Activity of Defined Mushroom Body Output Neurons Underlies Learned Olfactory Behavior in Drosophila

Abstract

SummaryDuring olfactory learning in fruit flies, dopaminergic neurons assign value to odor representations in the mushroom body Kenyon cells. Here we identify a class of downstream glutamatergic mushroom body output neurons (MBONs) called M4/6, or MBON-β2β′2a, MBON-β′2mp, and MBON-γ5β′2a, whose dendritic fields overlap with dopaminergic neuron projections in the tips of the β, β′, and γ lobes. This anatomy and their odor tuning suggests that M4/6 neurons pool odor-driven Kenyon cell synaptic outputs. Like that of mushroom body neurons, M4/6 output is required for expression of appetitive and aversive memory performance. Moreover, appetitive and aversive olfactory conditioning bidirectionally alters the relative odor-drive of M4β′ neurons (MBON-β′2mp). Direct block of M4/6 neurons in naive flies mimics appetitive conditioning, being sufficient to convert odor-driven avoidance into approach, while optogenetically activating these neurons induces avoidance behavior. We therefore propose that drive to the M4/6 neurons reflects odor-directed behavioral choice.

A Higher Brain Circuit for Immediate Integration of Conflicting Sensory Information in Drosophila

“…This reduction, however, was significantly smaller compared to the effect observed in starved flies (Figures S1G b and S1H b ). These results indicate that silencing MBONs can lead to different behavioral consequences than silencing of KCs, similar to what was recently reported by Owald et al [21]. In spite of this, they still indicate that the level of involvement of MBONs in processing the same odor depends on the internal state of the fly.…”

Common microbehavioral “footprint” of two distinct classes of conditioned aversion

“…This learned valence then can be added to the odor's innate valence and accordingly shift behavior toward more approach or more aversion-depending on the kind of odor and the kind of memory associated with it ( Fig. 5; Aso et al 2014b;Owald et al 2015;Schleyer et al 2015b). After paired aversive and unpaired appetitive training, the learned valence is negative, shifting the behavior toward aversion.…”

Parallel memory traces are built after an experience containing aversive and appetitive components in the crab Neohelice

“…Interestingly, it was shown in flies that instantaneous decisions taken on the basis of simultaneous stimuli that have opposite innate values involve the same mushroom body output neurons that participate on expression of appetitive and aversive memories (13). Thus, it is conceivable that opposite information acquired through experience is stored as independent memories that are integrated during retrieval according to the same rules used for stimuli with innate opposite values.…”

“…The hypothesis that appetitive and aversive information interact during memory processes gets support from pharmacological studies in crabs (6,7) and bees (8,9), which show that the neurotransmitter necessary for appetitive memory formation does, in turn, impair aversive memory, whereas the transmitter necessary for aversive memory impairs appetitive memory. In addition, studies in Drosophila, in which memory mechanisms can be dissected at the neuron level, provide evidence that the interaction between appetitive and aversive information occurs from the circuits that encode reward and punishment to circuits that regulate memory expression (10)(11)(12)(13)(14).…”