Memory formation is a highly complex and dynamic process. It consists of different phases, which depend on various neuronal and molecular mechanisms. In adult Drosophila it was shown that memory formation after aversive Pavlovian conditioning includes—besides other forms—a labile short-term component that consolidates within hours to a longer-lasting memory. Accordingly, memory formation requires the timely controlled action of different neuronal circuits, neurotransmitters, neuromodulators and molecules that were initially identified by classical forward genetic approaches. Compared to adult Drosophila , memory formation was only sporadically analyzed at its larval stage. Here we deconstruct the larval mnemonic organization after aversive olfactory conditioning. We show that after odor-high salt conditioning larvae form two parallel memory phases; a short lasting component that depends on cyclic adenosine 3’5’-monophosphate (cAMP) signaling and synapsin gene function. In addition, we show for the first time for Drosophila larvae an anesthesia resistant component, which relies on radish and bruchpilot gene function, protein kinase C activity, requires presynaptic output of mushroom body Kenyon cells and dopamine function. Given the numerical simplicity of the larval nervous system this work offers a unique prospect for studying memory formation of defined specifications, at full-brain scope with single-cell, and single-synapse resolution. Author Summary Learning and memory helps organisms to predict and adapt to events in their environment. Gained experience leaves traces of memory in the nervous system. Yet, memory formation in vertebrates and invertebrates is a highly complex and dynamic process that consists of different phases, which depend on various neuronal and molecular mechanisms. To understand which changes occur in a brain when it learns, we applied a reductionist approach. Instead of studying complex cases, we analyzed learning and memory in Drosophila larvae that have a simple brain that is genetically and behaviorally accessible and consists of only about 10,000 neurons. Drosophila larvae are able to learn to associate an odor with punishing high salt concentrations. It is therefore possible to correlate changes in larval behavior with molecular events in identifiable neurons after classical olfactory conditioning. We show that under these circumstances larvae form two parallel memory phases; a short lasting component (lSTM) that is molecularly conserved throughout the animal kingdom as it depends on the classical cAMP pathway. In parallel they establish a larval anesthesia resistant memory (lARM) that relies on a different molecular signal. lARM has not been described in larvae before.
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