Frontoparietal cortex controls spatial attention through modulation of anticipatory alpha rhythms

Abstract

A dorsal frontoparietal network, including regions in intraparietal sulcus (IPS) and frontal eye field (FEF), has been hypothesized to control the allocation of spatial attention to environmental stimuli. One putative mechanism of control is the desynchronization of electroencephalography (EEG) alpha rhythms (approximately 8-12 Hz) in visual cortex in anticipation of a visual target. We show that brief interference by repetitive transcranial magnetic stimulation (rTMS) with preparatory activity in right IPS or right FEF while subjects attend to a spatial location impairs identification of target visual stimuli approximately 2 s later. This behavioral effect is associated with the disruption of anticipatory (prestimulus) alpha desynchronization and its spatially selective topography in parieto-occipital cortex. Finally, the disruption of anticipatory alpha rhythms in occipital cortex after right IPS- or right FEF-rTMS correlates with deficits of visual identification. These results support the causal role of the dorsal frontoparietal network in the control of visuospatial attention, and suggest that this is partly exerted through the synchronization of occipital visual neurons.

Figure 1.

Task and rTMS localization. a, Sequence of events during a trial. b, Magnetic resonance imaging (MRI)-constructed stereotaxic template showing the sagittal (a), coronal (b), and axial (c) projections of the three rTMS sites on the right hemisphere. c, Inflated view of right hemisphere atlas brain with regions of dorsal and ventral attention network as in meta-analysis of He et al. (2007). Regions with coordinates are stimulated with rTMS in this experiment.

Figure 2.

Behavioral effects of rTMS at different cortical sites. a, Group means (±SE) of the reaction time (in milliseconds). Duncan post hoc tests: *p < 0.001, **p < 0.0001. b, Group means (±SE) of the accuracy (%).

Figure 3.

Topography of alpha power as function of rTMS conditions. a, Topographic maps of anticipatory low and high alpha ERD/ERS during the cue period (+500–2000 ms after the onset of the cue). b, Group means (±SE) of the low alpha ERD/ERS. Duncan post hoc tests: *p < 0.05, **p < 0.001. c, Group means (±SE) of the high alpha ERD/ERS.

Figure 4.

Contralateral spatial selectivity of alpha power by rTMS condition. Group means (±SE) of the high alpha ERD/ERS for the four Conditions (Sham, Right PrCe, Right FEF, Right IPS) divided by Hemisphere (contra or ipsi to cue stimulus).

Figure 5.

Across-subject correlation between alpha ERD/ERS and RTs. a, Scatter-plot showing the (positive) linear correlation between anticipatory low alpha ERD/ERS at P3 electrode and reaction time, for right “IPS” condition normalized with Sham condition. b, Scatter-plot showing the (positive) linear correlation between anticipatory high alpha ERD/ERS at O1 electrode and reaction time, for right “IPS” condition normalized with Sham condition.

Figure 6.

Within-subject relationship between alpha ERD/ERS and RTs. a, Group means (±SE) of the high alpha ERD for the canonical letter divided by reaction time (low or high). b, Group means (±SE) of the high alpha ERD for the rotated letter divided by reaction time (low or high). c, Scatter-plot showing the (positive) linear correlation between anticipatory high alpha ERD/ERS at P4 electrode and high reaction time (red square), for rotated target.

Figure 7.

Behavioral effects of rTMS as function of time of stimulation during delay. a, Group means (±SE) of the reaction time (in milliseconds) averaged over target visual field and cue validity. Duncan post hoc tests: *p < 0.03. b, Group means (±SE) of the accuracy (%).