Abstract
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.
Highlights
Mechanisms underlying memory can be as simple as a modulation of monosynaptic connection in the gill withdraw reflex of Aplysia [1]
How is a punishing event represented in the brain? We have found that at least three types of dopamine neurons in the Drosophila brain contribute to memory formation
We characterized aversive memories induced by these dopamine neurons
Summary
Mechanisms underlying memory can be as simple as a modulation of monosynaptic connection in the gill withdraw reflex of Aplysia [1]. The application of noxious stimuli, such as electric shock, activates only a subset of dopamine neurons [21,24], indicating that the response property greatly varies among individual cells within a cluster. Consistent with this observation, activation of specific subsets of these clusters, such as MB-M3 and MB-MP1 neurons, can induce aversive odor memory [25]. This dopamine input presumably modulates the pre-synaptic output of odor-representing Kenyon cells and drives memory formation [8,9]
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