attention leads to alternating periods of heightened or diminished perceptual sensitivity. Yet, the neural basis of these rhythmic fluctuations has remained largely unknown. We show that a dynamic interplay within the macaque frontoparietal network accounts for the rhythmic properties of spatial attention. Neural oscillations characterize functional interactions between the frontal eye fields (FEF) and the lateral intraparietal area (LIP), with theta phase (3–8 Hz) coordinating two rhythmically alternating states. The first is defined by FEF-dominated beta-band activity, associated with suppressed attentional shifts, and LIP-dominated gamma-band activity, associated with enhanced visual processing and better behavioral performance. The second is defined by LIP-specific alpha-band activity, associated with attenuated visual processing and worse behavioral performance. Our findings reveal how network-level interactions organize environmental sampling into rhythmic cycles. •Non-human primates, like humans, sample the visual scene in rhythmic cycles•Neural oscillations in the frontoparietal network modulate perceptual sensitivity•Theta phase acts as a clocking mechanism, organizing alternating attentional states•Temporal dynamics linked to specific function and cell type define attentional state Fiebelkorn et al. use simultaneous recordings in two hubs of the macaque frontoparietal network to demonstrate a neural basis of rhythmic sampling during spatial attention. Theta-organized, alternating attentional states, characterized by different spatiotemporal dynamics, shape environmental sampling.