Moth olfactory receptor neurons adjust their encoding efficiency to temporal statistics of pheromone fluctuations

The efficient coding hypothesis predicts that sensory neurons adjust their coding resources to optimally represent the stimulus statistics of their environment. To test this prediction in the moth olfactory system, we have developed a stimulation protocol that mimics the natural temporal structure within a turbulent pheromone plume. We report that responses of antennal olfactory receptor neurons to pheromone encounters follow the temporal fluctuations in such a way that the most frequent stimulus timescales are encoded with maximum accuracy. We also observe that the average coding precision of the neurons adjusted to the stimulus-timescale statistics at a given distance from the pheromone source is higher than if the same encoding model is applied at a shorter, non-matching, distance. Finally, the coding accuracy profile and the stimulus-timescale distribution are related in the manner predicted by the information theory for the many-to-one convergence scenario of the moth peripheral sensory system

Odor background increases pheromone coding efficiency in moth olfactory neurons

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Odor background increases pheromone coding efficiency in moth olfactory neurons

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Electroantennography of terpene volatile compounds with insecticidal activity

International audienceSynthetic insecticides have adverse effects on non-target organisms, ecosystems and human health due to their high toxicity and residual accumulation in different environmental components and organism tissues. Moreover, their long-term applications generate the development of pest resistance. This has led to a growing interest in novel, more environmentally friendly insecticides. Essential oils and their active constituents, especially monoterpenoids, which play an important role in plant defense system against microorganisms, insects, herbivores and allelopathic interactions, are considered as an alternative to synthetic insecticides. Electroantennography (EAG), a technique widely used in insect olfaction studies, is performed in the present work on males of the Noctuid Agrotis ipsilon to characterize the electrical response evoked by well-known natural insecticides from the peripheral nervous system of insects

Response termination in insect olfactory receptor neurons can be fast and precise

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Stimulus duration encoding by moth olfactory receptor neurons

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Olfactory coding in the turbulent realm.

Long-distance olfactory search behaviors depend on odor detection dynamics. Due to turbulence, olfactory signals travel as bursts of variable concentration and spacing and are characterized by long-tail distributions of odor/no-odor events, challenging the computing capacities of olfactory systems. How animals encode complex olfactory scenes to track the plume far from the source remains unclear. Here we focus on the coding of the plume temporal dynamics in moths. We compare responses of olfactory receptor neurons (ORNs) and antennal lobe projection neurons (PNs) to sequences of pheromone stimuli either with white-noise patterns or with realistic turbulent temporal structures simulating a large range of distances (8 to 64 m) from the odor source. For the first time, we analyze what information is extracted by the olfactory system at large distances from the source. Neuronal responses are analyzed using linear-nonlinear models fitted with white-noise stimuli and used for predicting responses to turbulent stimuli. We found that neuronal firing rate is less correlated with the dynamic odor time course when distance to the source increases because of improper coding during long odor and no-odor events that characterize large distances. Rapid adaptation during long puffs does not preclude however the detection of puff transitions in PNs. Individual PNs but not individual ORNs encode the onset and offset of odor puffs for any temporal structure of stimuli. A higher spontaneous firing rate coupled to an inhibition phase at the end of PN responses contributes to this coding property. This allows PNs to decode the temporal structure of the odor plume at any distance to the source, an essential piece of information moths can use in their tracking behavior

Pheromone Receptor Knock-Out Affects Pheromone Detection and Brain Structure in a Moth

International audienceSex pheromone receptors are crucial in insects for mate finding and contribute to species premating isolation. Many pheromone receptors have been functionally characterized, especially in moths, but loss of function studies are rare. Notably, the potential role of pheromone receptors in the development of the macroglomeruli in the antennal lobe (the brain structures processing pheromone signals) is not known. Here, we used CRISPR-Cas9 to knock-out the receptor for the major component of the sex pheromone of the noctuid moth Spodoptera littoralis, and investigated the resulting effects on electrophysiological responses of peripheral pheromone-sensitive neurons and on the structure of the macroglomeruli. We show that the inactivation of the receptor specifically affected the responses of the corresponding antennal neurons did not impact the number of macroglomeruli in the antennal lobe but reduced the size of the macroglomerulus processing input from neurons tuned to the main pheromone component. We suggest that this mutant neuroanatomical phenotype results from a lack of neuronal activity due to the absence of the pheromone receptor and potentially reduced neural connectivity between peripheral and antennal lobe neurons. This is the first evidence of the role of a moth pheromone receptor in macroglomerulus development and extends our knowledge of the different functions odorant receptors can have in insect neurodevelopment

Transcriptome Profiling of Starvation in the Peripheral Chemosensory Organs of the Crop Pest <i>Spodoptera littoralis</i> Caterpillars

Starvation is frequently encountered by animals under fluctuating food conditions in nature, and response to it is vital for life span. Many studies have investigated the behavioral and physiological responses to starvation. In particular, starvation is known to induce changes in olfactory behaviors and olfactory sensitivity to food odorants, but the underlying mechanisms are not well understood. Here, we investigated the transcriptional changes induced by starvation in the chemosensory tissues of the caterpillar Spodoptera littoralis, using Illumina RNA sequencing. Gene expression profiling revealed 81 regulated transcripts associated with several biological processes, such as glucose metabolism, immune defense, response to stress, foraging activity, and olfaction. Focusing on the olfactory process, we observed changes in transcripts encoding proteins putatively involved in the peri-receptor events, namely, chemosensory proteins and odorant-degrading enzymes. Such modulation of their expression may drive fluctuations in the dynamics and the sensitivity of the olfactory receptor neuron response. In combination with the enhanced presynaptic activity mediated via the short neuropeptide F expressed during fasting periods, this could explain an enhanced olfactory detection process. Our observations suggest that a coordinated transcriptional response of peripheral chemosensory organs participates in the regulation of olfactory signal reception and olfactory-driven behaviors upon starvation

Neuronal coding varies with time sub-regions during turbulent stimuli.

<p>(A) Four different sub-regions of stimulus sequences were defined with (a) onset of puffs, (b) end of long puffs, (c) offset of puffs and (d) end of long blanks; see text for detailed definition. (B) (ORNs and in dotted grey the subpopulation of ORNs stimulated with pheromone loads of 10^-5 and 10⁻⁴ ng) and (C) (PNs): median values and bootstrap confidence intervals (95%) of firing rate in the 4 sub-regions. (D) Correlation coefficient between consecutive responses of PNs to a sequence turbulent stimuli for the 4 sub-regions defined in (A). Distance was 16 m. Cell number = 13. For each cell, 4 grey dots joined by a grey line represent the median values of correlation coefficients θ during sub-regions. Black line joins the median values. Bottom: dual tests between sub-regions (*: p<0.05, **: p<0.01, ***: p<0.001, n.s.: non-significant, Wilcoxon’s signed rank tests). (E) Correlation coefficient between L-N prediction and ORN responses for the 4 sub-regions. Responses to all distances and doses are pulled together. Same conventions as in (D). (F) Correlation coefficient between L-N prediction and PN responses for the 4 sub-regions. Same conventions as in (D). (G) Correlation coefficient between L-N prediction and measured responses during the onset of puffs depends on the time delay from the end of the preceding puff. Plot shows median values and bootstrap confidence intervals. Grey: ORNs, dotted grey: subpopulation of ORNs stimulated with pheromone loads of 10⁻⁵ and 10⁻⁴ ng, black: PNs. Both for ORNs and for PNs, values with the same letters are not statistically different within a set of neurons (Wilcoxon’s signed rank test, p>0.05). (H) Correlation coefficient at the end of puffs depends on the duration of the preceding puff. Same convention as in (G).</p