Theta-Alpha Oscillations Bind the Hippocampus, Prefrontal Cortex, and Striatum during Recollection: Evidence from Simultaneous EEG-fMRI

Recollection of contextual information represents the core of human recognition memory. It has been associated with theta (4-8 Hz) power in electrophysiological recordings and, independently, with BOLD effects in a network including the hippocampus and frontal cortex. Although the notion of the hippocampus coordinating neocortical activity by synchronization in the theta range is common among theoretical models of recollection, direct evidence supporting this hypothesis is scarce. To address this apparent gap in our understanding of memory processes, we combined EEG and fMRI during a remember/know recognition task. We can show that recollection-specific theta-alpha (4-13 Hz) effects are correlated with increases in hippocampal connectivity with the PFC and, importantly, the striatum, areas that have been linked repeatedly to retrieval success. Together, our results provide compelling evidence that low-frequency oscillations in the theta and alpha range provide a mechanism to functionally bind the hippocampus, PFC, and striatum during successful recollection.

Significance statement: Low-frequency oscillations are supposed to drive the binding of information across a large-scale network centered on the hippocampus, which supports mnemonic functions. The electrophysiological means to investigate this phenomenon in humans (EEG/MEG), however, are inherently limited by their spatial resolution and therefore do not allow a precise localization of the brain regions involved. By combining EEG with BOLD-derived estimates of hippocampal connectivity during recognition, we can identify the striatum and specific areas in the medial and lateral PFC as part of a circuit linked to low-frequency oscillations (4-13 Hz) that promotes hippocampus-dependent context retrieval. Therefore, the current study closes an apparent gap in our understanding of the network dynamics of memory retrieval.