Three Dopamine Pathways Induce Aversive Odor Memories with Different Stability

By Yoshinori Aso, A. Herb, Maite Ogueta, Igor Siwanowicz, Thomas Templier, Anja B. Friedrich, Kei Ito, Henrike Scholz, Hiromu Tanimoto. 2012

259 citations recorded by the source corpus.

Animals acquire predictive values of sensory stimuli through reinforcement. In the brain of Drosophila melanogaster, activation of two types of dopamine neurons in the PAM and PPL1 clusters has been shown to induce aversive odor memory. Here, we identified the third cell type and characterized aversive memories induced by these dopamine neurons. These three dopamine pathways all project to the mushroom body but terminate in the spatially segregated subdomains. To understand the functional difference of these dopamine pathways in electric shock reinforcement, we blocked each one of them during memory acquisition. We found that all three pathways partially contribute to electric shock memory. Notably, the memories mediated by these neurons differed in temporal stability. Furthermore, combinatorial activation of two of these pathways revealed significant interaction of individual memory components rather than their simple summation. These results cast light on a cellular mechanism by which a noxious event induces different dopamine signals to a single brain structure to synthesize an aversive memory.

Subfields: Cellular and Molecular Neuroscience, Ecology, Evolution, Behavior and Systematics, Genetics

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Citations in the corpus

Dopaminergic neurons write and update memories with cell-type-specific rules (2016, methodology): “The observation that co-activation of PPL1-g2a01 and other DANs synergistically prolongs memory retention (Aso et al., 2012) raises the possibility that PPL1-g2a01 might act broadly to facilitate memory consolidation by promoting sleep after learning.”
Coordinated and Compartmentalized Neuromodulation Shapes Sensory Processing in Drosophila (2015, positive): “Distinct subsets of DANs are sufficient to drive learned olfactory associations (Aso et al., 2012; Claridge-Chang et al., 2009; Liu et al., 2012; Waddell, 2013; Yamagata et al., 2015), leading to the suggestion they may act autonomously to encode the rewarding or punishing contextual stimuli that…”
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): “These convergence zones are major sites of arborization for the dendrites of the DANs and axons of the MBONs.”
Short Neuropeptide F Acts as a Functional Neuromodulator for Olfactory Memory in Kenyon Cells of Drosophila Mushroom Bodies (2013, background): “…2008; Tanaka et al., 2008; Liu and Davis, 2009; Aso et al., 2010; Waddell, 2010; Blenau and Thamm, 2011; Lee et al., 2011; Sejourn é et al., 2011; Aso et al., 2012), a functional neurotransmitter or neuromodulator that mediates any of the MB-dependent behaviors in intrinsic MB neurons (Kenyon…”
A Higher Brain Circuit for Immediate Integration of Conflicting Sensory Information in Drosophila. (2015, result): “Previous studies showed that neurons of the PPL1 and PAM clusters encode negative valence during odor shock conditioning [23].”
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).”
A connectome of a learning and memory center in the adult Drosophila brain (2017, methodology): “…memory formation in this circuit by pairing odor delivery with artificial activation of DANs (Schroll et al., 2006; Claridge-Chang et al., 2009; Aso et al., 2010, 2012; Yamagata et al., 2015; Liu et al., 2012; Burke et al., 2012; Huetteroth et al., 2015; Perisse et al., 2013; Rohwedder et al.,…”
Drosophila Learn Opposing Components of a Compound Food Stimulus (2014, methodology): “It should be noted that the MP1 neurons have been previously implicated in shock- and sugar-reinforced learning and memory expression [6, 7, 9, 23].”
Different Kenyon Cell Populations Drive Learned Approach and Avoidance in Drosophila (2013, unknown): “…are repre- sented (Turner et al., 2008; Murthy et al., 2008; Honegger et al., 2011) and reinforcement signals conveyed (Claridge-Chang et al., 2009; Aso et al., 2010, 2012; Liu et al., 2012; Burke et al., 2012), it is not known how opposing behavioral programs of avoidance or approach are…”
Activity of Defined Mushroom Body Output Neurons Underlies Learned Olfactory Behavior in Drosophila (2015, background): “Value can be assigned to these odor representations during learning by the action of reinforcing dopaminergic neuronswhose presynaptic terminals are confined to discrete zones along the lobes of the MB (Schwaerzel et al., 2003; Riemensperger et al., 2005; Claridge-Chang et al., 2009; Aso et al., 201”
Dopaminergic neurons encode a distributed, asymmetric representation of temperature in Drosophila (2013, background): “…to negative reinforcers (Riemensperger et al., 2005; Mao and Davis, 2009), and stimulation of dopaminergic neurons in lieu of negative reinforcement leads to the formation of aversive memory in both larvae and adult flies (Schroll et al., 2006; Claridge-Chang et al., 2009; Aso et al., 2010, 2012).”
Converging circuits mediate temperature and shock aversive olfactory conditioning in Drosophila. (2014, unknown): “It is possible that the artificial electric shock stimulus recruits more than one specific pathway [3, 41, 45], whereas the ecologically relevant temperature stimulus is mediated by a more specific subset of dopamine neurons.”