To facilitate goal-directed actions, effective management of working memory (WM) is crucial, involving a hypothesized WM “gating mechanism.” We investigate the underlying neural basis through behavioral modeling and connectivity assessments between neuroanatomical regions linked to theta, alpha, and beta frequency bands. We found opposing, threshold-dependent mechanisms governing WM gate opening and closing. Directed beta band connectivity in the parieto-frontal and parahippocampal-occipital networks was crucial for threshold-dependent WM gating dynamics. Fronto-parahippocampal connectivity in the theta band was also notable for both gating processes, although weaker than that in the beta band. Distinct roles for theta, beta, and alpha bands emerge in maintaining information in WM and shielding against interference, whereby alpha band activity likely acts as a “gatekeeper” supporting processes reflected by beta and theta band activity. The study shows that the decision criterion for WM gate opening/closing relies on concerted interplay within neuroanatomical networks defined by beta and theta band activities.