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.

Institute of Ecology and Environmental Sciences INRA Versailles France

Institute of Physiology of the Czech Academy of Sciences Prague Czech Republic

Peuplements végétaux et bioagresseurs en milieu végétal CIRAD Université de la Réunion Saint Pierre Ile de la Réunion France

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Jones CD. Structure of instantaneous plumes in the atmosphere. J Hazard Mat. 1983;7(2):87–112. 10.1016/0304-3894(83)80001-6 DOI

Murlis J. Odor plumes and the signal they provide In: Carde RT, Minks A, editors. Insect Pheromone Research: New Directions. New York: Chapman and Hall; 1996. p. 221–231.

Celani A, Villermaux E, Vergassola M. Odor Landscapes in Turbulent Environments. Phys Rev X. 2014;4:041015.

Mylne KR, Mason PJ. Concentration fluctuation measurements in a dispersing plume at a range of up to 1000m. Q J Roy Meteo Soc. 1991;117(497):177–206. 10.1002/qj.49711749709 DOI

Murlis J, Willis MA, Cardé RT. Spatial and temporal structures of pheromone plumes in fields and forests. Physiol Entomol. 2000;25(3):211–222. 10.1046/j.1365-3032.2000.00176.x DOI

Willis MA, Ford EA, Avondet JL. Odor tracking flight of male Manduca sexta moths along plumes of different cross-sectional area. J Comp Physiol A. 2013;199(11):1015–1036. 10.1007/s00359-013-0856-0 PubMed DOI

Jacob V, Monsempès C, Rospars JP, Masson JB, Lucas P. Olfactory coding in the turbulent realm. PLoS Comput Biol. 2017;13(12):e1005870 10.1371/journal.pcbi.1005870 PubMed DOI PMC

Dean I, Harper NS, McAlpine D. Neural population coding of sound level adapts to stimulus statistics. Nat Neurosci. 2005;8(12):1684–1689. 10.1038/nn1541 PubMed DOI

Wen B, Wang GI, Dean I, Delgutte B. Dynamic range adaptation to sound level statistics in the auditory nerve. J Neurosci. 2009;29(44):13797–13808. 10.1523/JNEUROSCI.5610-08.2009 PubMed DOI PMC

Durant S, Clifford CWG, Crowder NA, Price NSC, Ibbotson MR. Characterizing contrast adaptation in a population of cat primary visual cortical neurons using Fisher information. J Opt Soc Am A. 2007;24(6):1529–1537. 10.1364/JOSAA.24.001529 PubMed DOI

Barlow HB. Possible principles underlying the transformation of sensory messages In: Rosenblith W, editor. Sensory Communication. Cambridge: MIT Press; 1961. p. 217–234.

Simoncelli EP, Olshausen BA. Natural image statistics and neural representation. Annu Rev Neurosci. 2001;24:1193–1216. 10.1146/annurev.neuro.24.1.1193 PubMed DOI

Lewicki MS. Efficient coding of natural sounds. Nat Neurosci. 2002;5(4):356–363. 10.1038/nn831 PubMed DOI

Wark B, Lundstrom BN, Fairhall A. Sensory adaptation. Curr Opin Neurobiol. 2007;17:423–429. 10.1016/j.conb.2007.07.001 PubMed DOI PMC

Kostal L, Lansky P, Rospars JP. Efficient olfactory coding in the pheromone receptor neuron of a moth. PLoS Comput Biol. 2008;4:e1000053 10.1371/journal.pcbi.1000053 PubMed DOI PMC

Watkins PV, Barbour DL. Specialized neuronal adaptation for preserving input sensitivity. Nat Neurosci. 2008;11(11):1259–1261. 10.1038/nn.2201 PubMed DOI

Watkins PV, Barbour DL. Level-Tuned Neurons in Primary Auditory Cortex Adapt Differently to Loud versus Soft Sounds. Cereb Cortex. 2011;21(1):178–190. 10.1093/cercor/bhq079 PubMed DOI PMC

Dahmen JC, Keating P, Nodal FR, Schulz AL, King AJ. Adaptation to Stimulus Statistics in the Perception and Neural Representation of Auditory Space. Neuron. 2010;66:937–948. 10.1016/j.neuron.2010.05.018 PubMed DOI PMC

Maier JK, Hehrmann P, Harper NS, Klump GM, Pressnitzer D, McAlpine D. Adaptive coding is constrained to midline locations in a spatial listening task. J Neurophysiol. 2012;108:1856–1868. 10.1152/jn.00652.2011 PubMed DOI PMC

Garcia-Lazaro JA, Ho SSM, Nair A, Schnupp JWH. Shifting and scaling adaptation to dynamic stimuli in somatosensory cortex. Eur J Neurosci. 2007;26:2359–2368. 10.1111/j.1460-9568.2007.05847.x PubMed DOI

Baker TC, Haynes KF. Field and laboratory electroantennographic measurements of pheromone plume structure correlated with oriental fruit moth behaviour. Physiol Entomol. 1989;14(1):1–12. 10.1111/j.1365-3032.1989.tb00931.x DOI

Poitout S, Buès R. Elevage de chenilles de vingt-huit espèces de Lépidoptères Noctuidae et de deux espèces d’Arctiidae sur milieu artificiel simple. Particularitès de l’èlevage selon les espèces. Ann Zool Ecol Anim. 1974;6(3):431–441.

R Core Team. R: A Language and Environment for Statistical Computing; 2017.

Hansson BS. Olfaction in Lepidoptera. Experientia. 1995;51:1003–1027. 10.1007/BF01946910 DOI

Tamborrino M, Ditlevsen S, Lansky P. Identification of noisy response latency. Phys Rev E. 2012;86:021128 10.1103/PhysRevE.86.021128 PubMed DOI

Levakova M, Tamborrino M, Ditlevsen S, Lansky P. A review of the methods for neuronal response latency estimation. Biosystems. 2015;136:23–34. 10.1016/j.biosystems.2015.04.008 PubMed DOI

Baker T, Haynes KF. Manoeuvres used by flying male oriental fruit moths to relocate a sex pheromone plume in an experimentally shifted wind-field. Physiol Entomol. 1987;12(3):263–279. 10.1111/j.1365-3032.1987.tb00751.x DOI

Dayan P, Abbott LF. The Effect of Correlated Variability on the Accuracy of a Population Code. Neural Comput. 1999;11(1):91–101. 10.1162/089976699300016827 PubMed DOI

Harper NS, McAlpine D. Optimal neural population coding of an auditory spatial cue. Nature. 2004;430(7000):682–686. 10.1038/nature02768 PubMed DOI

Greenwood PE, Lansky P. Optimum signal in a simple neuronal model with signal-dependent noise. Biol Cybern. 2005;92(3):199–205. 10.1007/s00422-005-0545-3 PubMed DOI

Jeffreys H. An invariant form for the prior probability in estimation problems. Proc Roy Soc A. 1946; p. 453–461. 10.1098/rspa.1946.0056 PubMed DOI

Berens P, Ecker AS, Gerwinn S, Tolias AS, Bethge M. Reassessing optimal neural population codes with neurometric functions. Proc Natl Acad Sci USA. 2011;108(11):4423–4428. 10.1073/pnas.1015904108 PubMed DOI PMC

Lehmann EL, Casella G. Theory of point estimation. New York: Springer Verlag; 1998.

Seung HS, Sompolinsky H. Simple models for reading neuronal population codes. Proc Natl Acad Sci USA. 1993;90(10):749–753. PubMed PMC

Seriès P, Latham PE, Pouget A. Tuning curve sharpening for orientation selectivity: coding efficiency and the impact of correlations. Nat Neurosci. 2004;7(10):1129–1135. 10.1038/nn1321 PubMed DOI

Zhang K, Ginzburg I, McNaughton BL, Sejnowski TJ. Interpreting neuronal population activity by reconstruction: unified framework with application to hippocampal place cells. J Neurophysiol. 1998;79(2):1017–1044. 10.1152/jn.1998.79.2.1017 PubMed DOI

Sreenivasan S, Fiete I. Grid cells generate an analog error-correcting code for singularly precise neural computation. Nat Neurosci. 2011;14(10):1330–1337. 10.1038/nn.2901 PubMed DOI

Levakova M, Tamborrino M, Kostal L, Lansky P. Accuracy of rate coding: When shorter time window and higher spontaneous activity help. Phys Rev E. 2017;95(2):022310 10.1103/PhysRevE.95.022310 PubMed DOI

Rospars JP, Gremiaux A, Jarriault D, Chaffiol A, Monsempes C, Deisig N, et al. Heterogeneity and Convergence of Olfactory First-Order Neurons Account for the High Speed and Sensitivity of Second-Order Neurons. PLoS Comput Biol. 2014;10(12):e1003975 10.1371/journal.pcbi.1003975 PubMed DOI PMC

van Drongelen W, Holley A, Døving KB. Convergence in the olfactory system: quantitative aspects of odour sensitivity. J Theor Biol. 1978;71:39–48. 10.1016/0022-5193(78)90212-6 PubMed DOI

Laughlin SB. A simple coding procedure enhances a neuron’s information capacity. Z Naturforsch. 1981;36(9-10):910–912. 10.1515/znc-1981-9-1040 PubMed DOI

de Ruyter van Steveninck RR, Laughlin SB. The rate of information transfer at graded-potential synapses. Nature. 1996;379(6566):642–644. 10.1038/379642a0 DOI

Ikeda S, Manton JH. Capacity of a single spiking neuron channel. Neural Comput. 2009;21(6):1714–1748. 10.1162/neco.2009.05-08-792 PubMed DOI

Suksompong P, Berger T. Capacity analysis for integrate-and-fire neurons with descending action potential thresholds. IEEE Trans Inf Theory. 2010;56(2):838–851. 10.1109/TIT.2009.2037042 DOI

Kostal L, Kobayashi R. Optimal decoding and information transmission in Hodgkin-Huxley neurons under metabolic cost constraints. BioSystems. 2015;136:3–10. 10.1016/j.biosystems.2015.06.008 PubMed DOI

Bernardo JM. Reference posterior distributions for Bayesian inference. J Roy Stat Soc B. 1979;41:113–147.

Brunel N, Nadal JP. Mutual information, Fisher information, and population coding. Neural Comput. 1998;10(7):1731–1757. 10.1162/089976698300017115 PubMed DOI

McDonnell MD, Stocks NG. Maximally informative stimuli and tuning curves for sigmoidal rate-coding neurons and populations. Phys Rev Lett. 2008;101(5):058103 10.1103/PhysRevLett.101.058103 PubMed DOI

Ganguli D, Simoncelli EP. Implicit encoding of prior probabilities in optimal neural populations In: Lafferty J, Williams C, Shawe-Taylor J, Zemel RS, Culotta A, editors. Advances in Neural Information Processing Systems (NIPS). vol. 23 Cambridge, Massachusetts: MIT Press; 2010. p. 658–666. PubMed PMC

Yarrow S, Challis E, Seriès P. Fisher and Shannon information in finite neural populations. Neural Comput. 2012;24(7):1740–1780. 10.1162/NECO_a_00292 PubMed DOI

Kostal L, Lansky P, McDonnell MD. Metabolic cost of neuronal information in an empirical stimulus-response model. Biol Cybern. 2013;107(3):355–365. 10.1007/s00422-013-0554-6 PubMed DOI

Shannon CE. Communication in the presence of noise. Proc IRE. 1949;37(1):10–21. 10.1109/JRPROC.1949.232969 DOI

Rieke F, de Ruyter van Steveninck RR, Warland D, Bialek W. Spikes: Exploring the Neural Code. Cambridge: MIT Press; 1997.

Kostal L. Stimulus reference frame and neural coding precision. J Math Psychol. 2016;71:22–27. 10.1016/j.jmp.2016.02.006 DOI

Wicher D. Tuning Insect Odorant Receptors. Front Cell Neurosci. 2018;12:94 10.3389/fncel.2018.00094 PubMed DOI PMC

Nakagawa T, Vosshall LB. Controversy and consensus: noncanonical signaling mechanisms in the insect olfactory system. Curr Opin Neurobiol. 2009;19(3):284–292. 10.1016/j.conb.2009.07.015 PubMed DOI PMC

Stengl M. Pheromone transduction in moths. Front Cell Neurosci. 2010;4:1–15. 10.3389/fncel.2010.00133 PubMed DOI PMC

Fleischer J, Pregitzer P, Breer H, Krieger J. Access to the odor world: olfactory receptors and their role for signal transduction in insects. Cell Mol Life Sci. 2018;75(3):485–508. 10.1007/s00018-017-2627-5 PubMed DOI PMC

Stengl M, Funk NW. The role of the coreceptor Orco in insect olfactory transduction. J Comp Physiol. 2013;199(11):897–909. 10.1007/s00359-013-0837-3 PubMed DOI

Wilson RI. Early olfactory processing in Drosophila: mechanisms and principles. Annu Rev Neurosci. 2013;36:217–241. 10.1146/annurev-neuro-062111-150533 PubMed DOI PMC

Cao LH, Jing BY, Yang D, Zeng X, Shen Y, Tu Y, et al. Distinct signaling of Drosophila chemoreceptors in olfactory sensory neurons. Proc Natl Acad Sci USA. 2016;113(7):E902–E911. 10.1073/pnas.1518329113 PubMed DOI PMC

Kaissling KE, Strausfeld CZ, Rumbo E. Adaptation processes in insect olfactory receptors. Ann NY Acad Sci. 1987;510(1):104–112. 10.1111/j.1749-6632.1987.tb43475.x PubMed DOI

Dolzer J, Fischer K, Stengl M. Adaptation in pheromone-sensitive trichoid sensilla of the hawkmoth Manduca sexta. J Exp Biol. 2003;206(9):1575–1588. 10.1242/jeb.00302 PubMed DOI

Lucas P, Shimahara T. Voltage- and calcium-activated currents in cultured olfactory receptor neurons of male Mamestra brassicae (Lepidoptera). Chem Senses. 2002;27(7):599–610. 10.1093/chemse/27.7.599 PubMed DOI

Kawai F. Ca2+-activated K+ currents regulate odor adaptation by modulating spike encoding of olfactory receptor cells. Biophys J. 2002;82(4):2005–2015. 10.1016/S0006-3495(02)75549-5 PubMed DOI PMC

Guo H, Kunwar K, Smith D. Odorant receptor sensitivity modulation in Drosophila. J Neurosci. 2017;37(39):9465–9473. 10.1523/JNEUROSCI.1573-17.2017 PubMed DOI PMC

Nolte A, Gawalek P, Koerte S, Wei H, Schumann R, Werckenthin A, et al. No evidence for ionotropic pheromone transduction in the Hawkmoth Manduca sexta. PLoS One. 2016;11(11):e0166060 10.1371/journal.pone.0166060 PubMed DOI PMC

Gorur-Shandilya S, Demir M, Long J, Clark DA, Emonet T. Olfactory receptor neurons use gain control and complementary kinetics to encode intermittent odorant stimuli. Elife. 2017;6:e27670 10.7554/eLife.27670 PubMed DOI PMC

The effect of inhibition on rate code efficiency indicators

Adaptive integrate-and-fire model reproduces the dynamics of olfactory receptor neuron responses in a moth