Evidence for immediate enhancement of hippocampal memory encoding by network-targeted theta-burst stimulation during concurrent fMRI

Molly S. Hermiller*, Yu Fen Chen, Todd B. Parrish, Joel L. Voss

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

62 Scopus citations

Abstract

The hippocampus supports episodic memory via interaction with a distributed brain network. Previous experiments using network-targeted noninvasive brain stimulation have identified episodic memory enhancements and modulation of activity within the hippocampal network. However, mechanistic insights were limited because these effects were measured long after stimulation and therefore could have reflected various neuroplastic aftereffects with extended time courses. In this experiment with human subjects of both sexes, we tested for immediate stimulation impact on encoding-related activity of the hippocampus and immediately adjacent medial-temporal cortex by delivering theta-burst transcranial magnetic stimulation (TBS) concurrent with fMRI, as an immediate impact of stimulation would suggest an influence on neural activity. We reasoned that TBS would be particularly effective for influencing the hippocampus because rhythmic neural activity in the theta band is associated with hippocampal memory processing. First, we demonstrated that it is possible to obtain robust fMRI correlates of task-related activity during concurrent TBS. We then identified immediate effects of TBS on encoding of visual scenes. Brief volleys of TBS targeting the hippocampal network increased activity of the targeted (left) hippocampus during scene encoding and increased subsequent recollection. Stimulation did not influence activity during an intermixed numerical task with no memory demand. Control conditions using beta band and out-of-network stimulation also did not influence hippocampal activity or recollection. TBS targeting the hippocampal network therefore immediately impacted hippocampal memory processing. This suggests direct, beneficial influence of stimulation on hippocampal neural activity related to memory and supports the role of theta-band activity in human episodic memory.

Original languageEnglish (US)
Pages (from-to)7155-7168
Number of pages14
JournalJournal of Neuroscience
Volume40
Issue number37
DOIs
StatePublished - Sep 9 2020

Funding

This work was supported by National Institute of Mental Health R01-MH106512 and R01-MH111790, and National Institute of Neurological Disorders and Stroke T32-NS047987 and F31-NS111892. This work was supported in part through the computational resources and staff contributions provided for Quest, the high-performance computing facility at Northwestern University, which is jointly supported by the Office of the Provost, the Office for Research, and Northwestern University Information Technology. Neuroimaging was performed at the Northwestern University Center for Translational Imaging, supported by Northwestern University Department of Radiology. The content is solely the responsibility of the authors and does not necessarily represent the official view of the National Institutes of Health. We thank Rachael A. Young and Stephen VanHaerents for contributing to data collection; and Plochman, Inc. for providing premium mustard. Correspondence should be addressed to Molly S. Hermiller at [email protected]. https://doi.org/10.1523/JNEUROSCI.0486-20.2020 Copyright © 2020 the authors

Keywords

  • Hippocampus
  • Memory
  • Noninvasive stimulation
  • Recollection
  • Simultaneous TMS/fMRI
  • Theta-burst

ASJC Scopus subject areas

  • General Neuroscience

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