Dopaminergic Modulation of cAMP Drives Nonlinear Plasticity across the Drosophila Mushroom Body Lobes

Tamara Boto; Thierry Louis; Kantiya Jindachomthong; Kees Jalink; Seth M. Tomchik

doi:10.1016/j.cub.2014.03.021

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Dopaminergic Modulation of cAMP Drives Nonlinear Plasticity across the Drosophila Mushroom Body Lobes

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Dopaminergic Modulation of cAMP Drives Nonlinear Plasticity across the Drosophila Mushroom Body Lobes

Tamara Boto, Thierry Louis, Kantiya Jindachomthong, Kees Jalink and Seth M. Tomchik

Current biology, Vol.24(8), pp.822-831

04/14/2014

DOI: 10.1016/j.cub.2014.03.021

PMCID: PMC4019670

PMID: 24684937

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Abstract

Background: Activity of dopaminergic neurons is necessary and sufficient to evoke learning-related plasticity in neuronal networks that modulate learning. During olfactory classical conditioning, large subsets of dopaminergic neurons are activated, releasing dopamine across broad sets of postsynaptic neurons. It is unclear how such diffuse dopamine release generates the highly localized patterns of plasticity required for memory formation. Results: Here we have mapped spatial patterns of dopaminergic modulation of intracellular signaling and plasticity in Drosophila mushroom body (MB) neurons, combining presynaptic thermogenetic stimulation of dopaminergic neurons with postsynaptic functional imaging in vivo. Stimulation of dopaminergic neurons generated increases in cyclic AMP (cAMP) across multiple spatial regions in the MB. However, odor presentation paired with stimulation of dopaminergic neurons evoked plasticity in Ca2+ responses in discrete spatial patterns. These patterns of plasticity correlated with behavioral requirements for each set of MB neurons in aversive and appetitive conditioning. Finally, broad elevation of cAMP differentially facilitated responses in the gamma lobe, suggesting that it is more sensitive to elevations of cAMP and that it is recruited first into dopamine-dependent memory traces. Conclusions: These data suggest that the spatial pattern of learning-related plasticity is dependent on the postsynaptic neurons' sensitivity to cAMP signaling. This may represent a mechanism through which single-cycle conditioning allocates short-term memory to a specific subset of eligible neurons (gamma neurons).

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Title: Subtitle: Dopaminergic Modulation of cAMP Drives Nonlinear Plasticity across the Drosophila Mushroom Body Lobes
Creators: Tamara Boto - Scripps Research Institute
Thierry Louis - Scripps Research Institute
Kantiya Jindachomthong - Scripps Research Institute
Kees Jalink - Netherlands Cancer Institute
Seth M. Tomchik - Scripps Research Institute
Resource Type: Journal article
Publication Details: Current biology, Vol.24(8), pp.822-831
DOI: 10.1016/j.cub.2014.03.021
PMID: 24684937
PMCID: PMC4019670
NLM abbreviation: Curr Biol
ISSN: 0960-9822
eISSN: 1879-0445
Publisher: Elsevier
Number of pages: 10
Grant note: R00MH092294 / NATIONAL INSTITUTE OF MENTAL HEALTH; United States Department of Health & Human Services; National Institutes of Health (NIH) - USA; NIH National Institute of Mental Health (NIMH) R00 MH092294 / NIH/NIMH; United States Department of Health & Human Services; National Institutes of Health (NIH) - USA; NIH National Institute of Mental Health (NIMH)
Language: English
Date published: 04/14/2014
Academic Unit: Iowa Neuroscience Institute; Neuroscience and Pharmacology
Record Identifier: 9984303852002771

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