Nitric oxide acts as a cotransmitter in a subset of dopaminergic neurons to diversify memory dynamics
- Janelia Research Campus, Howard Hughes Medical Institute, United States
- University of Virginia, United States
- Columbia University, United States
Abstract
Animals employ diverse learning rules and synaptic plasticity dynamics to record temporal and statistical information about the world. However, the molecular mechanisms underlying this diversity are poorly understood. The anatomically defined compartments of the insect mushroom body function as parallel units of associative learning, with different learning rates, memory decay dynamics and flexibility (Aso & Rubin 2016). Here we show that nitric oxide (NO) acts as a neurotransmitter in a subset of dopaminergic neurons in Drosophila. NO's effects develop more slowly than those of dopamine and depend on soluble guanylate cyclase in postsynaptic Kenyon cells. NO acts antagonistically to dopamine; it shortens memory retention and facilitates the rapid updating of memories. The interplay of NO and dopamine enables memories stored in local domains along Kenyon cell axons to be specialized for predicting the value of odors based only on recent events. Our results provide key mechanistic insights into how diverse memory dynamics are established in parallel memory systems.
Data availability
Complete transcript data were deposited to NCBI Gene Expression Omnibus (accession number GSE139889).
Article and author information
Author details
Ashok Litwin-Kumar
Funding
Howard Hughes Medical Institute
- Yoshinori Aso
- Robert P Ray
- Xi Long
- Daniel Bushey
- Teri-TB Ngo
- Brandi Sharp
- Christina Christoforou
- Amy Hu
- Andrew L Lemire
- Paul Tillberg
- Gerald M Rubin
National Institutes of Health (R01 GM84128)
- Karol Cichewicz
- Jay Hirsh
Simons Foundation (Global Brain)
- Yoshinori Aso
- Ashok Litwin-Kumar
- Gerald M Rubin
Burroughs Wellcome Foundation
- Ashok Litwin-Kumar
Gatsby Charitable Foundation
- Ashok Litwin-Kumar
National Science Foundation (DBI-1707398)
- Ashok Litwin-Kumar
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2019, Aso et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Further reading
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- Neuroscience
- Physics of Living Systems
Neurons generate and propagate electrical pulses called action potentials which annihilate on arrival at the axon terminal. We measure the extracellular electric field generated by propagating and annihilating action potentials and find that on annihilation, action potentials expel a local discharge. The discharge at the axon terminal generates an inhomogeneous electric field that immediately influences target neurons and thus provokes ephaptic coupling. Our measurements are quantitatively verified by a powerful analytical model which reveals excitation and inhibition in target neurons, depending on position and morphology of the source-target arrangement. Our model is in full agreement with experimental findings on ephaptic coupling at the well-studied Basket cell-Purkinje cell synapse. It is able to predict ephaptic coupling for any other synaptic geometry as illustrated by a few examples.
