Different Kenyon Cell Populations Drive Learned Approach and Avoidance in Drosophila

By E. Perisse, Yan Yin, Andrew C. Lin, Suewei Lin, Wolf Huetteroth, S. Waddell. 2013

124 citations recorded by the source corpus.

Summary In Drosophila, anatomically discrete dopamine neurons that innervate distinct zones of the mushroom body (MB) assign opposing valence to odors during olfactory learning. Subsets of MB neurons have temporally unique roles in memory processing, but valence-related organization has not been demonstrated. We functionally subdivided the αβ neurons, revealing a value-specific role for the ∼160 αβ core (αβc) neurons. Blocking neurotransmission from αβ surface (αβs) neurons revealed a requirement during retrieval of aversive and appetitive memory, whereas blocking αβc only impaired appetitive memory. The αβc were also required to express memory in a differential aversive paradigm demonstrating a role in relative valuation and approach behavior. Strikingly, both reinforcing dopamine neurons and efferent pathways differentially innervate αβc and αβs in the MB lobes. We propose that conditioned approach requires pooling synaptic outputs from across the αβ ensemble but only from the αβs for conditioned aversion.

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

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Citations in the corpus

Genetic dissection of mutual interference between two consecutive learning tasks in Drosophila (2022, background): “, 2018) or an appetitive learning task (Liu et al., 2012; Perisse et al., 2013; Pribbenow et al., 2022), which was less similar to the target task.”
Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila (2014, methodology): “DAN input to the compartments housing the dendrites of these feedforward MBONs induces aversive and appetitive memory, respectively (this work) (Perisse et al., 2013; Yamagata et al., in press).”
The neuronal architecture of the mushroom body provides a logic for associative learning (2014, background): “…of the lobes (the α/βp neurons) have their dendrites in the dorsal accessory calyx, a region spatially segregated from the dendritic arbors of other KCs (see Figure 7A), and their activity is decreased in response to odors (Perisse et al., 2013), suggesting a distinct role for these output neurons.”
Pain-relief learning in flies, rats, and man: basic research and applied perspectives (2014, background): “behavior (e.g., Krashes et al. 2009; Berry et al. 2012; Placais et al. 2012; Perisse et al. 2013; see also Burke et al. 2012); for these aspects too, the roles of dopamine and octopamine apparently”
Cell Type-Specific Transcriptome Analysis in the Drosophila Mushroom Body Reveals Memory-Related Changes in Gene Expression (2016, unknown): “In addition, MBONs and dopaminergic neurons (encoding either reward or punishment signals) innervate specific domains or compartments of each of the MB lobes (Aso et al., 2014a; Perisse et al., 2013).”
Neuronal mechanisms underlying innate and learned olfactory processing in Drosophila. (2019, background): “appetitive memory, perhaps through different connectivity with 265 DANs or MBONs [86,87].”
The complete connectome of a learning and memory centre in an insect brain (2017, background): “This extensive innervation provides MBONs access to the high-dimensional KC representation and suggests that individual KCs may be involved in the formation and storage of associations involving multiple stimuli and valences, as suggested for the adult 1;4;5 (but see 43 ).”
Spaced Training Forms Complementary Long-Term Memories of Opposite Valence in Drosophila (2019, unknown): “, 2019), relative shock (Perisse et al., 2013), absence of expected shock (Felsenberg et al.”
Drosophila Learn Opposing Components of a Compound Food Stimulus (2014, background): “However, recent studies suggested a requirement for modulation of the aversive system in appetitive learning [9] and demonstrated a role for rewarding dopaminergic neurons in relative aversive learning [31].”
Origins of Cell-Type-Specific Olfactory Processing in the Drosophila Mushroom Body Circuit. (2017, unknown): “In terms of function, a/b core and a/b surface KCs, for example, are shown to be involved in different aspects of olfactory learning (Perisse et al., 2013).”
Sweet Taste and Nutrient Value Subdivide Rewarding Dopaminergic Neurons in Drosophila (2015, methodology): “We used these and three established PAM lines [3, 4, 18] to express UAS-shi and tested LTM following sucrose-reinforced learning.”
Activity of Defined Mushroom Body Output Neurons Underlies Learned Olfactory Behavior in Drosophila (2015, methodology): “A single PI value is the average score from flies of the identical genotype tested with the reciprocal reinforced/ non-reinforced odor combination (Tully and Quinn, 1985; Perisse et al., 2013).”
A connectome of a learning and memory center in the adult Drosophila brain (2017, methodology): “It is possible to induce 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”
Reward signal in a recurrent circuit drives appetitive long-term memory formation (2015, unknown): “Output from the α/β KCs is required during conditioning Previous studies have highlighted the role of the output from α/β KCs for memory retrieval (Krashes et al., 2007; Trannoy et al., 2011; Cervantes-Sandoval et al., 2013; Perisse et al., 2013).”
Two independent mushroom body output circuits retrieve the six discrete components of Drosophila aversive memory. (2015, background): “Whether distinct forms of memory involve the same sets of neurons, and therefore act on the same synapses, has long been a subject of interest (Schwaerzel et al., 2003; Perisse et al., 2013).”
Heterosynaptic plasticity underlies aversive olfactory learning in Drosophila (2015, unknown): “, 2003), and the axonal projections of DANs responsible for appetitive and aversive memory are segregated in the MB lobes (Perisse et al., 2013).”