Internal representations are prioritized by frontal-parietal theta connectivity and suppressed by alpha oscillation dynamics: evidence from concurrent EEG-TMS and invasive-EEG

Control over internal representations requires the prioritization of relevant information and suppression of irrelevant information. The frontal-parietal network exhibits prominent neural oscillations during these distinct cognitive processes. Yet, the causal role of this network-scale activity is unclear. Here, we targeted theta-frequency frontal-parietal coherence and dynamic alpha oscillations in posterior parietal cortex using online rhythmic transcranial magnetic stimulation (TMS) in women and men while they prioritized or suppressed internally maintained working memory (WM) representations. Using concurrent high-density EEG, we provided evidence that we acutely drove the targeted neural oscillation and TMS improved WM capacity only when the evoked-activity corresponded with the desired cognitive process. To suppress an internal representation, we increased the amplitude of lateralized alpha oscillations in the posterior parietal cortex contralateral to the irrelevant visual field. For prioritization, we found that TMS to prefrontal cortex increased theta-frequency connectivity in the prefrontal-parietal network contralateral to the relevant visual field. To understand the spatial specificity of these effects, we administered the WM task in participants with implanted electrodes. We found that theta connectivity during prioritization was directed from lateral prefrontal to superior posterior parietal cortex. Together, these findings provide causal evidence in support of a model where a frontal-parietal theta network prioritizes internally maintained representations and alpha oscillations in posterior parietal cortex suppress irrelevant representations. Significance Statement Control over internal representations requires the prioritization of relevant information and suppression of irrelevant information. We targeted theta-frequency frontal-parietal coherence and lateralized alpha oscillations in posterior parietal cortex using online rhythmic transcranial magnetic stimulation (TMS) in human participants while they prioritized or suppressed internally maintained working memory (WM) representations. For suppression, alpha-TMS to posterior parietal cortex increased the amplitude of lateralized alpha oscillations contralateral to the irrelevant visual field. For prioritization, theta-TMS to prefrontal cortex increased theta-frequency connectivity in the prefrontal-parietal network contralateral to the relevant visual field. In a separate dataset of patients with implanted electrodes, we demonstrate anatomical specificity in that theta connectivity was directed from lateral prefrontal to posterior parietal cortex.