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GPCR voltage dependence controls neuronal plasticity and behavior

Author

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  • Eyal Rozenfeld

    (Tel Aviv University
    Tel Aviv University)

  • Merav Tauber

    (The Open University of Israel)

  • Yair Ben-Chaim

    (The Open University of Israel)

  • Moshe Parnas

    (Tel Aviv University
    Tel Aviv University)

Abstract

G-protein coupled receptors (GPCRs) play a paramount role in diverse brain functions. Almost 20 years ago, GPCR activity was shown to be regulated by membrane potential in vitro, but whether the voltage dependence of GPCRs contributes to neuronal coding and behavioral output under physiological conditions in vivo has never been demonstrated. Here we show that muscarinic GPCR mediated neuronal potentiation in vivo is voltage dependent. This voltage dependent potentiation is abolished in mutant animals expressing a voltage independent receptor. Depolarization alone, without a muscarinic agonist, results in a nicotinic ionotropic receptor potentiation that is mediated by muscarinic receptor voltage dependency. Finally, muscarinic receptor voltage independence causes a strong behavioral effect of increased odor habituation. Together, this study identifies a physiological role for the voltage dependency of GPCRs by demonstrating crucial involvement of GPCR voltage dependence in neuronal plasticity and behavior. Thus, this study suggests that GPCR voltage dependency plays a role in many diverse neuronal functions including learning and memory.

Suggested Citation

  • Eyal Rozenfeld & Merav Tauber & Yair Ben-Chaim & Moshe Parnas, 2021. "GPCR voltage dependence controls neuronal plasticity and behavior," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-27593-x
    DOI: 10.1038/s41467-021-27593-x
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    References listed on IDEAS

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    1. A. J. Venkatakrishnan & Xavier Deupi & Guillaume Lebon & Christopher G. Tate & Gebhard F. Schertler & M. Madan Babu, 2013. "Molecular signatures of G-protein-coupled receptors," Nature, Nature, vol. 494(7436), pages 185-194, February.
    2. Yair Ben-Chaim & Baron Chanda & Nathan Dascal & Francisco Bezanilla & Itzchak Parnas & Hanna Parnas, 2006. "Movement of ‘gating charge’ is coupled to ligand binding in a G-protein-coupled receptor," Nature, Nature, vol. 444(7115), pages 106-109, November.
    3. Shawn R. Olsen & Rachel I. Wilson, 2008. "Lateral presynaptic inhibition mediates gain control in an olfactory circuit," Nature, Nature, vol. 452(7190), pages 956-960, April.
    4. Daniel M. Rosenbaum & Søren G. F. Rasmussen & Brian K. Kobilka, 2009. "The structure and function of G-protein-coupled receptors," Nature, Nature, vol. 459(7245), pages 356-363, May.
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    Cited by:

    1. Eyal Rozenfeld & Nadine Ehmann & Julia E. Manoim & Robert J. Kittel & Moshe Parnas, 2023. "Homeostatic synaptic plasticity rescues neural coding reliability," Nature Communications, Nature, vol. 14(1), pages 1-14, December.

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