Dedicated olfactory neurons mediating attraction behavior to ammonia and amines in Drosophila

Abstract

Animals across various phyla exhibit odor-evoked innate attraction behavior that is developmentally programmed. The mechanism underlying such behavior remains unclear because the odorants that elicit robust attraction responses and the neuronal circuits that mediate this behavior have not been identified. Here, we describe a functionally segregated population of olfactory sensory neurons (OSNs) and projection neurons (PNs) in Drosophila melanogaster that are highly specific to ammonia and amines, which act as potent attractants. The OSNs express IR92a, a member of the chemosensory ionotropic receptor (IR) family and project to a pair of glomeruli in the antennal lobe, termed VM1. In vivo calcium-imaging experiments showed that the OSNs and PNs innervating VM1 were activated by ammonia and amines but not by nonamine odorants. Flies in which the IR92a + neurons or IR92a gene was inactivated had impaired amine-evoked physiological and behavioral responses. Tracing neuronal pathways to higher brain centers showed that VM1-PN axonal projections within the lateral horn are topographically segregated from those of V-PN and DC4-PN, which mediate innate avoidance behavior to carbon dioxide and acidity, respectively, suggesting that these sensory stimuli of opposing valence are represented in spatially distinct neuroanatomic loci within the lateral horn. These experiments identified the neurons and their cognate receptor for amine detection, and mapped amine attractive olfactory inputs to higher brain centers. This labeled-line mode of amine coding appears to be hardwired to attraction behavior.olfaction | neural circuit | odorant receptor T he olfactory system of adult Drosophila melanogaster serves as a genetically and anatomically simple model for studying how sensory input is translated into behavior output. The majority of olfactory sensory neurons (OSNs) express one functional receptor that is composed of an odorant receptor coreceptor (ORCO) and one of ∼45 odorant receptors (ORs) (1-3). About a quarter of the OSNs that do not express ORs recently were shown to express a second family of insect olfactory receptors termed the "ionotropic receptors" (IRs) (4). Each of these OSN types expresses a single or multiple IRs together with a coreceptor, IR8a or IR25a (or rarely both) (5). OR and IR sensory neurons expressing the same receptor send their axonal projections to one or rarely two of ∼50 spatially invariant glomeruli within the antennal lobe (AL) (4, 6-8) where they provide significant synaptic inputs to second-order projection neurons (PNs) that convey the sensory information to higher brain centers such as the mushroom body (MB) and the lateral horn (LH) (9-12).This genetic and anatomical simplicity of Drosophila has allowed us to further our understanding of a general principle of innate behavior. The emerging characteristics of a neural circuit that is hardwired to a specific behavior include (i) the specificity of the sensory neurons to a single chemical cue and (ii) the discrete spatial representation of tha...

Chemicals and chemoreceptors: ecologically relevant signals driving behavior in Drosophila

“…In addition, IR92 + neurons detect ammonia and several different amines and activate a specific neuronal pathway dedicated to attractive behavior . Interestingly, ammonia and amines are highly attractive for both flies and mosquito, although the ecological context in which they find them is different; flies may perceive ammonia and amines produced by fruit decomposition, while mosquito are attracted to the same compounds but emanated from animal hosts (Meijerink et al, 2001;Min et al, 2013). Anyway, in both species, a specific receptor to ammonia and amines appears to be important for the detection of a food source.…”

Ir40a neurons are not DEET detectors

“…We propose that this sensory pathway is not relevant for DEET detection; future work will determine its role in behavioural responses to ammonia, an olfactory cue of ecological importance for many insects 10,11 .…”

Potencies of effector genes in silencing odor-guided behavior inDrosophila melanogaster

“…The contribution of OSN types to odor evaluation has so far been tested in several studies, each concerned with single OSN types using a wide variety of different behavioral paradigms (Ai et al, 2010;Dweck et al, 2013Dweck et al, , 2015aGrosjean et al, 2011;Kurtovic et al, 2007;Min et al, 2013;Ronderos et al, 2014;Semmelhack and Wang, 2009;Stensmyr et al, 2012;Suh et al, 2004). Also, a correlation between the activities of different projection neuron (PN) types and behavior to a large odor set has been established previously .…”

“…Therefore, the identity of most odors is encoded in the combinatorial activity of the OSN population as a whole (Malnic et al, 1999). Nevertheless, recent evidence suggests that the innate hedonic valence of odors can already be predicted on the basis of the identity of OSNs the odors activate (Ai et al, 2010;Dweck et al, 2013Dweck et al, , 2015aGrosjean et al, 2011;Knaden et al, 2012;Kurtovic et al, 2007;Min et al, 2013;Ronderos et al, 2014;Semmelhack and Wang, 2009;Stensmyr et al, 2012;Suh et al, 2004;Thoma et al, 2014). It is therefore tempting to remove specific OSN populations from the activity pattern and in this way to investigate their contribution to the overall valence of a given odor.…”

“…With one exception, i.e. the CO 2 detection system comprising two gustatory receptors (GRs) (Jones et al, 2007;Kwon et al, 2007), all antennally expressed olfactory chemoreceptors in D. melanogaster belong to one of two gene families, the evolutionarily ancient ionotropic receptors (IRs) detecting mainly -but not exclusivelyhydrophilic chemicals Ai et al, 2010;Benton et al, 2009;Grosjean et al, 2011;Min et al, 2013;Silbering et al, 2011) and the insect-specific odorant receptors (ORs) Gao and Chess, 1999;Vosshall et al, 1999). All D. melanogaster ORs rely on the ubiquitously expressed coreceptor Orco for intracellular trafficking (Larsson et al, 2004) and signal transduction (Sato et al, 2008;Wicher et al, 2008), and ORexpressing OSNs lacking the Orco protein are generally unresponsive to odors.…”