6 These authors contributed equally to this work. 2 Aversive olfactory memory is formed in the Drosophila mushroom bodies (MB).Memory retrieval requires MB output, but it remains unknown how a memory trace in the MB drives conditioned avoidance of a learned odour. To identify neurons involved in olfactory memory retrieval, we performed an anatomical and functional screen of defined sets of MB extrinsic neurons. Here we show that MB-V2 neurons are essential for retrieval of both short-and long-lasting memory, but neither for memory formation nor for memory consolidation. We further show that MB-V2 are cholinergic efferent neurons that project from the MB vertical lobes to the middle superiormedial protocerebrum and the lateral horn (LH). Notably, the odour response of MB-V2 neurons is modified after conditioning. As the LH is implicated in innate responses to repellent odorants, we propose that during memory retrieval, MB-V2 neurons reinforce the olfactory pathway involved in innate odour avoidance.Different odours induce innate approach or avoidance behaviours in Drosophila. Innate odour responses can be modulated by experience, such as associative learning. After simultaneous exposure to an electric shock and an odorant, flies form aversive memory and show robust conditioned odour avoidance that lasts for hours to days, depending on the training protocol [1][2][3] . The neural pathways for odour or shock processing and signal integration in the fly brain have been intensely studied in recent years. Odour information is first represented in the antennal lobes in the form of olfactory receptor neuron activity 4 . Projection neurons then convey this information to higher order processing centres 4 : the mushroom bodies (MB) and the lateral horn (LH). In contrast, aversive reinforcement signals in response to electric shock are relayed to the MB via dopaminergic neurons [5][6][7] . The olfactory and 3 electric shock signals are integrated in the MB to form aversive olfactory memory 1, 2 . The MB are however dispensable for innate avoidance of the repellent odours 8,9 .In adult Drosophila, the MB consist of approximately 2000 Kenyon cells per brain hemisphere, which may be classified into three major types based on their axonal projection: γ neurons, which form only a medial lobe, α/β neurons, whose axons branch to form a vertical (α) and a medial (β) lobe, and α'/β' neurons, which also form a vertical (α') and a medial (β') lobe 10 . Functional brain imaging has revealed localised activation of cAMP/PKA signalling in the MB α lobe in response to simultaneous cholinergic and dopaminergic stimulation 11,12 , that represent respectively the odorant and electric shock pathways.Following associative conditioning, calcium imaging studies have shown that a short-term memory trace is formed in the α'/β' neurons 13, and a long-term one in α lobes 14 . Previous studies have shown that the output of the α/β neurons is necessary for the retrieval of all phases of olfactory memory 15,16 , but the neural circuits that translate ...
SummaryHoneybees constitute established model organisms for the study of appetitive learning and memory. In recent years, the establishment of the technique of olfactory conditioning of the sting extension response (SER) has yielded new insights into the rules and mechanisms of aversive learning in insects. In olfactory SER conditioning, a harnessed bee learns to associate an olfactory stimulus as the conditioned stimulus with the noxious stimulation of an electric shock as the unconditioned stimulus. Here, we review the multiple aspects of honeybee aversive learning that have been uncovered using Pavlovian conditioning of the SER. From its behavioral principles and sensory variants to its cellular bases and implications for understanding social organization, we present the latest advancements in the study of punishment learning in bees and discuss its perspectives in order to define future research avenues and necessary improvements. The studies presented here underline the importance of studying honeybee learning not only from an appetitive but also from an aversive perspective, in order to uncover behavioral and cellular mechanisms of individual and social plasticity.
Within a honey bee colony, individuals performing different tasks exhibit different sensitivities to noxious stimuli. Noxious-stimulus sensitivity can be quantified in harnessed bees by measuring the sting extension response (SER) to a series of increasing voltages. Biogenic amines play a crucial role in the control of insect responsiveness. Whether or not these neurotransmitters affect the central control of aversive responsiveness, and more specifically of electric-shock responsiveness, remains unknown. Here we studied the involvement of the biogenic amines octopamine, dopamine and serotonin, and of the ecdysteroid 20-hydroxyecdisone in the central control of sting responsiveness to electric shocks. We injected pharmacological antagonists of these signaling pathways into the brain of harnessed bees and determined the effect of blocking these different forms of neurotransmission on shock responsiveness. We found that both octopamine and 20-hydroxyecdisone are dispensable for shock responsiveness while dopamine and serotonin act as down-regulators of sting responsiveness. As a consequence, antagonists of these two biogenic amines induce an increase in shock responsiveness to shocks of intermediate voltage; serotonin, can also increase non-specific responsiveness. We suggest that different classes of dopaminergic neurons exist in the bee brain and we define at least two categories: an instructive class mediating aversive labeling of conditioned stimuli in associative learning, and a global gain-control class which down-regulates responsiveness upon perception of noxious stimuli. Serotonergic signaling together with down-regulating dopaminergic signaling may play an essential role in attentional processes by suppressing responses to irrelevant, non-predictive stimuli, thereby allowing efficient behavioral performances.
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