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Neurally Encoding Time for Olfactory Navigation

DOI: 10.1371/journal.pcbi.1004682

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Abstract:

Accurately encoding time is one of the fundamental challenges faced by the nervous system in mediating behavior. We recently reported that some animals have a specialized population of rhythmically active neurons in their olfactory organs with the potential to peripherally encode temporal information about odor encounters. If these neurons do indeed encode the timing of odor arrivals, it should be possible to demonstrate that this capacity has some functional significance. Here we show how this sensory input can profoundly influence an animal’s ability to locate the source of odor cues in realistic turbulent environments—a common task faced by species that rely on olfactory cues for navigation. Using detailed data from a turbulent plume created in the laboratory, we reconstruct the spatiotemporal behavior of a real odor field. We use recurrence theory to show that information about position relative to the source of the odor plume is embedded in the timing between odor pulses. Then, using a parameterized computational model, we show how an animal can use populations of rhythmically active neurons to capture and encode this temporal information in real time, and use it to efficiently navigate to an odor source. Our results demonstrate that the capacity to accurately encode temporal information about sensory cues may be crucial for efficient olfactory navigation. More generally, our results suggest a mechanism for extracting and encoding temporal information from the sensory environment that could have broad utility for neural information processing.

References

[1]  Fleet D, Wagner H, Heeger D. Neural encoding of binocular disparity: energy models, position shifts and phase shifts. Vision Res. 1996;36:1839–1857. doi: 10.1016/0042-6989(95)00313-4. pmid:8759452
[2]  Grothe B, Pecka M, McAlpine D. Mechanisms of sound localization in mammals. Physiol Rev. 2010;90:983–1012. doi: 10.1152/physrev.00026.2009. pmid:20664077
[3]  Bregman AS. Auditory Scene Analysis: The Perceptual Organization of Sound. Cambridge: MIT press; 1994.
[4]  Ache BW. Phylogeny of smell and taste. In: Getchell T, Bartoshuk L, Doty R, Snow J, editors. Smell and Taste in Health and Disease. New York: Raven Press; 1991.
[5]  Mountain DC, Hubbard AE. Sensing scenes with silicon. Biol Bull. 2001;200:227–234. doi: 10.2307/1543321. pmid:11341589
[6]  Porter J, Craven B, Khan RM, Chang SJ, Kang I, Judkewicz B, et al. Mechanisms of scent-tracking in humans. Nature Neuroscience. 2007;10:27–29. doi: 10.1038/nn0207-263d. pmid:17173046
[7]  Murlis J, Elkington JS, Cardé RT. Odor plumes and how insects use them. Annu Rev Entomol. 1992;37:505–532. doi: 10.1146/annurev.en.37.010192.002445.
[8]  Atema J. Chemical signals in the marine environment: dispersal, detection, and temporal signal analysis. Proc Natl Acad Sci USA. 1992;92(62–66). doi: 10.1073/pnas.92.1.62.
[9]  Weissburg MJ. The fluid dynamical context of chemosensory behavior. Biol Bull. 2000;198(188–202). doi: 10.2307/1542523. pmid:10786940
[10]  van Breugel F, Dickinson MH. Plume-Tracking behavior of flying Drosophila emerges from a set of distinct sensory-motor reflexes. Current Biology. 2014;24:274–286. doi: 10.1016/j.cub.2013.12.023. pmid:24440395
[11]  Riffell JA, Shlizerman E, Sanders E, Abrell L, Medina B, Hinterwirth AJ, et al. Flower discrimination by pollinators in a dynamic chemical environment. Science. 2014;344:1515–1518. doi: 10.1126/science.1251041. pmid:24970087
[12]  Balkovsky E, Shraiman B. Olfactory search at high Reynolds number. Proc Natl Acad Sci USA. 2002;99(20):12589. doi: 10.1073/pnas.192393499. pmid:12228727
[13]  Vergassola M, Villermaux E, Shraiman B. ‘Infotaxis’ as a strategy for searching without gradients. Nature. 2007;445(7126):406–409. doi: 10.1038/nature05464. pmid:17251974
[14]  Celani A, Villermaux E, Vergassola M. Odor landscapes in turbulent environments. Phys Rev X. 2014;4:041015. doi: 10.1103/physrevx.4.041015
[15]  Hein AM, McKinley SA. Sensing and decision-making in random search. Proc Natl Acad Sci USA. 2012;109(30):12070–12074. doi: 10.1073/pnas.1202686109. pmid:22778446
[16]  Gardiner JM, Atema J. Sharks need the lateral line to locate odor sources: rheotaxis and eddy chemotaxis. J Exp Biol. 2007;210:1925–1934. doi: 10.1242/jeb.000075. pmid:17515418
[17]  Gardiner JM, Atema J. The function of bilateral odor arrival time differences in olfactory orientation of sharks. Current Biology. 2010;20:1187–1191. doi: 10.1016/j.cub.2010.04.053. pmid:20541411
[18]  Reidenbach MA, Koehl MA. The spatial and temporal patterns of odors sampled by lobsters and crabs in a turbulent plume. J Exp Biol. 2011;214:3138–3153. doi: 10.1242/jeb.057547. pmid:21865526
[19]  Park IM, Bobkov YV, Ache BW, Príncipe . Intermittency coding in the primary olfactory system: a neural substrate for olfactory scene analysis. J Neurosci. 2014;34:941–952. doi: 10.1523/JNEUROSCI.2204-13.2014. pmid:24431452
[20]  Bobkov YV, Ache BW. Intrinsically bursting olfactory receptor neurons. J Neurophysiol. 2007;97:1052–1057. doi: 10.1152/jn.01111.2006. pmid:17135465
[21]  Reisert J, Matthews HR. Response properties of isolated mouse olfactory receptor cells. J Physiol. 2001;530:1130122. doi: 10.1111/j.1469-7793.2001.0113m.x.
[22]  Sicard G. Electrophysiological recordings from olfactory receptor cells in adult mice. Brain Res. 1986;397:405–408. doi: 10.1016/0006-8993(86)90648-7. pmid:3801881
[23]  Frings S, Lindemann B. Odorant response of isolated olfactory receptor cells is blocked by amiloride. J Membr Biol. 1988;105:233–242. doi: 10.1007/BF01871000. pmid:3265442
[24]  Arnson HA, Holy TE. Chemosensory burst coding by mouse vomeronasal sensory neuyrons. J Neurophysiol. 2011;106:409–420. doi: 10.1152/jn.00108.2011. pmid:21525370
[25]  Schulze A, Gomez-Martin A, G RV, Lott G, Musy M, Ahammad P, et al. Dynamical feature extraction at the sensory periphery guides chemotaxis. eLife. 2015;4:e06694. doi: 10.7554/eLife.06694.
[26]  Ganguili S, Huh D, Sompolinsky H. Memory traces in dynamical systems. Proc Natl Acad Sci USA. 2008;105:18970–18975. doi: 10.1073/pnas.0804451105.
[27]  Laje R, Buonomano DV. Robust timing and motor patterns by taming chaos in recurrent neural networks. Nat Neurosci. 2013;16:925–933. doi: 10.1038/nn.3405. pmid:23708144
[28]  Bueti D. The sensory representation of time. Front Integr Neurosci. 2011;5:34. doi: 10.3389/fnint.2011.00034. pmid:21852967
[29]  Reisert J, Matthews HR. Response to prolonged odour stimulation in frog olfactory receptor cells. J Physiol. 2001;534:179–191. doi: 10.1111/j.1469-7793.2001.t01-1-00179.x. pmid:11433001
[30]  Jones CD. On the structure of instantaneous plumes in the atmosphere. J Hazard Mater. 1983;7:87–112. doi: 10.1016/0304-3894(83)80001-6.
[31]  Murlis J, Willis MA, Cardé RT. Spatial and temporal structures of pheromone plumes in fields and forests. Physiol Entomol. 2000;25:211–222. doi: 10.1046/j.1365-3032.2000.00176.x.
[32]  Hein AM, McKinley SA. Senory information and encounter rates of interacting species. PLoS Comp Biol. 2013;9:e1003178. doi: 10.1371/journal.pcbi.1003178.
[33]  Shelhamer M. Nonlinear Dynamics in Physiology: a State-Space Approach. Hackensack: World Scientific; 2006.
[34]  Iwanski JS, Bradley E. Recurrence plots of experimental data: to embed or not to embed? Chaos. 1998;8:861–871. doi: 10.1063/1.166372. pmid:12779793
[35]  Takens F. Detecting strange attractors in turbulence. In: Dynamical Systems and Turbulence, Warwick 1980. vol. 898. Berlin, Heidelberg: Springer; 1981. p. 366–381.
[36]  Poincaré H. On the three-body problem and the equations of dynamics. In: Brush SG, Hall NS, editors. The Kinetic Theory of Gases. London: Imperial College Press; 1890. p. 368–376.
[37]  Barreira L. Poincaré recurrence: old and new. In: Zambrini JC, editor. XIVth International Congress on Mathematical Physics. Hackensack: World Scienrific; 2006. p. 415–422.
[38]  Eckmann JP, Kamphorst SO, Ruelle D. Recurrence plots of dynamical systems. Europhys Lett. 1987;4:973–977. doi: 10.1209/0295-5075/4/9/004.
[39]  Gao JB. Recurrence time statistics for chaotic ystems and their applications. Phys Rev Lett. 1999;83:3178–3181. doi: 10.1103/PhysRevLett.83.3178.
[40]  Ngamga EJ. Distinguishing dynamics using recurrence-time statistics. Phys Rev E. 2012;85:026217. doi: 10.1103/PhysRevE.85.026217.
[41]  Reeder PB, Ache BW. Chemotaxis in the Florida spiny lobster, Panulirus argus. Anim Behav. 1980;28:831–839. doi: 10.1016/S0003-3472(80)80143-6.
[42]  Grasso FW, Consi TR, Mountain DC, Atema J. Biomimetic robot lobster performs chemo-orientation in turbulence using a pair of spatially separated sensors: Progress and challenges. Rob Auton Syst. 2000;30:115–131. doi: 10.1016/S0921-8890(99)00068-8.
[43]  Moore PA, Scholz N, Atema J. Chemical orientation of lobsters, Homarus americanus, in turbulent odor plumes. J Chem Ecol. 1991;17:1293–1307. doi: 10.1007/BF00983763. pmid:24257791
[44]  Kozlowski C, Yopak K, Voigt R, Atema J. An initial study on the effects of signal intermittency on the odor plume tracking behavior of the American lobster, Homarus americanus. Biol Bull. 2001;201:274–276. doi: 10.2307/1543362. pmid:11687420
[45]  Masson JB. Olfactory searches with limited space perception. Proc Natl Acad Sci USA. 2013;110:11261–11266. doi: 10.1073/pnas.1221091110. pmid:23803855
[46]  van Breugel F, Riffell J, Fairhall A, Dickinson MH. Mosquitoes use vision to associate odor plumes with thermal targets. Curr Biol. 2015;25:2123–2129. doi: 10.1016/j.cub.2015.06.046. pmid:26190071
[47]  Tabuchi M, Sakurai T, Mitsuno H, Namiki S, Minegishi R, Shiotsuki T, et al. Pheromone responsiveness threshold depends on temporal integration by antennal lobe projection neurons. Proc Natl Acad Sci USA. 2013;110:15455–15460. doi: 10.1073/pnas.1313707110. pmid:24006366
[48]  Szyszka P, Stierle JS, Biergans S, Galizia CG. The speed of smell: odor-object segregation within milliseconds. PLoS One. 2012;7:e36096. doi: 10.1371/journal.pone.0036096. pmid:22558344
[49]  Rokni D, Hemmelder V, Kapoor V, Murthy VN. An olfactory cocktail party: figure-ground segregation of odorants in rodents. Nature Neuroscience. 2014;17:1225–1232. doi: 10.1038/nn.3775. pmid:25086608
[50]  Ukhanov K, Bobkov YV, Ache BW. Imaging ensemble activity in arthropod olfactory receptor neurons in situ. Cell Calcium. 2011;49:100–107. doi: 10.1016/j.ceca.2010.10.009. pmid:21232792
[51]  Finelli CM, Pentcheff ND, Zimmer-Faust RK, Wethey DS. Odor transport in turbulent flows: Constraints on animal navigation. Limnol Oceanogr. 1999;44:1056–1071. doi: 10.4319/lo.1999.44.4.1056.
[52]  Elkington JS, Cardé RT, Mason CJ. Evaluation of time-average dispersion models for estimating pheromone concentration in a deciduous forest. J Chem Ecol. 1984;10:1081–1108. doi: 10.1007/BF00987515.

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