Dopaminergic neurons establish a distinctive axonal arbor with a majority of non‐synaptic terminals

Charles Ducrot, Marie‐Josée Bourque, Constantin V. L. Delmas, Anne‐Sophie Racine, Dainelys Guadarrama Bello, Benoît Delignat‐Lavaud, Matthew Domenic Lycas, Aurélie Fallon, Charlotte Michaud‐Tardif, Samuel Burke Nanni, Freja Herborg, Ulrik Gether, Antonio Nanci, Hideto Takahashi, Martin Parent, Louis‐Eric Trudeau
FASEB j.. 2021-07-28; 35(8):
DOI: 10.1096/fj.202100201RR

PubMed
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Ducrot C(1)(2)(3), Bourque MJ(1)(2)(3), Delmas CVL(4), Racine AS(1)(2)(3), Guadarrama Bello D(5), Delignat-Lavaud B(1)(2)(3), Domenic Lycas M(6), Fallon A(7)(8)(9), Michaud-Tardif C(1)(2)(3), Burke Nanni S(1)(2)(3), Herborg F(6), Gether U(6), Nanci A(5), Takahashi H(7)(8)(9), Parent M(4), Trudeau LE(1)(2)(3).

Author information:
(1)Department of Pharmacology and Physiology, Faculty of Medicine, Université de Montréal, Montréal, QC, Canada.
(2)Department of Neurosciences, Faculty of Medicine, Université de Montréal, Montréal, QC, Canada.
(3)CNS Research Group (GRSNC), Montréal, QC, Canada.
(4)Department of Psychiatry and Neurosciences, Faculty of Medicine, CERVO Brain Research Centre, Université Laval, Québec, QC, Canada.
(5)Department of Neuroscience, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark.
(6)Department of Stomatology, Faculty of Dental Medicine, Université de Montréal, Montréal, QC, Canada.
(7)Synapse Development and Plasticity Research Unit, Institut de Recherches Cliniques de Montréal, Montréal, QC, Canada.
(8)Department of Medicine, Université de Montréal, Montréal, QC, Canada.
(9)Integrated Program in Neuroscience, McGill University, Montréal, QC, Canada.

Chemical neurotransmission typically occurs through synapses. Previous ultrastructural examinations of monoamine neuron axon terminals often failed to identify a pre- and postsynaptic coupling, leading to the concept of “volume” transmission. Whether this results from intrinsic properties of these neurons remains undefined. We find that dopaminergic neurons in vitro establish a distinctive axonal arbor compared to glutamatergic or GABAergic neurons in both size and propensity of terminals to avoid direct contact with target neurons. While most dopaminergic varicosities are active and contain exocytosis proteins like synaptotagmin 1, only ~20% of these are synaptic. The active zone protein bassoon was found to be enriched in dopaminergic terminals that are in proximity to a target cell. Finally, we found that the proteins neurexin-1αSS4- and neuroligin-1A+B play a critical role in the formation of synapses by dopamine (DA) neurons. Our findings suggest that DA neurons are endowed with a distinctive developmental connectivity program.

© 2021 Federation of American Societies for Experimental Biology.

 

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