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Lateralized hippocampal oscillations underlie distinct aspects of human spatial memory and navigation

Author

Listed:
  • Jonathan Miller

    (Columbia University)

  • Andrew J. Watrous

    (Columbia University)

  • Melina Tsitsiklis

    (Columbia University)

  • Sang Ah Lee

    (Korea Advanced Institute of Science and Technology)

  • Sameer A. Sheth

    (Baylor College of Medicine)

  • Catherine A. Schevon

    (Columbia University Medical Center)

  • Elliot H. Smith

    (Columbia University Medical Center)

  • Michael R. Sperling

    (Thomas Jefferson University)

  • Ashwini Sharan

    (Thomas Jefferson University)

  • Ali Akbar Asadi-Pooya

    (Thomas Jefferson University
    Shiraz University of Medical Sciences)

  • Gregory A. Worrell

    (Mayo Clinic)

  • Stephen Meisenhelter

    (Geisel School of Medicine at Dartmouth)

  • Cory S. Inman

    (Emory University School of Medicine)

  • Kathryn A. Davis

    (Hospital of the University of Pennsylvania)

  • Bradley Lega

    (University of Texas–Southwestern)

  • Paul A. Wanda

    (University of Pennsylvania)

  • Sandhitsu R. Das

    (Hospital of the University of Pennsylvania)

  • Joel M. Stein

    (Hospital of the University of Pennsylvania)

  • Richard Gorniak

    (Thomas Jefferson University)

  • Joshua Jacobs

    (Columbia University)

Abstract

The hippocampus plays a vital role in various aspects of cognition including both memory and spatial navigation. To understand electrophysiologically how the hippocampus supports these processes, we recorded intracranial electroencephalographic activity from 46 neurosurgical patients as they performed a spatial memory task. We measure signals from multiple brain regions, including both left and right hippocampi, and we use spectral analysis to identify oscillatory patterns related to memory encoding and navigation. We show that in the left but not right hippocampus, the amplitude of oscillations in the 1–3-Hz “low theta” band increases when viewing subsequently remembered object–location pairs. In contrast, in the right but not left hippocampus, low-theta activity increases during periods of navigation. The frequencies of these hippocampal signals are slower than task-related signals in the neocortex. These results suggest that the human brain includes multiple lateralized oscillatory networks that support different aspects of cognition.

Suggested Citation

  • Jonathan Miller & Andrew J. Watrous & Melina Tsitsiklis & Sang Ah Lee & Sameer A. Sheth & Catherine A. Schevon & Elliot H. Smith & Michael R. Sperling & Ashwini Sharan & Ali Akbar Asadi-Pooya & Gregor, 2018. "Lateralized hippocampal oscillations underlie distinct aspects of human spatial memory and navigation," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:9:y:2018:i:1:d:10.1038_s41467-018-04847-9
    DOI: 10.1038/s41467-018-04847-9
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    Cited by:

    1. Isabella C. Wagner & Luise P. Graichen & Boryana Todorova & Andre Lüttig & David B. Omer & Matthias Stangl & Claus Lamm, 2023. "Entorhinal grid-like codes and time-locked network dynamics track others navigating through space," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    2. Sabrina L. L. Maoz & Matthias Stangl & Uros Topalovic & Daniel Batista & Sonja Hiller & Zahra M. Aghajan & Barbara Knowlton & John Stern & Jean-Philippe Langevin & Itzhak Fried & Dawn Eliashiv & Nanth, 2023. "Dynamic neural representations of memory and space during human ambulatory navigation," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    3. Felippe Toledo & Fraser Carson, 2022. "Neurobiological Features of Posttraumatic Stress Disorder (PTSD) and Their Role in Understanding Adaptive Behavior and Stress Resilience," IJERPH, MDPI, vol. 19(16), pages 1-14, August.
    4. Lukas M. von Ziegler & Amalia Floriou-Servou & Rebecca Waag & Rebecca R. Gupta & Oliver Sturman & Katharina Gapp & Christina A. Maat & Tobias Kockmann & Han-Yu Lin & Sian N. Duss & Mattia Privitera & , 2022. "Multiomic profiling of the acute stress response in the mouse hippocampus," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    5. Thibault Cholvin & Marlene Bartos, 2022. "Hemisphere-specific spatial representation by hippocampal granule cells," Nature Communications, Nature, vol. 13(1), pages 1-14, December.

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