%0 Generic
%A Hörtzsch, Jan Niklas
%D 2017
%F heidok:21854
%R 10.11588/heidok.00021854
%T A Single Pair of Neurons Defines a Neuropeptide-Dependent Aversive Memory Channel in Drosophila melanogaster
%U https://archiv.ub.uni-heidelberg.de/volltextserver/21854/
%X Parallel information processing in distinct channels is a common functional principle of nervous systems to facilitate rapid and precise extraction of specific features. A hallmark of such parallel processing is that the originally acquired information is initially segregated into individual processing channels that are tuned to extract distinct features of the input before re-converging them to guide appropriate responses. Parallel processing also applies to aversive olfactory memories in Drosophila where the metabolically costly and more enduring memory channel is sensitive to cold anesthesia (ASM) whereas the parallel anesthesia resistant memory channel (ARM) is only transient. The molecular basis and functional significance of this segregation of aversive olfactory memories in parallel channels is currently unclear. Here, we show that an aversive unconditioned stimulus (US) used in classical olfactory conditioning experiments is responsible for synaptic activity-driven neuronal nuclear calcium transients in distinct areas of the fly brain. These areas include the fly's association center, the mushroom bodies (MBs), as well as the fly's master regulator of its neuropeptidergic system, the pars intercerebralis (PI). Blockade of nuclear calcium signaling allowed us to functionally and morphologically separate the role of cAMP, a classical signaling pathway in learning and memory, and nuclear calcium signaling in the establishment of consolidated long-term memories (LTM) (Weislogel et al., 2013). In addition, we show that the US activates the fly’s widespread neuropeptidergic system and, in particular, the PI which results in multiple local signaling events or even systemic responses. Furthermore, we show that the acquisition and formation of all ASM phases requires additional release of mature neuropeptides from a single pair of dorsal paired medial (DPM) neurons. DPM neurons form a recurrent network with mushroom body neurons that has been shown to be involved in the formation of serotonin-dependent ARM, consolidation of memory and linking these consolidation processes to sleep. Our results reveal that DPMs define a qualitatively distinct parallel memory channel that strictly depends on mature neuropeptides and that is, within the first hours after training, behaviorally additive to the neuropeptide-independent ARM channel. Afterwards, in its subsequent consolidated phase, the ASM channel becomes exclusive towards the ARM channel. Thus, we propose that DPM neurons are capable of gating the simultaneous formation of two parallel memory channels by means of using two distinct signaling systems. Finally, given that neuropeptide signaling appears to be more widely involved in the processing of the US, it could represent a general mean of defining parallel processing channels.