Partial connectomes of labeled dopaminergic circuits reveal non-synaptic communication and axonal remodeling after exposure to cocaine

Wildenberg, Gregg; Sorokina, Anastasia; Koranda, Jessica; Monical, Alexis; Heer, Chad; Sheffield, Mark; Zhuang, Xiaoxi; McGehee, Daniel; Kasthuri, Bobby

doi:10.7554/elife.71981

Title: Partial connectomes of labeled dopaminergic circuits reveal non-synaptic communication and axonal remodeling after exposure to cocaine

Journal Article · 28 December 2021 · eLife

DOI: https://doi.org/10.7554/elife.71981 · OSTI ID:2469958

^[1]; Sorokina, Anastasia ^[1]; Koranda, Jessica ^[2]; Monical, Alexis ^[2]; Heer, Chad ^[2]; Sheffield, Mark ^[2]; Zhuang, Xiaoxi ^[2]; McGehee, Daniel ^[2];

^[1]

University of Chicago, IL (United States); Argonne National Laboratory (ANL), Argonne, IL (United States)
University of Chicago, IL (United States)

Dopaminergic (DA) neurons exert profound influences on behavior including addiction. However, how DA axons communicate with target neurons and how those communications change with drug exposure remains poorly understood. We leverage cell type-specific labeling with large volume serial electron microscopy to detail DA connections in the nucleus accumbens (NAc) of the mouse (Mus musculus) before and after exposure to cocaine. We find that individual DA axons contain different varicosity types based on their vesicle contents. Spatially ordering along individual axons further suggests that varicosity types are non-randomly organized. DA axon varicosities rarely make specific synapses (<2%, 6/410), but instead are more likely to form spinule-like structures (15%, 61/410) with neighboring neurons. Days after a brief exposure to cocaine, DA axons were extensively branched relative to controls, formed blind-ended ‘bulbs’ filled with mitochondria, and were surrounded by elaborated glia. Finally, mitochondrial lengths increased by ~2.2 times relative to control only in DA axons and NAc spiny dendrites after cocaine exposure. We conclude that DA axonal transmission is unlikely to be mediated via classical synapses in the NAc and that the major locus of anatomical plasticity of DA circuits after exposure to cocaine are large-scale axonal re-arrangements with correlated changes in mitochondria.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 2469958

Journal Information:: eLife, Journal Name: eLife Vol. 10; ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.Copyright Statement

Country of Publication:: United States

Language:: English

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