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Rapid modulation of striatal cholinergic interneurons and dopamine release by satellite astrocytes

Author

Listed:
  • Jeffrey Stedehouder

    (University of Oxford
    University of Oxford)

  • Bradley M. Roberts

    (University of Oxford
    University of Oxford)

  • Shinil Raina

    (University of Oxford
    University of Oxford
    Aligning Science Across Parkinson’s (ASAP) Collaborative Research Network)

  • Simon Bossi

    (University of Oxford
    University of Oxford
    Aligning Science Across Parkinson’s (ASAP) Collaborative Research Network)

  • Alan King Lun Liu

    (University of Oxford
    University of Oxford)

  • Natalie M. Doig

    (Aligning Science Across Parkinson’s (ASAP) Collaborative Research Network
    University of Oxford)

  • Kevin McGerty

    (University of Oxford)

  • Peter J. Magill

    (University of Oxford
    Aligning Science Across Parkinson’s (ASAP) Collaborative Research Network
    University of Oxford)

  • Laura Parkkinen

    (University of Oxford
    University of Oxford)

  • Stephanie J. Cragg

    (University of Oxford
    University of Oxford
    Aligning Science Across Parkinson’s (ASAP) Collaborative Research Network)

Abstract

Astrocytes are increasingly appreciated to possess underestimated and important roles in modulating neuronal circuits. Astrocytes in striatum can regulate dopamine transmission by governing the extracellular tone of axonal neuromodulators, including GABA and adenosine. However, here we reveal that striatal astrocytes occupy a cell type-specific anatomical and functional relationship with cholinergic interneurons (ChIs), through which they rapidly excite ChIs and govern dopamine release via nicotinic acetylcholine receptors on subsecond timescales. We identify that ChI somata are in unexpectedly close proximity to astrocyte somata, in mouse and human, forming a “soma-to-soma” satellite-like configuration not typically observed for other striatal neurons. We find that transient depolarization of astrocytes in mouse striatum reversibly regulates ChI excitability by decreasing extracellular calcium. These findings reveal a privileged satellite astrocyte-interneuron interaction for striatal ChIs operating on subsecond timescales via regulation of extracellular calcium dynamics to shape downstream striatal circuit activity and dopamine signaling.

Suggested Citation

  • Jeffrey Stedehouder & Bradley M. Roberts & Shinil Raina & Simon Bossi & Alan King Lun Liu & Natalie M. Doig & Kevin McGerty & Peter J. Magill & Laura Parkkinen & Stephanie J. Cragg, 2024. "Rapid modulation of striatal cholinergic interneurons and dopamine release by satellite astrocytes," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-54253-7
    DOI: 10.1038/s41467-024-54253-7
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    References listed on IDEAS

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    1. Philip Hasel & Owen Dando & Zoeb Jiwaji & Paul Baxter & Alison C. Todd & Samuel Heron & Nóra M. Márkus & Jamie McQueen & David W. Hampton & Megan Torvell & Sachin S. Tiwari & Sean McKay & Abel Eraso-P, 2017. "Neurons and neuronal activity control gene expression in astrocytes to regulate their development and metabolism," Nature Communications, Nature, vol. 8(1), pages 1-18, August.
    2. Bradley M. Roberts & Natalie M. Doig & Katherine R. Brimblecombe & Emanuel F. Lopes & Ruth E. Siddorn & Sarah Threlfell & Natalie Connor-Robson & Nora Bengoa-Vergniory & Nicholas Pasternack & Richard , 2020. "GABA uptake transporters support dopamine release in dorsal striatum with maladaptive downregulation in a parkinsonism model," Nature Communications, Nature, vol. 11(1), pages 1-17, December.
    3. Tara Deemyad & Joel Lüthi & Nelson Spruston, 2018. "Astrocytes integrate and drive action potential firing in inhibitory subnetworks," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    4. Arne Battefeld & Jan Klooster & Maarten H. P. Kole, 2016. "Myelinating satellite oligodendrocytes are integrated in a glial syncytium constraining neuronal high-frequency activity," Nature Communications, Nature, vol. 7(1), pages 1-13, September.
    5. J. A. Gomez & J. M. Perkins & G. M. Beaudoin & N. B. Cook & S. A. Quraishi & E. A. Szoeke & K. Thangamani & C. W. Tschumi & M. J. Wanat & A. M. Maroof & M. J. Beckstead & P. A. Rosenberg & C. A. Palad, 2019. "Ventral tegmental area astrocytes orchestrate avoidance and approach behavior," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    6. Mark D. Condon & Nicola J. Platt & Yan-Feng Zhang & Bradley M. Roberts & Michael A. Clements & Stefania Vietti-Michelina & Min-Yee Tseu & Katherine R. Brimblecombe & Sarah Threlfell & Edward O. Mann &, 2019. "Plasticity in striatal dopamine release is governed by release-independent depression and the dopamine transporter," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    7. Yihui Cui & Yan Yang & Zheyi Ni & Yiyan Dong & Guohong Cai & Alexandre Foncelle & Shuangshuang Ma & Kangning Sang & Siyang Tang & Yuezhou Li & Ying Shen & Hugues Berry & Shengxi Wu & Hailan Hu, 2018. "Astroglial Kir4.1 in the lateral habenula drives neuronal bursts in depression," Nature, Nature, vol. 554(7692), pages 323-327, February.
    8. Matthijs C. Dorst & Anna Tokarska & Ming Zhou & Kwang Lee & Stefanos Stagkourakis & Christian Broberger & Sotiris Masmanidis & Gilad Silberberg, 2020. "Polysynaptic inhibition between striatal cholinergic interneurons shapes their network activity patterns in a dopamine-dependent manner," Nature Communications, Nature, vol. 11(1), pages 1-17, December.
    9. N. Lozovaya & S. Eftekhari & R. Cloarec & L. A. Gouty-Colomer & A. Dufour & B. Riffault & M. Billon-Grand & A. Pons-Bennaceur & N. Oumar & N. Burnashev & Y. Ben-Ari & C. Hammond, 2018. "GABAergic inhibition in dual-transmission cholinergic and GABAergic striatal interneurons is abolished in Parkinson disease," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
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