IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-33507-2.html
   My bibliography  Save this article

Behaviourally modulated hippocampal theta oscillations in the ferret persist during both locomotion and immobility

Author

Listed:
  • Soraya L. S. Dunn

    (University College London
    University College London)

  • Stephen M. Town

    (University College London)

  • Jennifer K. Bizley

    (University College London)

  • Daniel Bendor

    (University College London)

Abstract

Theta oscillations are a hallmark of hippocampal activity across mammals and play a critical role in many hippocampal models of memory and spatial navigation. To reconcile the cross-species differences observed in the presence and properties of theta, we recorded hippocampal local field potentials in rats and ferrets during auditory and visual localisation tasks designed to vary locomotion and sensory attention. Here, we show that theta oscillations occur during locomotion in both ferrets and rats, however during periods of immobility, theta oscillations persist in the ferret, contrasting starkly with the switch to large irregular activity (LIA) in the rat. Theta during immobility in the ferret is identified as analogous to Type 2 theta that has been observed in rodents due to its sensitivity to atropine, and is modulated by behavioural state with the strongest theta observed during reward epochs. These results demonstrate that even under similar behavioural conditions, differences exist between species in the relationship between theta and behavioural state.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33507-2
    DOI: 10.1038/s41467-022-33507-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-33507-2
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-33507-2?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Michael M. Yartsev & Menno P. Witter & Nachum Ulanovsky, 2011. "Grid cells without theta oscillations in the entorhinal cortex of bats," Nature, Nature, vol. 479(7371), pages 103-107, November.
    2. Katherine C. Wood & Stephen M. Town & Jennifer K. Bizley, 2019. "Neurons in primary auditory cortex represent sound source location in a cue-invariant manner," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    3. Torkel Hafting & Marianne Fyhn & Sturla Molden & May-Britt Moser & Edvard I. Moser, 2005. "Microstructure of a spatial map in the entorhinal cortex," Nature, Nature, vol. 436(7052), pages 801-806, August.
    4. 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.
    5. Bates, Douglas & Mächler, Martin & Bolker, Ben & Walker, Steve, 2015. "Fitting Linear Mixed-Effects Models Using lme4," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 67(i01).
    6. Berens, Philipp, 2009. "CircStat: A MATLAB Toolbox for Circular Statistics," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 31(i10).
    7. Natalia Grion & Athena Akrami & Yangfang Zuo & Federico Stella & Mathew E Diamond, 2016. "Coherence between Rat Sensorimotor System and Hippocampus Is Enhanced during Tactile Discrimination," PLOS Biology, Public Library of Science, vol. 14(2), pages 1-26, February.
    8. Véronique D. Bohbot & Milagros S. Copara & Jean Gotman & Arne D. Ekstrom, 2017. "Low-frequency theta oscillations in the human hippocampus during real-world and virtual navigation," Nature Communications, Nature, vol. 8(1), pages 1-7, April.
    9. Iain Stitt & Zhe Charles Zhou & Susanne Radtke-Schuller & Flavio Fröhlich, 2018. "Arousal dependent modulation of thalamo-cortical functional interaction," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. 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.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Davide Spalla & Alessandro Treves & Charlotte N. Boccara, 2022. "Angular and linear speed cells in the parahippocampal circuits," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    2. 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.
    3. Jennifer B Tennessen & Marla M Holt & Brianna M Wright & M Bradley Hanson & Candice K Emmons & Deborah A Giles & Jeffrey T Hogan & Sheila J Thornton & Volker B Deecke, 2023. "Divergent foraging strategies between populations of sympatric matrilineal killer whales," Behavioral Ecology, International Society for Behavioral Ecology, vol. 34(3), pages 373-386.
    4. 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.
    5. Eric Reifenstein & Martin Stemmler & Andreas V M Herz & Richard Kempter & Susanne Schreiber, 2014. "Movement Dependence and Layer Specificity of Entorhinal Phase Precession in Two-Dimensional Environments," PLOS ONE, Public Library of Science, vol. 9(6), pages 1-11, June.
    6. Tiziano D’Albis & Richard Kempter, 2017. "A single-cell spiking model for the origin of grid-cell patterns," PLOS Computational Biology, Public Library of Science, vol. 13(10), pages 1-41, October.
    7. Benjamin Dunn & Maria Mørreaunet & Yasser Roudi, 2015. "Correlations and Functional Connections in a Population of Grid Cells," PLOS Computational Biology, Public Library of Science, vol. 11(2), pages 1-21, February.
    8. 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.
    9. JANSSENS, Jochen & DE CORTE, Annelies & SÖRENSEN, Kenneth, 2016. "Water distribution network design optimisation with respect to reliability," Working Papers 2016007, University of Antwerp, Faculty of Business and Economics.
    10. Raymond Hernandez & Elizabeth A. Pyatak & Cheryl L. P. Vigen & Haomiao Jin & Stefan Schneider & Donna Spruijt-Metz & Shawn C. Roll, 2021. "Understanding Worker Well-Being Relative to High-Workload and Recovery Activities across a Whole Day: Pilot Testing an Ecological Momentary Assessment Technique," IJERPH, MDPI, vol. 18(19), pages 1-17, October.
    11. Elisabeth Beckmann & Lukas Olbrich & Joseph Sakshaug, 2024. "Multivariate assessment of interviewer-related errors in a cross-national economic survey (Lukas Olbrich, Elisabeth Beckmann, Joseph W. Sakshaug)," Working Papers 253, Oesterreichische Nationalbank (Austrian Central Bank).
    12. Valentina Krenz & Arjen Alink & Tobias Sommer & Benno Roozendaal & Lars Schwabe, 2023. "Time-dependent memory transformation in hippocampus and neocortex is semantic in nature," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    13. Morán-Ordóñez, Alejandra & Ameztegui, Aitor & De Cáceres, Miquel & de-Miguel, Sergio & Lefèvre, François & Brotons, Lluís & Coll, Lluís, 2020. "Future trade-offs and synergies among ecosystem services in Mediterranean forests under global change scenarios," Ecosystem Services, Elsevier, vol. 45(C).
    14. Damian M. Herz & Manuel Bange & Gabriel Gonzalez-Escamilla & Miriam Auer & Keyoumars Ashkan & Petra Fischer & Huiling Tan & Rafal Bogacz & Muthuraman Muthuraman & Sergiu Groppa & Peter Brown, 2022. "Dynamic control of decision and movement speed in the human basal ganglia," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    15. Dongyan Liu & Chongran Zhou & John K. Keesing & Oscar Serrano & Axel Werner & Yin Fang & Yingjun Chen & Pere Masque & Janine Kinloch & Aleksey Sadekov & Yan Du, 2022. "Wildfires enhance phytoplankton production in tropical oceans," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    16. Zhaogeng Yang & Yanhui Li & Peijin Hu & Jun Ma & Yi Song, 2020. "Prevalence of Anemia and its Associated Factors among Chinese 9-, 12-, and 14-Year-Old Children: Results from 2014 Chinese National Survey on Students Constitution and Health," IJERPH, MDPI, vol. 17(5), pages 1-10, February.
    17. Marco Lopez-Cruz & Fernando M. Aguate & Jacob D. Washburn & Natalia Leon & Shawn M. Kaeppler & Dayane Cristina Lima & Ruijuan Tan & Addie Thompson & Laurence Willard Bretonne & Gustavo los Campos, 2023. "Leveraging data from the Genomes-to-Fields Initiative to investigate genotype-by-environment interactions in maize in North America," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    18. Baumann, Elias & Kern, Jana & Lessmann, Stefan, 2019. "Usage Continuance in Software-as-a-Service," IRTG 1792 Discussion Papers 2019-005, Humboldt University of Berlin, International Research Training Group 1792 "High Dimensional Nonstationary Time Series".
    19. repec:cup:judgdm:v:16:y:2021:i:1:p:201-237 is not listed on IDEAS
    20. C. Gabriel Hidalgo Pizango & Eurídice N. Honorio Coronado & Jhon del Águila-Pasquel & Gerardo Flores Llampazo & Johan de Jong & César J. Córdova Oroche & José M. Reyna Huaymacari & Steve J. Carver & D, 2022. "Sustainable palm fruit harvesting as a pathway to conserve Amazon peatland forests," Nature Sustainability, Nature, vol. 5(6), pages 479-487, June.
    21. 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.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33507-2. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.