Dopaminergic modulation of cAMP drives nonlinear plasticity across the Drosophila mushroom body lobes

By Tamara Boto, Thierry Louis, Kantiya Jindachomthong, K. Jalink, Seth M. Tomchik. 2014

97 citations recorded by the source corpus.

SUMMARY 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 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).

Subfields: Cellular and Molecular Neuroscience, Immunology, Molecular Biology

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Citations in the corpus

Dopaminergic neurons write and update memories with cell-type-specific rules (2016, background): “…Dopamine signaling to KCs has been implicated in both learning and forgetting (Schwaerzel et al., 2003; Schroll et al., 2006, Kim et al., 2007; Tomchik and Davis, 2009; Gervasi et al., 2010; Qin et al., 2012; Placais et al., 2012; Berry et al., 2012; Boto et al., 2014; Shuai et al., 2015).”
Distinct dopamine receptor pathways underlie the temporal sensitivity of associative learning (2019, background): “We find that the spatial patterns of dopamine release and dopamine receptor second-messenger cascades adhere to the compartmentalized architecture of the lobes (Boto et al., 2014), permitting different synapses along the same KC axon to be independently regulated (Cohn et al.”
Reward signal in a recurrent circuit drives appetitive long-term memory formation (2015, unknown): “Several lines of evidence suggest that D1-like dopamine receptor (DopR1) is required in KCs for appetitive memory (Kim et al., 2007; Liu et al., 2012; Boto et al., 2014).”
Heterosynaptic plasticity underlies aversive olfactory learning in Drosophila (2015, unknown): “However, Boto et al. (2014) did not observe any change in odor-evoked calcium responses in the KC axons in the g1 region after pairing odor with DAN activation using TH-GAL4, even though we observed very robust LTD in MBON-g1pedc using the same GAL4 line (Figures 5E–5H).”
Active Protection: Learning-Activated Raf/MAPK Activity Protects Labile Memory from Rac1-Independent Forgetting. (2018, unknown): “First, g neurons are believed to be a primary location for the acquisition and expression of early memory (Boto et al., 2014; Guven-Ozkan and Davis, 2014; Hige et al., 2015; Qin et al., 2012; Zhang and Roman, 2013).”
Postsynaptic plasticity of cholinergic synapses underlies the induction and expression of appetitive and familiarity memories in Drosophila (2022, background): “…that both pre- and postsynaptic mechanisms of memory storage exist in vertebrates, invertebrate memory- related synaptic plasticity has been largely localized to the presynaptic compartment (Bilz et al., 2020; Boto et al., 2014; Handler et al., 2019; Ehmann et al., 2018; Tully et al., 1994).”
Distinct dopamine neurons mediate reward signals for short- and long-term memories (2014, background): “As dopaminergic modulation of cAMP drives nonlinear plasticity across the MB lobes (43), it is perhaps not surprising that sugar responses are widely distributed beyond the PAM subsets.”
Spaced Training Forms Complementary Long-Term Memories of Opposite Valence in Drosophila (2019, unknown): “, 2016) via dopamine receptor directed cAMPdependent plasticity (Yu et al., 2006; Kim et al., 2007; Tomchik and Davis, 2009; Qin et al., 2012; Zhang and Roman, 2013; Boto et al., 2014; Hige et al., 2015).”
A connectome of a learning and memory center in the adult Drosophila brain (2017, background): “…1 p e d c > α /β (2 ) α lobe DPM APL dependent adenylate cyclase rutabaga, which initiates a cAMP signaling cascade that leads to the biochemical changes underlying synaptic plasticity (Livingstone et al., 1984; Levin et al., 1992; Boto et al., 2014; Gervasi et al., 2010; Tomchik and Davis, 2009).”