Hippocampal theta coordinates memory processing during visual exploration

James E. Kragel*, Stephen Vanhaerents, Jessica W. Templer, Stephan Schuele, Joshua M. Rosenow, Aneesha S. Nilakantan, Donna J. Bridge

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

48 Scopus citations

Abstract

The hippocampus supports memory encoding and retrieval, which may occur at distinct phases of the theta cycle. These processes dynamically interact over rapid timescales, especially when sensory information conflicts with memory. The ability to link hippocampal dynamics to memory-guided behaviors has been limited by experiments that lack the temporal resolution to segregate encoding and retrieval. Here, we simultaneously tracked eye movements and hippocampal field potentials while neurosurgical patients performed a spatial memory task. Phase-locking at the peak of theta preceded fixations to retrieved locations, indicating that the hippocampus coordinates memory-guided eye movements. In contrast, phase-locking at the trough of theta followed fixations to novel object-locations and predicted intact memory of the original location. Theta-gamma phase amplitude coupling increased during fixations to conflicting visual content, but predicted memory updating. Hippocampal theta thus supports learning through two interleaved processes: strengthening encoding of novel information and guiding exploration based on prior experience.

Original languageEnglish (US)
Article numbere52108
JournaleLife
Volume9
DOIs
StatePublished - Mar 2020

Funding

We are grateful to Dr. Christina Zelano for helpful discussions, Irena Bellinski for assistance with patient recruitment, and the Laboratory of Human Neuroscience at Northwestern University for sharing resources; DJB acknowledges the support of NIH/National Institute of Mental Health (NIMH; grant R21MH115366) and National Center for Advancing Translational Sciences, Grant Number UL1TR001422. JEK was supported in part by National Institute of Neurological Disorders and Stroke grant T32NS047987.

ASJC Scopus subject areas

  • General Neuroscience
  • General Immunology and Microbiology
  • General Biochemistry, Genetics and Molecular Biology

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