Hippocampal theta coordinates memory processing during visual exploration

Abstract

The hippocampus supports memory encoding and retrieval, with distinct phases of theta oscillations modulating the amplitude of gamma-band activity during each process. Encoding and retrieval operations dynamically interact over rapid timescales, especially when sensory information conflicts with memory. The ability to link hippocampal dynamics to specific memory-guided behaviors has been limited by experiments that lack the temporal resolution to segregate when encoding and retrieval occur. To resolve this issue, we simultaneously tracked eye movements and hippocampal field potentials while neurosurgical patients performed a spatial memory task. Novelty-driven fixations increased phase-locking to the theta rhythm, which predicted successful memory performance. Theta to gamma phase amplitude coupling increased during these viewing behaviors and predicted forgetting of conflicting memories. In contrast, theta phase-locking preceded fixations initiated by memory retrieval, indicating that the hippocampus coordinates memory-guided eye movements. These findings suggest that theta oscillations in the hippocampus support learning through two interleaved processes: strengthening the encoding of novel information and guiding exploration based on prior experience.