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.

Eye movements support behavioral pattern completion

“…Finally, results of the accuracy model further revealed a significant positive relationship between the number of cumulative fixations made across the four study presentations of each image and accuracy on the recognition task. This finding is consistent with previous work linking encoding-related EMs to memory performance (47)(48)(49) and hippocampal activity (41), and further suggests that EMs during both encoding and retrieval reflect memory success.…”

Interoceptive insular cortex participates in sensory processing of gastrointestinal malaise and associated behaviors

“…In our work, most of the neurons that showed theta activity during LOB were classified as putative pyramidal neurons recorded from the deeper layers. Interestingly, most of the evidence suggests that theta is associated with exploration, for instance sniffing is temporally related with hippocampal theta rhythm 35 , as well theta is reflecting hippocampal and prefrontal-directed strategic control during exploratory choices 36 , 37 ; however, rats do not explore during LOB a behavioral proxy of GI malaise. In addition, LiCl reduces high frequency breathing, a main component of sniffing 28 .…”

Feedforward prediction error signals during episodic memory retrieval

“…6c) and greater coherence when compared to the repeated condition (t(7) = 2.33, p = 0.05). The involvement of low frequency coherence raises the possibility that low and high frequency activity may be coupled, as suggested by recent evidence demonstrating such interactions in the MTL during successful memory updating 21 . We did not observe significant changes in theta-or alpha-high frequency coupling in the MTL across conditions ( Supplementary Fig.…”