Synchronous theta networks characterize successful memory retrieval
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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. How these regions communicate to organize retrieval-specific processing, however, remains unclear. 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 413 neurosurgical patients 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. Network hubs, which systematically synchronize with other regions, appear throughout the prefrontal cortex and lateral and medial temporal lobes, as well as other areas. The recall accuracy network, derived from a correct recall–intrusion contrast, includes synchronous hubs concentrated in the temporal lobe and desynchronous hubs in the parietal lobe. 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 contrast, and theta power and synchrony positively correlate throughout the theta band. These results implicate diffuse brain-wide synchronization of theta rhythms, especially slow theta, in episodic memory retrieval.
Significance Statement
Analyzing intracranial recordings from 413 subjects who completed an episodic free recall experiment, we analyze the brain-wide theta synchrony effects of memory retrieval. The literature has not previously described the whole-brain regional distribution of these effects nor studied them with respect to intrusions. We show that synchronous medial temporal hubs and desynchronous parietal hubs mark the recall accuracy network, and that theta synchrony in the successful encoding, successful retrieval, and recall accuracy contrasts correlates positively with theta power increases at a region. These findings significantly advance our understanding of the role and localization of theta synchrony effects during human memory retrieval.