Adaptive integrate-and-fire model reproduces the dynamics of olfactory receptor neuron responses in a moth
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
31387478
PubMed Central
PMC6731495
DOI
10.1098/rsif.2019.0246
Knihovny.cz E-zdroje
- Klíčová slova
- adaptive threshold, integrate-and-fire model, olfactory receptor neuron,
- MeSH
- akční potenciály fyziologie MeSH
- biologické modely MeSH
- čichové buňky účinky léků fyziologie MeSH
- elektrofyziologické jevy MeSH
- fyziologická adaptace * MeSH
- můry fyziologie MeSH
- sexuální lákadla farmakologie MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- sexuální lákadla MeSH
In order to understand how olfactory stimuli are encoded and processed in the brain, it is important to build a computational model for olfactory receptor neurons (ORNs). Here, we present a simple and reliable mathematical model of a moth ORN generating spikes. The model incorporates a simplified description of the chemical kinetics leading to olfactory receptor activation and action potential generation. We show that an adaptive spike threshold regulated by prior spike history is an effective mechanism for reproducing the typical phasic-tonic time course of ORN responses. Our model reproduces the response dynamics of individual neurons to a fluctuating stimulus that approximates odorant fluctuations in nature. The parameters of the spike threshold are essential for reproducing the response heterogeneity in ORNs. The model provides a valuable tool for efficient simulations of olfactory circuits.
Department of Informatics SOKENDAI 2 1 2 Hitotsubashi Chiyoda ku Tokyo Japan
Institute of Ecology and Environmental Sciences INRA route de St Cyr 78000 Versailles France
Zobrazit více v PubMed
Hildebrand JG, Shepherd GM. 1997. Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu. Rev. Neurosci. 20, 595–631. (10.1146/annurev.neuro.20.1.595) PubMed DOI
Wilson RI, Mainen ZF. 2006. Early events in olfactory processing. Annu. Rev. Neurosci. 29, 163–201. (10.1146/annurev.neuro.29.051605.112950) PubMed DOI
Lánský P, Rospars J-P. 1998. Odorant concentration and receptor potential in olfactory sensory neurons. BioSystems 48, 131–138. (10.1016/S0303-2647(98)00058-6) PubMed DOI
Lindemann B. 2001. Predicted profiles of ion concentrations in olfactory cilia in the steady state. Biophys. J. 80, 1712–1721. (10.1016/S0006-3495(01)76142-5) PubMed DOI PMC
Suzuki N, Takahata M, Sato K. 2002. Oscillatory current responses of olfactory receptor neurons to odorants and computer simulation based on a cyclic AMP transduction model. Chem. Senses 27, 789–801. (10.1093/chemse/27.9.789) PubMed DOI
Dougherty DP, Wright GA, Yew AC. 2005. Computational model of the cAMP-mediated sensory response and calcium-dependent adaptation in vertebrate olfactory receptor neurons. Proc. Natl Acad. Sci. USA 102, 10 415–10 420. (10.1073/pnas.0504099102) PubMed DOI PMC
Gu Y, Lucas P, Rospars J-P. 2009. Computational model of the insect pheromone transduction cascade. PLOS Comput. Biol. 5, e1000321 (10.1371/journal.pcbi.1000321) PubMed DOI PMC
Kaissling K-E. 2009. Olfactory perireceptor and receptor events in moths: a kinetic model revised. J. Comp. Physiol. A 195, 895–922. (10.1007/s00359-009-0461-4) PubMed DOI PMC
Schmuker M, Yamagata N, Nawrot M, Menzel R. 2011. Parallel representation of stimulus identity and intensity in a dual pathway model inspired by the olfactory system of the honeybee. Front. Neuroeng. 4, 17 (10.3389/fneng.2011.00017) PubMed DOI PMC
Wessnitzer J, Young JM, Armstrong JD, Webb B. 2012. A model of non-elemental olfactory learning in Drosophila. J. Comput. Neurosci. 32, 197–212. (10.1007/s10827-011-0348-6) PubMed DOI
Kee T, Sanda P, Gupta N, Stopfer M, Bazhenov M. 2015. Feed-forward versus feedback inhibition in a basic olfactory circuit. PLOS Comput. Biol. 11, e1004531 (10.1371/journal.pcbi.1004531) PubMed DOI PMC
MaBouDi H, Shimazaki H, Giurfa M, Chittka L. 2017. Olfactory learning without the mushroom bodies: spiking neural network models of the honeybee lateral antennal lobe tract reveal its capacities in odour memory tasks of varied complexities. PLoS Comput. Biol. 13, e1005551 (10.1371/journal.pcbi.1005551) PubMed DOI PMC
Rospars J-P, Lánský P, Tuckwell HC, Vermeulen A. 1996. Coding of odor intensity in a steady-state deterministic model of an olfactory receptor neuron. J. Comput. Neurosci. 3, 51–72. (10.1007/BF00158337) PubMed DOI
Gorur-Shandilya S, Demir M, Long J, Clark DA, Emonet T. 2017. Olfactory receptor neurons use gain control and complementary kinetics to encode intermittent odorant stimuli. Elife 6, e27670 (10.7554/eLife.27670) PubMed DOI PMC
Kostal L, Lansky P, Rospars J-P. 2008. Efficient olfactory coding in the pheromone receptor neuron of a moth. PLoS Comput. Biol. 4, e1000053 (10.1371/journal.pcbi.1000053) PubMed DOI PMC
Rospars J-P, Lánský P, Křivan V. 2003. Extracellular transduction events under pulsed stimulation in moth olfactory sensilla. Chem. Senses 28, 509–522. (10.1093/chemse/28.6.509) PubMed DOI
Gu Y, Rospars J-P. 2011. Dynamical modeling of the moth pheromone-sensitive olfactory receptor neuron within its sensillar environment. PLoS ONE 6, e17422 (10.1371/journal.pone.0017422) PubMed DOI PMC
Reingruber J, Holcman D. 2009. Gated narrow escape time for molecular signaling. Phys. Rev. Lett. 103, 148102 (10.1103/PhysRevLett.103.148102) PubMed DOI
Lapicque L. 1907. Recherches quantitatives sur lexcitation electrique des nerfs traitee comme une polarization. J. Physiol. Pathol. Gen. 9, 620–635.
Stein RB. 1965. A theoretical analysis of neuronal variability. Biophys. J. 5, 173–194. (10.1016/S0006-3495(65)86709-1) PubMed DOI PMC
Burkitt AN. 2006. A review of the integrate-and-fire neuron model: I. Homogeneous synaptic input. Biol. Cybern. 95, 1–19. (10.1007/s00422-006-0068-6) PubMed DOI
Rauch A, La Camera G, Luscher H-R, Senn W, Fusi S. 2003. Neocortical pyramidal cells respond as integrate-and-fire neurons to in vivo-like input currents. J. Neurophysiol. 90, 1598–1612. (10.1152/jn.00293.2003) PubMed DOI
Jolivet R, Kobayashi R, Rauch A, Naud R, Shinomoto S, Gerstner W. 2008. A benchmark test for a quantitative assessment of simple neuron models. J. Neurosci. Methods 169, 417–424. (10.1016/j.jneumeth.2007.11.006) PubMed DOI
Borisyuk R. 2002. Oscillatory activity in the neural networks of spiking elements. BioSystems 67, 3–16. (10.1016/S0303-2647(02)00058-8) PubMed DOI
Helias M, Deger M, Diesmann M, Rotter S. 2010. Equilibrium and response properties of the integrate-and-fire neuron in discrete time. Front. Comput. Neurosci. 3, 29 (10.3389/neuro.10.029.2009) PubMed DOI PMC
Lánský P, Rospars J-P, Vermeulen A. 1994. Basic mechanisms of coding stimulus intensity in the olfactory sensory neuron. Neural Process. Lett. 1, 9–12. (10.1007/bf02312394) DOI
Celani A, Villermaux E, Vergassola M. 2014. Odor landscapes in turbulent environments. Phys. Rev. X 4, 041015 (10.1103/physrevx.4.041015) DOI
Grémiaux A, Nowotny T, Martinez D, Lucas P, Rospars J-P. 2012. Modelling the signal delivered by a population of first-order neurons in a moth olfactory system. Brain Res. 1434, 123–135. (10.1016/j.brainres.2011.09.035) PubMed DOI
Rospars J-P, Grémiaux A, Jarriault D, Chaffiol A, Monsempes C, Deisig N, Anton S, Lucas P, Martinez D. 2014. Heterogeneity and convergence of olfactory first-order neurons account for the high speed and sensitivity of second-order neurons. PLoS Comp. Biol. 10, e1003975 (10.1371/journal.pcbi.1003975) PubMed DOI PMC
Kaissling K-E. 2001. Olfactory perireceptor and receptor events in moths: a kinetic model. Chem. Senses 26, 125–150. (10.1093/chemse/26.2.125) PubMed DOI
Kaissling K-E, Rospars J-P. 2004. Dose-response relationships in an olfactory flux detector model revisited. Chem. Senses 29, 529–531. (10.1093/chemse/bjh057) PubMed DOI
Dayan P, Abbott LF. 2001. Theoretical neuroscience: computational and mathematical modeling of neural systems. Cambridge, UK: MIT Press.
Chacron MJ, Pakdaman K, Longtin A. 2003. Interspike interval correlations, memory, adaptation, and refractoriness in a leaky integrate-and-fire model with threshold fatigue. Neural Comput. 15, 253–278. (10.1162/089976603762552915) PubMed DOI
Jolivet R, Rauch A, Lüscher H-R, Gerstner W. 2006. Predicting spike timing of neocortical pyramidal neurons by simple threshold models. J. Comput. Neurosci. 21, 35–49. (10.1007/s10827-006-7074-5) PubMed DOI
Kobayashi R, Tsubo Y, Shinomoto S. 2009. Made-to-order spiking neuron model equipped with a multi-timescale adaptive threshold. Front. Comput. Neurosci. 3, 9 (10.3389/neuro.10.009.2009) PubMed DOI PMC
Kobayashi R, Kitano K. 2016. Impact of slow K+ currents on spike generation can be described by an adaptive threshold model. J. Comput. Neurosci. 40, 347–362. (10.1007/s10827-016-0601-0) PubMed DOI PMC
Rospars J-P, Křivan V, Lánský P. 2000. Perireceptor and receptor events in olfaction. Comparison of concentration and flux detectors: a modeling study. Chem. Senses 25, 293–311. (10.1093/chemse/25.3.293) PubMed DOI
Minor A, Kaissling K-E. 2003. Cell responses to single pheromone molecules may reflect the activation kinetics of olfactory receptor molecules. J. Comp. Physiol. A 189, 221–230. PubMed
Lucas P, Shimahara T. 2002. Voltage-and calcium-activated currents in cultured olfactory receptor neurons of male Mamestra brassicae (Lepidoptera). Chem. Senses 27, 599–610. (10.1093/chemse/27.7.599) PubMed DOI
Zufall F, Stengl M, Franke C, Hildebrand JG, Hatt H. 1991. Ionic currents of cultured olfactory receptor neurons from antennae of male Manduca sexta. J. Neurosci. 11, 956–965. (10.1523/JNEUROSCI.11-04-00956.1991) PubMed DOI PMC
Geffen MN, Broome BM, Laurent G, Meister M. 2009. Neural encoding of rapidly fluctuating odors. Neuron 61, 570–586. (10.1016/j.neuron.2009.01.021) PubMed DOI
Jacob V, Monsempès C, Rospars J-P, Masson J-B, Lucas P. 2017. Olfactory coding in the turbulent realm. PLoS Comput. Biol. 13, e1005870 (10.1371/journal.pcbi.1005870) PubMed DOI PMC
Grosmaitre X, Vassalli A, Mombaerts P, Shepherd GM, Ma M. 2006. Odorant responses of olfactory sensory neurons expressing the odorant receptor MOR23: a patch clamp analysis in gene-targeted mice. Proc. Natl Acad. Sci. USA 103, 1970–1975. (10.1073/pnas.0508491103) PubMed DOI PMC
Liu Y-H, Wang X-J. 2001. Spike-frequency adaptation of a generalized leaky integrate-and-fire model neuron. J. Comput. Neurosci. 10, 25–45. (10.1023/A:1008916026143) PubMed DOI
Nagel KI, Wilson RI. 2011. Biophysical mechanisms underlying olfactory receptor neuron dynamics. Nat. Neurosci. 14, 208–216. (10.1038/nn.2725) PubMed DOI PMC
Hopfield JJ. 1995. Pattern recognition computation using action potential timing for stimulus representation. Nature 376, 33–36. (10.1038/376033a0) PubMed DOI
Brody CD, Hopfield J. 2003. Simple networks for spike-timing-based computation, with application to olfactory processing. Neuron 37, 843–852. (10.1016/S0896-6273(03)00120-X) PubMed DOI
Cassenaer S, Laurent G. 2007. Hebbian STDP in mushroom bodies facilitates the synchronous flow of olfactory information in locusts. Nature 448, 709–713. (10.1038/nature05973) PubMed DOI
Coulon A, Beslon G, Soula HA. 2011. Enhanced stimulus encoding capabilities with spectral selectivity in inhibitory circuits by STDP. Neural Comput. 23, 882–908. (10.1162/NECO_a_00100) PubMed DOI
Kaissling K-E, Strausfeld CZ, Rumbo E. 1987. Adaptation processes in insect olfactory receptors. Ann. N. Y. Acad. Sci. 510, 104–112. (10.1111/j.1749-6632.1987.tb43475.x) PubMed DOI
Dolzer J, Fischer K, Stengl M. 2003. Adaptation in pheromone-sensitive trichoid sensilla of the hawkmoth Manduca sexta. J. Exp. Biol. 206, 1575–1588. (10.1242/jeb.00302) PubMed DOI
Goldman MS, Golowasch J, Marder E, Abbott L. 2001. Global structure, robustness, and modulation of neuronal models. J. Neurosci. 21, 5229–5238. (10.1523/JNEUROSCI.21-14-05229.2001) PubMed DOI PMC
Achard P, De-Schutter E. 2006. Complex parameter landscape for a complex neuron model. PLOS Comp. Biol. 2, e94 (10.1371/journal.pcbi.0020094) PubMed DOI PMC
Cao LH, Jing BY, Yang D, Zeng X, Shen Y, Tu Y, Luo DG. 2016. Distinct signaling of Drosophila chemoreceptors in olfactory sensory neurons. Proc. Natl Acad. Sci. USA 113, E902–E911. (10.1073/pnas.1518329113) PubMed DOI PMC
Kawai F. 2002. Ca2+-activated K+ currents regulate odor adaptation by modulating spike encoding of olfactory receptor cells. Biophys. J. 82, 2005–2015. (10.1016/S0006-3495(02)75549-5) PubMed DOI PMC
Wicher D. 2018. Tuning insect odorant receptors. Front. Cell. Neurosci. 12, 94 (10.3389/fncel.2018.00094) PubMed DOI PMC
Stengl M. 2010. Pheromone transduction in moths. Front. Cell. Neurosci. 4, 1–15. (10.3389/fncel.2010.00133) PubMed DOI PMC
Martelli C, Carlson JR, Emonet T. 2013. Intensity invariant dynamics and odor-specific latencies in olfactory receptor neuron response. J. Neurosci. 33, 6285–6297. (10.1523/JNEUROSCI.0426-12.2013) PubMed DOI PMC
Levakova M, Kostal L, Monsempès C, Jacob V, Lucas P. 2018. Moth olfactory receptor neurons adjust their encoding efficiency to temporal statistics of pheromone fluctuations. PLoS Comp. Biol. 14, e1006586 (10.1371/journal.pcbi.1006586) PubMed DOI PMC
Nolte A, Gawalek P, Koerte S, Wei H, Schumann R, Werckenthin A, Krieger J, Stengl M. 2016. No evidence for ionotropic pheromone transduction in the hawkmoth Manduca sexta. PLoS ONE 11, e0166060 (10.1371/journal.pone.0166060) PubMed DOI PMC
R Core Team. 2017. R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austria.
Poitout S, Bues R. 1974. Elevage de chenilles de vingt-huit espèces de Lépidoptères Noctuidae et de deux espèces d’arctiidae sur milieu artificiel simple. particularités de l’élevage selon les espèces. Ann. Zool. Ecol. Anim. 6, 431–441.
Nawrot M, Aertsen A, Rotter S. 1999. Single-trial estimation of neuronal firing rates: from single-neuron spike trains to population activity. J. Neurosci. Methods 94, 81–92. (10.1016/S0165-0270(99)00127-2) PubMed DOI
Shimazaki H, Shinomoto S. 2010. Kernel bandwidth optimization in spike rate estimation. J. Comput. Neurosci. 29, 171–182. (10.1007/s10827-009-0180-4) PubMed DOI PMC
Nelder JA, Mead R. 1965. A simplex method for function minimization. Comput. J. 7, 308–313. (10.1093/comjnl/7.4.308) DOI
The effect of inhibition on rate code efficiency indicators