Cargando…

Functionally distinct high and low theta oscillations in the human hippocampus

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 fr...

Descripción completa

Detalles Bibliográficos
Autores principales: Goyal, Abhinav, Miller, Jonathan, Qasim, Salman E., Watrous, Andrew J., Zhang, Honghui, Stein, Joel M., Inman, Cory S., Gross, Robert E., Willie, Jon T., Lega, Bradley, Lin, Jui-Jui, Sharan, Ashwini, Wu, Chengyuan, Sperling, Michael R., Sheth, Sameer A., McKhann, Guy M., Smith, Elliot H., Schevon, Catherine, Jacobs, Joshua
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7235253/
https://www.ncbi.nlm.nih.gov/pubmed/32424312
http://dx.doi.org/10.1038/s41467-020-15670-6
_version_ 1783535925745156096
author Goyal, Abhinav
Miller, Jonathan
Qasim, Salman E.
Watrous, Andrew J.
Zhang, Honghui
Stein, Joel M.
Inman, Cory S.
Gross, Robert E.
Willie, Jon T.
Lega, Bradley
Lin, Jui-Jui
Sharan, Ashwini
Wu, Chengyuan
Sperling, Michael R.
Sheth, Sameer A.
McKhann, Guy M.
Smith, Elliot H.
Schevon, Catherine
Jacobs, Joshua
author_facet Goyal, Abhinav
Miller, Jonathan
Qasim, Salman E.
Watrous, Andrew J.
Zhang, Honghui
Stein, Joel M.
Inman, Cory S.
Gross, Robert E.
Willie, Jon T.
Lega, Bradley
Lin, Jui-Jui
Sharan, Ashwini
Wu, Chengyuan
Sperling, Michael R.
Sheth, Sameer A.
McKhann, Guy M.
Smith, Elliot H.
Schevon, Catherine
Jacobs, Joshua
author_sort Goyal, Abhinav
collection PubMed
description 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.
format Online
Article
Text
id pubmed-7235253
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-72352532020-05-20 Functionally distinct high and low theta oscillations in the human hippocampus Goyal, Abhinav Miller, Jonathan Qasim, Salman E. Watrous, Andrew J. Zhang, Honghui Stein, Joel M. Inman, Cory S. Gross, Robert E. Willie, Jon T. Lega, Bradley Lin, Jui-Jui Sharan, Ashwini Wu, Chengyuan Sperling, Michael R. Sheth, Sameer A. McKhann, Guy M. Smith, Elliot H. Schevon, Catherine Jacobs, Joshua Nat Commun Article 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. Nature Publishing Group UK 2020-05-18 /pmc/articles/PMC7235253/ /pubmed/32424312 http://dx.doi.org/10.1038/s41467-020-15670-6 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Goyal, Abhinav
Miller, Jonathan
Qasim, Salman E.
Watrous, Andrew J.
Zhang, Honghui
Stein, Joel M.
Inman, Cory S.
Gross, Robert E.
Willie, Jon T.
Lega, Bradley
Lin, Jui-Jui
Sharan, Ashwini
Wu, Chengyuan
Sperling, Michael R.
Sheth, Sameer A.
McKhann, Guy M.
Smith, Elliot H.
Schevon, Catherine
Jacobs, Joshua
Functionally distinct high and low theta oscillations in the human hippocampus
title Functionally distinct high and low theta oscillations in the human hippocampus
title_full Functionally distinct high and low theta oscillations in the human hippocampus
title_fullStr Functionally distinct high and low theta oscillations in the human hippocampus
title_full_unstemmed Functionally distinct high and low theta oscillations in the human hippocampus
title_short Functionally distinct high and low theta oscillations in the human hippocampus
title_sort functionally distinct high and low theta oscillations in the human hippocampus
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7235253/
https://www.ncbi.nlm.nih.gov/pubmed/32424312
http://dx.doi.org/10.1038/s41467-020-15670-6
work_keys_str_mv AT goyalabhinav functionallydistincthighandlowthetaoscillationsinthehumanhippocampus
AT millerjonathan functionallydistincthighandlowthetaoscillationsinthehumanhippocampus
AT qasimsalmane functionallydistincthighandlowthetaoscillationsinthehumanhippocampus
AT watrousandrewj functionallydistincthighandlowthetaoscillationsinthehumanhippocampus
AT zhanghonghui functionallydistincthighandlowthetaoscillationsinthehumanhippocampus
AT steinjoelm functionallydistincthighandlowthetaoscillationsinthehumanhippocampus
AT inmancorys functionallydistincthighandlowthetaoscillationsinthehumanhippocampus
AT grossroberte functionallydistincthighandlowthetaoscillationsinthehumanhippocampus
AT williejont functionallydistincthighandlowthetaoscillationsinthehumanhippocampus
AT legabradley functionallydistincthighandlowthetaoscillationsinthehumanhippocampus
AT linjuijui functionallydistincthighandlowthetaoscillationsinthehumanhippocampus
AT sharanashwini functionallydistincthighandlowthetaoscillationsinthehumanhippocampus
AT wuchengyuan functionallydistincthighandlowthetaoscillationsinthehumanhippocampus
AT sperlingmichaelr functionallydistincthighandlowthetaoscillationsinthehumanhippocampus
AT shethsameera functionallydistincthighandlowthetaoscillationsinthehumanhippocampus
AT mckhannguym functionallydistincthighandlowthetaoscillationsinthehumanhippocampus
AT smithellioth functionallydistincthighandlowthetaoscillationsinthehumanhippocampus
AT schevoncatherine functionallydistincthighandlowthetaoscillationsinthehumanhippocampus
AT jacobsjoshua functionallydistincthighandlowthetaoscillationsinthehumanhippocampus