A chemogenetic approach for dopamine imaging with tunable sensitivity

Marie A. Labouesse, Maria Wilhelm, Zacharoula Kagiampaki, Andrew G. Yee, Raphaelle Denis, Masaya Harada, Andrea Gresch, Alina-Măriuca Marinescu, Kanako Otomo, Sebastiano Curreli, Laia Serratosa Capdevila, Xuehan Zhou, Reto B. Cola, Luca Ravotto, Chaim Glück, Stanislav Cherepanov, Bruno Weber, Xin Zhou, Jason Katner, Kjell A. Svensson, Tommaso Fellin, Louis-Eric Trudeau, Christopher P. Ford, Yaroslav Sych and Tommaso Patriarchi ()
Additional contact information
Marie A. Labouesse: University of Zürich
Maria Wilhelm: University of Zürich
Zacharoula Kagiampaki: University of Zürich
Andrew G. Yee: University of Colorado School of Medicine
Raphaelle Denis: Université de Montréal
Masaya Harada: University of Zürich
Andrea Gresch: University of Zürich
Alina-Măriuca Marinescu: ETH Zürich
Kanako Otomo: ETH Zürich
Sebastiano Curreli: Istituto Italiano di Tecnologia
Laia Serratosa Capdevila: University of Zürich
Xuehan Zhou: University of Zürich
Reto B. Cola: University of Zürich
Luca Ravotto: University of Zürich
Chaim Glück: University of Zürich
Stanislav Cherepanov: University of Strasbourg
Bruno Weber: University of Zürich
Xin Zhou: Eli Lilly and Company
Jason Katner: Eli Lilly and Company
Kjell A. Svensson: Eli Lilly and Company
Tommaso Fellin: Istituto Italiano di Tecnologia
Louis-Eric Trudeau: Université de Montréal
Christopher P. Ford: University of Colorado School of Medicine
Yaroslav Sych: University of Strasbourg
Tommaso Patriarchi: University of Zürich

Nature Communications, 2024, vol. 15, issue 1, 1-22

Abstract: Abstract Genetically-encoded dopamine (DA) sensors enable high-resolution imaging of DA release, but their ability to detect a wide range of extracellular DA levels, especially tonic versus phasic DA release, is limited by their intrinsic affinity. Here we show that a human-selective dopamine receptor positive allosteric modulator (PAM) can be used to boost sensor affinity on-demand. The PAM enhances DA detection sensitivity across experimental preparations (in vitro, ex vivo and in vivo) via one-photon or two-photon imaging. In vivo photometry-based detection of optogenetically-evoked DA release revealed that DETQ administration produces a stable 31 minutes window of potentiation without effects on animal behavior. The use of the PAM revealed region-specific and metabolic state-dependent differences in tonic DA levels and enhanced single-trial detection of behavior-evoked phasic DA release in cortex and striatum. Our chemogenetic strategy can potently and flexibly tune DA imaging sensitivity and reveal multi-modal (tonic/phasic) DA signaling across preparations and imaging approaches.

Date: 2024
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DOI: 10.1038/s41467-024-49442-3

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