Assessing TMS-evoked cognitive network responses depending on neurocognitive and oscillatory brain state: A simultaneous TMS-EEG-fMRI project

Human cognition arises from information exchange within and between functionally connected brain networks. Alterations in such signal propagation across networks are linked to numerous disorders. Brain-wide signal propagation can be experimentally studied with simultaneous transcranial magnetic stimulation (TMS) and functional magnetic resonance imaging (fMRI), where TMS pulses introduce a signal at a certain network node and fMRI charts its propagation through the network. Yet, this approach ignores the fact that the (network) impact of a TMS pulse depends on brain state, where brain state fluctuates spontaneously from moment to moment (e.g. oscillatory state) as well as depending on what a participant does (neurocognitive state). Here, we assessed TMS-evoked fMRI activations as a function of neurocognitive state (eyes open versus eyes closed in complete darkness) and oscillatory state (low versus high pre-TMS alpha power, as measured with simultaneous electroencephalography (EEG)). We applied supra-versus sub-threshold triple-pulse TMS to the right posterior parietal cortex in eight participants, while simultaneously recording EEG and fMRI during two different ocular states. In this first application of the multimodal TMS-EEG-fMRI paradigm to a cognitive network hub, we did not find evidence for a brain state modulation of TMS-induced signal propagation. Instead, we found state-independent TMS-evoked fMRI responses mostly in sensory areas such as the insula, superior temporal gyrus, anterior cingulate cortex, and thalamus, but also in the frontal eye fields. Interestingly, neurocognitive state did seem to modulate the fMRI response to indirect TMS effects such as sensory stimulation. These results lead to several important insights for future cognitive multimodal TMS experiments.