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Rapid multi-directed cholinergic transmission in the central nervous system

S. Sethuramanujam,A. Matsumoto,Geoff deRosenroll,Benjamin L Murphy-Baum,C. Grosman,J. McIntosh,Miao Jing,Yulong Li,D. Berson,Keisuke Yonehara,G. Awatramani

Published 2021 in Nature Communications

ABSTRACT

In many parts of the central nervous system, including the retina, it is unclear whether cholinergic transmission is mediated by rapid, point-to-point synaptic mechanisms, or slower, broad-scale ‘non-synaptic’ mechanisms. Here, we characterized the ultrastructural features of cholinergic connections between direction-selective starburst amacrine cells and downstream ganglion cells in an existing serial electron microscopy data set, as well as their functional properties using electrophysiology and two-photon acetylcholine (ACh) imaging. Correlative results demonstrate that a ‘tripartite’ structure facilitates a ‘multi-directed’ form of transmission, in which ACh released from a single vesicle rapidly (~1 ms) co-activates receptors expressed in multiple neurons located within ~1 µm of the release site. Cholinergic signals are direction-selective at a local, but not global scale, and facilitate the transfer of information from starburst to ganglion cell dendrites. These results suggest a distinct operational framework for cholinergic signaling that bears the hallmarks of synaptic and non-synaptic forms of transmission. Cholinergic neurons may transmit information via fast synaptic, point-to-point signaling or diffuse, slow extra-synaptic signaling. The authors show that ACh from a single vesicle triggers synchronous miniature currents in two neurons, showing that ACh can spread significant distances to drive rapid ‘synaptic’ signals.

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