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Functionally distinct high and low theta oscillations in the human hippocampus

Author

Listed:
  • Abhinav Goyal

    (Mayo Clinic College of Medicine and Science, Mayo Clinic)

  • Jonathan Miller

    (Columbia University)

  • Salman E. Qasim

    (Columbia University)

  • Andrew J. Watrous

    (University of Texas)

  • Honghui Zhang

    (Columbia University)

  • Joel M. Stein

    (University of Pennsylvania)

  • Cory S. Inman

    (Emory University)

  • Robert E. Gross

    (Emory University)

  • Jon T. Willie

    (Emory University)

  • Bradley Lega

    (University of Texas Southwestern)

  • Jui-Jui Lin

    (University of Texas Southwestern)

  • Ashwini Sharan

    (Thomas Jefferson University
    Thomas Jefferson University)

  • Chengyuan Wu

    (Thomas Jefferson University)

  • Michael R. Sperling

    (Thomas Jefferson University
    Thomas Jefferson University)

  • Sameer A. Sheth

    (Baylor College of Medicine)

  • Guy M. McKhann

    (Columbia University Medical Center)

  • Elliot H. Smith

    (University of Utah)

  • Catherine Schevon

    (Columbia University Medical Center)

  • Joshua Jacobs

    (Columbia University)

Abstract

Based on rodent models, researchers have theorized that the hippocampus supports episodic memory and navigation via the theta oscillation, a ~4–10 Hz rhythm that coordinates brain-wide neural activity. However, recordings from humans have indicated that hippocampal theta oscillations are lower in frequency and less prevalent than in rodents, suggesting interspecies differences in theta’s function. To characterize human hippocampal theta, we examine the properties of theta oscillations throughout the anterior–posterior length of the hippocampus as neurosurgical subjects performed a virtual spatial navigation task. During virtual movement, we observe hippocampal oscillations at multiple frequencies from 2 to 14 Hz. The posterior hippocampus prominently displays oscillations at ~8-Hz and the precise frequency of these oscillations correlates with the speed of movement, implicating these signals in spatial navigation. We also observe slower ~3 Hz oscillations, but these signals are more prevalent in the anterior hippocampus and their frequency does not vary with movement speed. Our results converge with recent findings to suggest an updated view of human hippocampal electrophysiology. Rather than one hippocampal theta oscillation with a single general role, high- and low-frequency theta oscillations, respectively, may reflect spatial and non-spatial cognitive processes.

Suggested Citation

  • Abhinav Goyal & Jonathan Miller & Salman E. Qasim & Andrew J. Watrous & Honghui Zhang & Joel M. Stein & Cory S. Inman & Robert E. Gross & Jon T. Willie & Bradley Lega & Jui-Jui Lin & Ashwini Sharan & , 2020. "Functionally distinct high and low theta oscillations in the human hippocampus," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
  • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-15670-6
    DOI: 10.1038/s41467-020-15670-6
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    Cited by:

    1. Marije ter Wal & Juan Linde-Domingo & Julia Lifanov & Frédéric Roux & Luca D. Kolibius & Stephanie Gollwitzer & Johannes Lang & Hajo Hamer & David Rollings & Vijay Sawlani & Ramesh Chelvarajah & Bernh, 2021. "Theta rhythmicity governs human behavior and hippocampal signals during memory-dependent tasks," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    2. Diego B. Piza & Benjamin W. Corrigan & Roberto A. Gulli & Sonia Carmo & A. Claudio Cuello & Lyle Muller & Julio Martinez-Trujillo, 2024. "Primacy of vision shapes behavioral strategies and neural substrates of spatial navigation in marmoset hippocampus," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    3. Soraya L. S. Dunn & Stephen M. Town & Jennifer K. Bizley & Daniel Bendor, 2022. "Behaviourally modulated hippocampal theta oscillations in the ferret persist during both locomotion and immobility," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    4. Dominik P. Koller & Michael Schirner & Petra Ritter, 2024. "Human connectome topology directs cortical traveling waves and shapes frequency gradients," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    5. Tamara Gedankien & Ryan Joseph Tan & Salman Ehtesham Qasim & Haley Moore & David McDonagh & Joshua Jacobs & Bradley Lega, 2023. "Acetylcholine modulates the temporal dynamics of human theta oscillations during memory," Nature Communications, Nature, vol. 14(1), pages 1-13, December.

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