Specific dopaminergic neurons for the formation of labile aversive memory

By Yoshinori Aso, Igor Siwanowicz, L. Bräcker, Kei Ito, T. Kitamoto, Hiromu Tanimoto. 2010

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A paired presentation of an odor and electric shock induces aversive odor memory in Drosophila melanogaster. Electric shock reinforcement is mediated by dopaminergic neurons, and it converges with the odor signal in the mushroom body (MB). Dopamine is synthesized in approximately 280 neurons that form distinct cell clusters and is involved in a variety of brain functions. Recently, one of the dopaminergic clusters (PPL1) that includes MB-projecting neurons was shown to signal reinforcement for aversive odor memory. As each dopaminergic cluster contains multiple types of neurons with different projections and physiological characteristics, functional understanding of the circuit for aversive memory requires cellular identification. Here, we show that MB-M3, a specific type of dopaminergic neurons in the PAM cluster, is preferentially required for the formation of labile memory. Strikingly, flies formed significant aversive odor memory without electric shock when MB-M3 was selectively stimulated together with odor presentation. In addition, we identified another type of dopaminergic neurons in the PPL1 cluster, MB-MP1, which can induce aversive odor memory. As MB-M3 and MB-MP1 target the distinct subdomains of the MB, these reinforcement circuits might induce different forms of aversive memory in spatially segregated synapses in the MB.

Subfields: Cell Biology, Cellular and Molecular Neuroscience, Cognitive Neuroscience

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Citations in the corpus

Dopaminergic neurons write and update memories with cell-type-specific rules (2016, background): “DOI: 10.7554/eLife.16135 1 of 15 MBONs and DANs overlap precisely, defining 15 distinct compartmental units that tile the MB lobes of adult Drosophila (Tanaka et al., 2008; Aso et al., 2014a).”
Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila (2014, background): “…associative memory Recent studies of dopamine signaling have implicated distinct sites of memory formation within the MB lobes (summarized in Figure 1A) (Schroll et al., 2006; Claridge-Chang et al., 2009; Aso et al., 2010, 2012; Burke et al., 2012; Liu et al., 2012; Perisse et al., 2013).”
The neuronal architecture of the mushroom body provides a logic for associative learning (2014, methodology): “In accord with this model, DAN activity is required during learning (Schwaerzel et al., 2003; Aso et al., 2010, 2012; Burke et al., 2012; Liu et al., 2012) and exogenous activation of DAN subpopulations can serve as an US in associative learning paradigms (Schroll et al., 2006; Claridge-Chang et…”
The Drosophila Mushroom Body: From Architecture to Algorithm in a Learning Circuit. (2020, background): “In fact, it is possible to train animals by pairing the odor cue with direct activation of DANs (Aso et al. 2010, 2012; Burke & Waddell 2011; Claridge-Chang et al. 2009; Huetteroth et al. 2015; Liu et al. 2012; Schroll et al. 2006, Yamagata et al. 2015).”
Do the right thing: neural network mechanisms of memory formation, expression and update in Drosophila (2018, background): “The presynaptic terminals of different subsets of dopaminergic neurons (DANs), encoding positive or negative valence, occupy distinct, nonoverlapping compartments of the mushroom body neuropil which are precisely matched by the dendritic fields of discrete MBONs (Figure 1) [16,18,19,22,23,34 ,35,36]”
Bruchpilot, A Synaptic Active Zone Protein for Anesthesia-Resistant Memory (2011, background): “In the lobes, Kenyon cell axons have multiple compartments that are intersected by transverse extrin- sic neurons (Tanaka et al., 2008; Aso et al., 2010).”
Competing dopamine neurons drive oviposition choice for ethanol in Drosophila (2013, background): “The PPL1 neurons signal punishment in the context of shock-conditioned odor memory (35, 45) but also play a role in modulating sugar-conditioned odor memory (17).”
Parallel processing of appetitive short- and long-term memories in Drosophila. (2011, background): “The partial inhibition observed with NP21 and 1471 GAL4 drivers might be due to the fact that MB247 shows a very strong expression in g neurons [26], unlike 1471 [26] or NP21 [32].”
Distinct dopamine neurons mediate reward signals for short- and long-term memories (2014, methodology): “Appetitive conditioning and reward substitution with thermoactivation were performed according to previously described protocols of differential conditioning (19, 29, 30).”
Pain-relief learning in flies, rats, and man: basic research and applied perspectives (2014, methodology): “ISSN 1549-5485/14; www.learnmem.org 232 Learning & Memory”
Spaced Training Forms Complementary Long-Term Memories of Opposite Valence in Drosophila (2019, unknown): “3 provide reinforcement signals that modulate connections between MB Kenyon Cells (KCs) and MB output neurons (MBONs), whose dendrites occupy the same MB compartment (Claridge-Chang et al., 2009; Aso et al., 2010; Burke et al., 2012; Liu et al., 2012; Lin et al., 2014).”
Converging circuits mediate temperature and shock aversive olfactory conditioning in Drosophila. (2014, unknown): “Increased Temperature and Shock Signaling Converge on a Dopamine Reinforcement Pathway Dopamine serves as the main neurotransmitter for signaling aversive reinforcement in flies during olfactory shock conditioning [2, 3].”
Dopaminergic neurons encode a distributed, asymmetric representation of temperature in Drosophila (2013, background): “In Drosophila, dopaminergic neurons innervate the mushroom body (among other regions) (Mao and Davis, 2009), in which they modulate aversive learning (Schwaerzel et al., 2003; Claridge-Chang et al., 2009; Aso et al., 2010; Davis, 2011), forgetting (Berry et al.”
Drosophila ORB protein in two mushroom body output neurons is necessary for long-term memory formation (2013, background): “The specificity of RNAi knockdowns was addressed by misexpressing the RNAi transgenes in mushroom body M3 (MB-M3) neurons, a different set of MB extrinsic neurons required for 3-h memory (29); 1-d memory after spaced training was normal in these cases (Fig.”
γ neurons mediate dopaminergic input during aversive olfactory memory formation in Drosophila (2012, unknown): “This conclusion is consistent with findings from previous attempts to map the subset of DA neurons that convey the US to MBs using either inhibition or activation of neural transmission to block or mimic the US signal [3, 4].”