The role of brain oscillations in flexible attentional control

Fehér, Daniel Kristoffer (2018). The role of brain oscillations in flexible attentional control (Submitted). (Dissertation, Universitäre Psychiatrische Dienste Bern, Universität Bern, Medizinische Fakultät)

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Our capacity to quickly adapt to changing cognitive demands fundamentally relies on the ability of our brain to quickly establish the appropriate communication among brain areas that are relevant for the task at hand. This ability to flexibly reconfigure communication in the brain underlies for instance our capacity to swiftly reorient our attention according to our goals, or to flexibly filter relevant information from ever changing distractors. Oscillatory brain activities have been considered to enable this type of flexible effective communication structure on top of the anatomical communication structure (Fries, 2005). However, amidst accumulating correlational observations supporting the connection between oscillatory neural activity and neuronal communication, there is currently still a lack of direct experimental demonstration that oscillatory activity causally modulates neural transmission. Transcranial alternating current stimulation (tACS) has held great promises in elucidating the causal role of neural oscillations in neuronal communication and in behaviour, in a non-invasive manner. However, we still know little about the actual modulatory mechanism of tACS.

The goal of the present thesis was to develop a new method to measure the immediate effect of tACS on local excitability and signalling efficacy across cortical networks, with the purpose of addressing how oscillatory brain activity subserves flexible attentional control by modulating neuronal communication. To this end, the thesis comprises of the following three publications.

In the first publication, we establish our experimental protocol and technical advices for simultaneous electroencephalography (EEG) recording during tACS. Concurrent EEG-tACS can offer a means to address the immediate neurophysiological effect of tACS, however the approach comes with several challenges. We show how, when improperly carried out, the artifacts introduced by tACS into the EEG data renders the data unrecoverable through any artifact removal approach.

In the second publication, we establish a new method using concurrent tACS, transcranial magnetic stimulation (TMS) and EEG to address the causal role of neural oscillations in modulating transmission efficacy in cortical networks. The rationale of the concurrent tACSTMS-EEG method is that while introducing oscillatory activity with tACS, we can measure neural transmission as TMS-induced neural activity with EEG. Through tACS, we introduced theta oscillatory activity in the dorsolateral prefrontal cortex (DLPFC). For assessing resultant changes in the efficacy of neural transmission, we simultaneously apply subthreshold singlepulse TMS over the DLPFC at four different phases of tACS (90°, 180°, 270°, 360°) and measure the spread of TMS-evoked EEG potentials (TEPs). The amount of current spread is modulated by the functional status of the neural network, thereby providing a measure of changes in signalling efficacy. We demonstrate that we can successfully remove tACS artifacts from TMS-EEG data, and find that the amplitude of TEPs depends on the phase of the introduced 6 Hz activity during tACS.

In the third publication, we address the causal role of inter-regional oscillatory phaserelations in modulating cortico-cortical signalling efficacy. For this purpose, we again employ our concurrent tACS-TMS-EEG method. Through tACS we introduce theta oscillatory activity in the DLPFC and the posterior parietal cortex (PPC); two nodes of the frontoparietal network. We apply 6 Hz tACS to the DLPFC and PPC simultaneously in an in-phase or anti-phase manner. We demonstrate that the tACS-induced theta oscillations modulate TEPs in a phase-dependent manner during in-phase and anti-phase tACS, and that the induced phase-relation across the human frontoparietal network affects the propagation of signal through as well as beyond the frontoparietal network, from the PPC to area V5. Our results therefore suggest that inter-nodal phase-relations of oscillatory neural activity impact neural transmission beyond the synchronizing network nodes. Our results lend support for the causal role of phase-synchronized endogenous oscillatory activity in modulating inter-regional neuronal communication.

To sum up, the studies conducted as part of this thesis focus on addressing the causal role of neuronal oscillations in modulation brain network communication. The methodological groundwork carried out as part of this thesis will enable us to proceed to address how informational routing through dynamically established oscillatory coherence serves to enable flexible attentional control. The concurrent tACS-TMS-EEG also hold great promise in shedding new light on sources of variability in efficacy of tACS and could help pave the way for new clinical treatment avenues for disorders of attentional control.

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