Post-eclosion odor experience modifies olfactory receptor neuron coding in Drosophila

Abstract

Olfactory responses of Drosophila undergo pronounced changes after eclosion. The flies develop attraction to odors to which they are exposed and aversion to other odors. Behavioral adaptation is correlated with changes in the firing pattern of olfactory receptor neurons (ORNs). In this article, we present an information-theoretic analysis of the firing pattern of ORNs. Flies reared in a synthetic odorless medium were transferred after eclosion to three different media: (i) a synthetic medium relatively devoid of odor cues, (ii) synthetic medium infused with a single odorant, and (iii) complex cornmeal medium rich in odors. Recordings were made from an identified sensillum (type II), and the Jensen-Shannon divergence (D JS ) was used to assess quantitatively the differences between ensemble spike responses to different odors. Analysis shows that prolonged exposure to ethyl acetate and several related esters increases sensitivity to these esters but does not improve the ability of the fly to distinguish between them. Flies exposed to cornmeal display varied sensitivity to these odorants and at the same time develop greater capacity to distinguish between odors. Deprivation of odor experience on an odorless synthetic medium leads to a loss of both sensitivity and acuity. Rich olfactory experience thus helps to shape the ORNs response and enhances its discriminative power. The experiments presented here demonstrate an experience-dependent adaptation at the level of the receptor neuron.imaginal conditioning | sensory adaptation | odor imprinting | JensenShannon divergence | chemo receptor tuning O lfaction in the fruit fly, Drosophila melanogaster, is crucial for a variety of behaviors, including associative learning (1, 2), courtship (3), foraging (4), and flight (5, 6). Odorants are detected by approximately 1,300 olfactory receptor neurons (ORNs), which are housed in sensilla on the third antennal segment and individually express one of approximately 50 functional odor receptors in adults (7-9). All ORNs expressing the same olfactory receptor project to one of approximately 50 glomeruli in the antennal lobe, where they synapse with a set of projection neurons (PNs) (10, 11). The activity of ORNs, either excitation or inhibition, provides behaviorally relevant information about odorants such as their identity, concentration, and source. The information transduced by an ORN is processed in the antennal lobe (12, 13) and sent via PNs to the mushroom bodies, which are believed to be centers for olfactory learning and memory (14, 15).Experience-dependent modifiability (i.e., plasticity) of olfactory representation at the level of the central nervous system is well known (2,16,17). Relatively little attention has been paid to long-term changes in sensory neuron activity resulting from odor experiences. It was previously shown that exposure of newly born imago to a particular set of odorants alters their responses to these odors (18,19). The flies develop an attraction to the chemicals to which they are exposed and an av...

Experience-dependent modulation of antennal sensitivity and input to antennal lobes in male moths (Spodoptera littoralis) pre-exposed to sex pheromone

“…This is consistent with previous studies that have shown long-term effects of olfactory exposure on odorant receptor expression (Zhou et al, 2009), odorant-evoked responses of ORNs (Iyengar et al, 2010) or glomerular volume (Devaud et al, 2001;Sachse et al, 2007). However, to our knowledge this is the first report of multi-level changes in a given model species.…”

“…This lower response threshold was observed without any change in ORN spontaneous activity, thus indicating that it was not due to any change in basal firing probability. Along the same lines, it was shown recently that young fruitflies exposed early in life to a given odorant later displayed increased ORN sensitivity to this odorant (Iyengar et al, 2010). Our findings that pre-exposure to the pheromone leads to increased ORN responses and an increase in the volume of the main MGC glomerulus indicate that an increased input to the AL may contribute to the reduced response threshold found in AL neurons after preexposure in a previous study (Anderson et al, 2007).…”

“…Contrasting with this view, many recent studies have shown that, like mammals, insects also display a high degree of plasticity (Menzel and Giurfa, 2006;Giurfa, 2007;Groh and Meinertzhagen, 2010). This is particularly well illustrated by the numerous examples of how previous experience of odorants with strong biological significance may lead to adaptive behavioural and neural changes Vergoz et al, 2009;Arenas et al, 2009;Beggs et al, 2007;Iyengar et al, 2010;Urlacher et al, 2010). Many insect species are capable of olfactory learning, and their olfactory pathways exhibit high degrees of neural plasticity.…”

Brief predator sound exposure elicits behavioral and neuronal long-term sensitization in the olfactory system of an insect

“…One way to achieve such adaptive behavior is through plasticity of the nervous system, whereby modifications can be induced depending on sensory input. Previous studies have shown that exposure to environmental signals during development and in early adult life might influence the precise design and sensitivity of the targeted sensory system (1)(2)(3). The development of the peripheral and central visual, auditory, somatosensory, and olfactory systems in vertebrates has been shown to be highly influenced by experience (e.g., refs.…”

Central Adaptation to Odorants Depends on PI3K Levels in Local Interneurons of the Antennal Lobe

“…In particular, our data do not show a crucial role for MB neurons in adaptation of the response following exposure, though further experiments based on complementary GAL4 lines expressed in different subsets of MB neurons would be necessary to confirm this. The requirement for a balanced connectivity between eLNs and iLNs may be important to adjust the system's response to modified sensory input: indeed, odor exposure during early adulthood can alter adult OSN responses (Iyengar et al, 2010). Here, we have not addressed the possible role of sensory input since we have targeted central neurons, but we do not exclude the possibility that peripheral receptor plasticity may contribute indirectly to the modifications of connectivity in central neurons shown here.…”