Causal evidence for increased theta and gamma phase consistency in a parieto-frontal network during the maintenance of visual attention

Abstract

Endogenous visuo-spatial attention is under the control of a fronto-parietal network of brain regions. One key node in this network, the intra-parietal sulcus (IPS), plays a crucial role in maintaining endogenous attention, but little is known about its ongoing physiology and network dynamics during different attentional states. Here, we investigated the reactivity of the left IPS in response to brain stimulation under different states of selective attention. We recorded electroencephalography (EEG) in response to single pulses of transcranial magnetic stimulation (TMS) of the IPS, while participants (N = 44) viewed bilateral random-dot motion displays. Individual MRI-guided TMS pulses targeted the left IPS, while the left primary somatosensory cortex (S1) served as an active control site. In separate blocks of trials, participants were cued to attend covertly to the motion display in one hemifield (left or right) and to report brief coherent motion targets. The perceptual load of the task was manipulated by varying the degree of motion coherence of the targets. Excitability, variability and information content of the neural responses to TMS were assessed by analysing TMS-evoked potential (TEP) amplitude and inter-trial phase clustering (ITPC), and by performing multivariate decoding of attentional state. Results revealed that a left posterior region displayed reduced variability in the phase of theta and gamma oscillations following TMS of the IPS, but not of S1, when attention was directed contralaterally, rather than ipsilaterally to the stimulation site. A right frontal cluster also displayed reduced theta variability and increased amplitude of TEPs when attention was directed contralaterally rather than ipsilaterally, after TMS of the IPS but not S1. Reliable decoding of attentional state was achieved after TMS pulses of both S1 and IPS. Taken together, our findings suggest that endogenous control of visuo-spatial attention leads to changes in the intrinsic oscillatory properties of the IPS and its associated fronto-parietal network.