IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-39497-z.html
   My bibliography  Save this article

Striatal cholinergic interneuron membrane voltage tracks locomotor rhythms in mice

Author

Listed:
  • Sanaya N. Shroff

    (Boston University)

  • Eric Lowet

    (Boston University)

  • Sudiksha Sridhar

    (Boston University)

  • Howard J. Gritton

    (Boston University
    University of Illinois at Urbana-Champaign)

  • Mohammed Abumuaileq

    (Boston University)

  • Hua-An Tseng

    (Boston University)

  • Cyrus Cheung

    (Boston University)

  • Samuel L. Zhou

    (Boston University)

  • Krishnakanth Kondabolu

    (Boston University)

  • Xue Han

    (Boston University)

Abstract

Rhythmic neural network activity has been broadly linked to behavior. However, it is unclear how membrane potentials of individual neurons track behavioral rhythms, even though many neurons exhibit pace-making properties in isolated brain circuits. To examine whether single-cell voltage rhythmicity is coupled to behavioral rhythms, we focused on delta-frequencies (1–4 Hz) that are known to occur at both the neural network and behavioral levels. We performed membrane voltage imaging of individual striatal neurons simultaneously with network-level local field potential recordings in mice during voluntary movement. We report sustained delta oscillations in the membrane potentials of many striatal neurons, particularly cholinergic interneurons, which organize spikes and network oscillations at beta-frequencies (20–40 Hz) associated with locomotion. Furthermore, the delta-frequency patterned cellular dynamics are coupled to animals’ stepping cycles. Thus, delta-rhythmic cellular dynamics in cholinergic interneurons, known for their autonomous pace-making capabilities, play an important role in regulating network rhythmicity and movement patterning.

Suggested Citation

  • Sanaya N. Shroff & Eric Lowet & Sudiksha Sridhar & Howard J. Gritton & Mohammed Abumuaileq & Hua-An Tseng & Cyrus Cheung & Samuel L. Zhou & Krishnakanth Kondabolu & Xue Han, 2023. "Striatal cholinergic interneuron membrane voltage tracks locomotor rhythms in mice," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39497-z
    DOI: 10.1038/s41467-023-39497-z
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-39497-z
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-39497-z?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. Edward A. Stern & Dieter Jaeger & Charles J. Wilson, 1998. "Membrane potential synchrony of simultaneously recorded striatal spiny neurons in vivo," Nature, Nature, vol. 394(6692), pages 475-478, July.
    2. Kiryl D. Piatkevich & Seth Bensussen & Hua-an Tseng & Sanaya N. Shroff & Violeta Gisselle Lopez-Huerta & Demian Park & Erica E. Jung & Or A. Shemesh & Christoph Straub & Howard J. Gritton & Michael F., 2019. "Population imaging of neural activity in awake behaving mice," Nature, Nature, vol. 574(7778), pages 413-417, October.
    3. Mark M. Churchland & John P. Cunningham & Matthew T. Kaufman & Justin D. Foster & Paul Nuyujukian & Stephen I. Ryu & Krishna V. Shenoy, 2012. "Neural population dynamics during reaching," Nature, Nature, vol. 487(7405), pages 51-56, July.
    4. M. W. Howe & D. A. Dombeck, 2016. "Rapid signalling in distinct dopaminergic axons during locomotion and reward," Nature, Nature, vol. 535(7613), pages 505-510, July.
    5. J. Ito & S. Roy & Y. Liu & Y. Cao & M. Fletcher & L. Lu & J.D. Boughter & S. Grün & D.H. Heck, 2014. "Whisker barrel cortex delta oscillations and gamma power in the awake mouse are linked to respiration," Nature Communications, Nature, vol. 5(1), pages 1-10, May.
    6. Britton A. Sauerbrei & Jian-Zhong Guo & Jeremy D. Cohen & Matteo Mischiati & Wendy Guo & Mayank Kabra & Nakul Verma & Brett Mensh & Kristin Branson & Adam W. Hantman, 2020. "Cortical pattern generation during dexterous movement is input-driven," Nature, Nature, vol. 577(7790), pages 386-391, January.
    Full references (including those not matched with items on IDEAS)

    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. Eric A. Kirk & Keenan T. Hope & Samuel J. Sober & Britton A. Sauerbrei, 2024. "An output-null signature of inertial load in motor cortex," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    2. John N. J. Reynolds & Riccardo Avvisati & Paul D. Dodson & Simon D. Fisher & Manfred J. Oswald & Jeffery R. Wickens & Yan-Feng Zhang, 2022. "Coincidence of cholinergic pauses, dopaminergic activation and depolarisation of spiny projection neurons drives synaptic plasticity in the striatum," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    3. Harman Ghuman & Kyungsoo Kim & Sapeeda Barati & Karunesh Ganguly, 2023. "Emergence of task-related spatiotemporal population dynamics in transplanted neurons," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    4. Shan Yu & Andreas Klaus & Hongdian Yang & Dietmar Plenz, 2014. "Scale-Invariant Neuronal Avalanche Dynamics and the Cut-Off in Size Distributions," PLOS ONE, Public Library of Science, vol. 9(6), pages 1-12, June.
    5. Ian S Howard & David W Franklin, 2015. "Neural Tuning Functions Underlie Both Generalization and Interference," PLOS ONE, Public Library of Science, vol. 10(6), pages 1-21, June.
    6. Pierre O. Boucher & Tian Wang & Laura Carceroni & Gary Kane & Krishna V. Shenoy & Chandramouli Chandrasekaran, 2023. "Initial conditions combine with sensory evidence to induce decision-related dynamics in premotor cortex," Nature Communications, Nature, vol. 14(1), pages 1-28, December.
    7. Anthony Renard & Evan R. Harrell & Brice Bathellier, 2022. "Olfactory modulation of barrel cortex activity during active whisking and passive whisker stimulation," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    8. Adrian M Haith & David M Huberdeau & John W Krakauer, 2015. "Hedging Your Bets: Intermediate Movements as Optimal Behavior in the Context of an Incomplete Decision," PLOS Computational Biology, Public Library of Science, vol. 11(3), pages 1-21, March.
    9. Nozomu H. Nakamura & Hidemasa Furue & Kenta Kobayashi & Yoshitaka Oku, 2023. "Hippocampal ensemble dynamics and memory performance are modulated by respiration during encoding," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    10. Nir Even-Chen & Blue Sheffer & Saurabh Vyas & Stephen I Ryu & Krishna V Shenoy, 2019. "Structure and variability of delay activity in premotor cortex," PLOS Computational Biology, Public Library of Science, vol. 15(2), pages 1-17, February.
    11. Josh Merel & Donald M Pianto & John P Cunningham & Liam Paninski, 2015. "Encoder-Decoder Optimization for Brain-Computer Interfaces," PLOS Computational Biology, Public Library of Science, vol. 11(6), pages 1-25, June.
    12. Hagai Lalazar & L F Abbott & Eilon Vaadia, 2016. "Tuning Curves for Arm Posture Control in Motor Cortex Are Consistent with Random Connectivity," PLOS Computational Biology, Public Library of Science, vol. 12(5), pages 1-27, May.
    13. Ayaka Kato & Kenji Morita, 2016. "Forgetting in Reinforcement Learning Links Sustained Dopamine Signals to Motivation," PLOS Computational Biology, Public Library of Science, vol. 12(10), pages 1-41, October.
    14. Zhenrui Liao & Kevin C. Gonzalez & Deborah M. Li & Catalina M. Yang & Donald Holder & Natalie E. McClain & Guofeng Zhang & Stephen W. Evans & Mariya Chavarha & Jane Simko & Christopher D. Makinson & M, 2024. "Functional architecture of intracellular oscillations in hippocampal dendrites," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    15. Vincent Paget-Blanc & Marlene E. Pfeffer & Marie Pronot & Paul Lapios & Maria-Florencia Angelo & Roman Walle & Fabrice P. Cordelières & Florian Levet & Stéphane Claverol & Sabrina Lacomme & Mélina Pet, 2022. "A synaptomic analysis reveals dopamine hub synapses in the mouse striatum," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    16. Daniel S. Kluger & Carina Forster & Omid Abbasi & Nikos Chalas & Arno Villringer & Joachim Gross, 2023. "Modulatory dynamics of periodic and aperiodic activity in respiration-brain coupling," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    17. Edward A. B. Horrocks & Fabio R. Rodrigues & Aman B. Saleem, 2024. "Flexible neural population dynamics govern the speed and stability of sensory encoding in mouse visual cortex," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
    18. Benjamin R Cowley & Matthew A Smith & Adam Kohn & Byron M Yu, 2016. "Stimulus-Driven Population Activity Patterns in Macaque Primary Visual Cortex," PLOS Computational Biology, Public Library of Science, vol. 12(12), pages 1-31, December.
    19. A. Barri & M. T. Wiechert & M. Jazayeri & D. A. DiGregorio, 2022. "Synaptic basis of a sub-second representation of time in a neural circuit model," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    20. Tianwei Wang & Yun Chen & Yiheng Zhang & He Cui, 2024. "Multiplicative joint coding in preparatory activity for reaching sequence in macaque motor cortex," Nature Communications, Nature, vol. 15(1), pages 1-15, 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:14:y:2023:i:1:d:10.1038_s41467-023-39497-z. 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.