Right Prefrontal TMS Disrupts Interregional Anticipatory EEG Alpha Activity during Shifting of Visuospatial Attention

Abstract

Visual attention can be shifted in space without moving the eyes. Amplitude decrease of rhythmical brain activity around 10 Hz (so called alpha activity) at contralateral posterior sites has been reported during covered shifts of visuospatial attention to one visual hemi-field. Alpha amplitude increase, on the other hand, can be found at ipsilateral visual cortex. There is some evidence suggesting an involvement of prefrontal brain areas during the control of attention-related anticipatory alpha amplitude asymmetry. This open question has been studied in detail using a multimodal approach combining transcranial magnetic stimulation (TMS) and multichannel electroencephalography (EEG) in healthy humans. Slow (1 Hz) repetitive TMS leading to reduced excitability of the stimulation site was delivered either to right frontal eye field (FEF) or a control site (vertex). Subsequently, participants had to perform a spatial cuing task in which covert shifts of attention were required to either the left or the right visual hemi-field. After stimulation at the vertex (control condition) a pattern of anticipatory, attention-related ipsilateral alpha increase/contralateral alpha decrease over posterior recording sites could be obtained. Additionally, there was pronounced coupling between (in particular right) FEF and posterior brain sites at EEG alpha frequency. When, however, right prefrontal cortex had been virtually lesioned preceding the task, these EEG correlates of visuospatial attention were attenuated. Notably, the effect of TMS at the right FEF on interregional fronto-parietal alpha coupling predicted the effect of TMS on response times. This suggests that visual attention processes associated with posterior EEG alpha activity are at least partly top-down controlled by the prefrontal cortex.

Keywords: frontal eye field; fronto-parietal attention network; repetitive transcranial magnetic stimulation; top-down control.

Figure 1

Mean response times as a function of experimental and stimulation condition. Only in valid trials response times were delayed after rTMS at the right FEF compared to stimulation at the vertex (control site). This was the case for trials with the left visual hemi-field attended as well as when attention had been shifted toward the right visual hemi-field.

Figure 2

Lateralized attention-related alpha amplitude. Topographical maps display anticipatory upper alpha amplitude difference values between conditions with attention directed to the left minus right visual hemi-field. Since ipsilateral alpha amplitude is increased compared to contralateral activity these difference values (attention left minus attention right) are positive for electrode sites over the left hemisphere, and they are negative for recording sites at the right hemisphere. Positive difference values are coded by warm, negative values by cold colors. Note that increased ipsilateral upper alpha amplitude at posterior recording sites as correlate of shifting visuospatial attention is only obtained after rTMS delivered at the control site. This pattern is absent after setting a virtual lesion at the right FEF.

Figure 3

Stable upper alpha latency shifts during directing of visuospatial attention. Arrows indicate consistent upper alpha latency shifts between recording sites. Note that prefrontal sites are always leading posterior sites during shifts of visuospatial attention. Red arrows indicate stable latency shifts after rTMS at the control stimulation site whereas green arrows indicate latency shifts after FEF rTMS. Top-down control from (right) prefrontal to posterior electrodes is strongly attenuated after stimulation of the right FEF.

Figure 4

(A) Maximal cross-correlation coefficient as a function of hemisphere and stimulation condition. Averaged maxima of cross-correlation coefficient between recording site FC4 and all posterior electrodes of interest as well as FC3 and posterior recording sites are shown. After rTMS to the right FEF attenuated cross-correlation coefficients between FC4 (overlying the stimulation site) and posterior sites is obtained. (B) Hemispheric differences of cross-correlation strength between frontal and posterior sites. Note that in contrast to FC3 there is no significant difference found for coupling between right frontal and either left or right posterior sites. This suggests the right FEF to top-down control bilateral visual cortex.

Figure 5

Correlations between rTMS dependent interregional coupling strength and response times. Subjects exhibiting a stronger attenuation of cross-correlation coefficients after stimulation of the right FEF compared to vertex rTMS show larger response time increase. Note that in this effect there are always posterior sites involved that are located contralateral to the attended visual hemi-field.