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Abstract
Single neurons in the brains of insects often have individual genetic identities and can be unambiguously identified between animals. The overall neuronal connectivity is also genetically determined and hard-wired to a large degree. Experience-dependent structural and functional plasticity is believed to be superimposed onto this more-or-less fixed connectome. However, in Drosophila melanogaster, it has been shown that the connectivity between the olfactory projection neurons (OPNs) and Kenyon cells, the intrinsic neurons of the mushroom body, is highly stochastic and idiosyncratic between individuals. Ensembles of distinctly and sparsely activated Kenyon cells represent information about the identity of the olfactory input, and behavioral relevance can be assigned to this representation in the course of associative olfactory learning. Previously, we showed that in the absence of any direct sensory input, artificially and stochastically activated groups of Kenyon cells could be trained to encode aversive cues when their activation coincided with aversive stimuli. Here, we have tested the hypothesis that the mushroom body can learn any stochastic neuronal input pattern as behaviorally relevant, independent of its exact origin. We show that fruit flies can learn thermogenetically generated, stochastic activity patterns of OPNs as conditioned stimuli, irrespective of glomerular identity, the innate valence that the projection neurons carry, or inter-hemispheric symmetry.
Highlights
Drosophila melanogaster is a model organism, widely used in studies of the neuronal basis of behavior
To test whether the animals can associate the activity of stochastic sets of Olfactory projection neurons (OPNs) with a punishing electric shock, OPNs expressing mCherry-dTRPA1 were thermogenetically activated at 30◦C and this activation was temporally paired with 2 min of electric shocks of 90 V
Stereotyped gene expression and neuronal circuit wiring reflect innate ecological and behavioral programs. This is reflected in stereotyped chemotopic maps, observable in the antennal lobes (Fiala et al, 2002; Wang et al, 2003), that result from fixed olfactory-receptor expression and hard-wired neuronal connectivity (Vosshall et al, 2000; Couto et al, 2005; Fishilevich and Vosshall, 2005)
Summary
Drosophila melanogaster is a model organism, widely used in studies of the neuronal basis of behavior. Even at the level of gene expression, individual OPN types can be unambiguously distinguished, highlighting their genetic individualities (Li et al, 2017) This connectivity leads to chemotopic maps in those higherorder brain regions targeted by OPNs (Fiala et al, 2002; Jefferis et al, 2007). This deterministic, hard-wired connectivity, together with specific sensory receptors, has led to the idea of multiple neuronal “labeled lines,” wherein each olfactory input stimulates a route of connections that evoke an appropriate behavioral response, such as the avoidance of harmful substances (Suh et al, 2007; Stensmyr et al, 2012), egglaying on odorous substrates (Dweck et al, 2015), or pheromoneinduced courtship behavior (van der Goes van Naters and Carlson, 2007; Datta et al, 2008)
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