Synchronous Theta Networks Characterize Successful Memory Retrieval

Memory retrieval activates regions across the brain, including not only the hippocampus and medial temporal lobe (MTL), but also frontal, parietal, and lateral temporal cortical regions. What remains unclear, however, is how these regions communicate to organize retrieval-specific processing. Here, we elucidate the role of theta (3-8 Hz) synchronization, broadly implicated in memory function, during the spontaneous retrieval of episodic memories. Analyzing a dataset of 382 neurosurgical patients (213 males, 168 females, and 1 unknown) implanted with intracranial electrodes who completed a free-recall task, we find that synchronous networks of theta phase synchrony span the brain in the moments before spontaneous recall, in comparison to periods of deliberation and incorrect recalls. Hubs of the retrieval network, which systematically synchronize with other regions, appear throughout the prefrontal cortex and lateral and medial temporal lobes, as well as other areas. Theta synchrony increases appear more prominently for slow (3 Hz) theta than for fast (8 Hz) theta in the recall-deliberation contrast, but not in the encoding or recall-intrusion contrasts, and theta power and synchrony correlate positively throughout the theta band. These results implicate diffuse brain-wide synchronization of theta rhythms, especially slow theta, in episodic memory retrieval.