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Information about space from time: how mammals navigate the odour landscape

  • Tobias Ackels

    Tobias Ackels is a senior postdoctoral researcher at the Francis Crick Institute in London. He received his Diploma in Biology from RWTH Aachen University, where he also completed his PhD studies in 2015 in the Department of Chemosensation with Prof. Marc Spehr. His doctoral research mainly focused on signalling mechanisms in the olfactory system. Supported by a postdoctoral fellowship from the DFG, he moved to the laboratory of Prof. Andreas Schaefer at the Francis Crick Institute, where his interest lies in the investigation of how natural sensory stimuli are perceived and processed in the mammalian brain on the cellular and network level using physiological and behavioural techniques.

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Published/Copyright: June 14, 2022
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Neuroforum
From the journal Neuroforum Volume 28 Issue 3

Abstract

Sensory input across modalities is highly dynamic, continuously confronting the brain with the task of making sense of the external world. Olfaction is a key sense that many species depend on for survival, for example to locate food sources and mating partners or to avoid encountering predators. In the absence of visual cues, olfactory cues are especially useful, as they provide information over a large range of distances. Natural odours form temporally complex plumes that show rapid fluctuations in odour concentration carrying information about the location of an odour source. This review focuses on how primarily mammals use this spatial information from olfactory cues to navigate their environment. I highlight progress made on the physical description of dynamically fluctuating odours, behavioural paradigms to investigate odour-guided navigation and review initial findings on the underlying neural mechanisms that allow mammals to extract spatial information from the dynamic odour landscape.

Zusammenfassung

Sensorische Eindrücke aller Sinnesmodalitäten sind hoch dynamisch und stellen das Gehirn ununterbrochen vor die Aufgabe, die Außenwelt in ihrer Gesamtheit zu erfassen. Der Geruchssinn spielt für viele Spezies eine überlebenswichtige Rolle, zum Beispiel um Nahrungsquellen und Artgenossen zu finden, oder Begegnungen mit Raubtieren zu vermeiden. Olfaktorische Signale liefern sensorische Information über kurze und lange Entfernungen, auch wenn optische Eindrücke fehlen. Natürliche Gerüche bilden komplexe Duftwolken mit rapide fluktuierender Konzentration, die Informationen über den Ort einer Geruchsquelle tragen. Dieser Artikel gibt einen Überblick darüber wie vor allem Säugetiere räumliche Information aus Geruchssignalen ziehen können, um ihre Umwelt zu navigieren. Beleuchtet werden Fortschritte in der physikalischen Beschreibung dynamischer Gerüche, Verhaltensparadigmen zur Untersuchung olfaktorischer Navigation, sowie erste Erkenntisse über potentielle zu Grunde liegende neuronale Mechanismen, die es Säugern erlauben, räumliche Information aus der dynamischen Geruchswelt zu erlangen.

Keywords: active sampling; navigation; odour plume; olfaction; temporally complex structure
Schlüsselwörter: aktives Samplen; Duftwolke; Geruchssinn; Navigation; zeitlich komplexe Struktur
Corresponding author: Tobias Ackels, Sensory Circuits and Neurotechnology Laboratory, The Francis Crick Institute, London, UK, E-mail:

Funding source: Medical Research Council

Award Identifier / Grant number: FC001153

Funding source: Wellcome Trust

Award Identifier / Grant number: 110174/Z/15/Z

Award Identifier / Grant number: FC001153

Funding source: Cancer Research UK

Award Identifier / Grant number: FC001153

Funding source: Deutsche Forschungsgemeinschaft

Award Identifier / Grant number: Postdoctoral fellowship

Funding source: NeuroNex program

Award Identifier / Grant number: From Odor to Action

About the author

Tobias Ackels

Tobias Ackels is a senior postdoctoral researcher at the Francis Crick Institute in London. He received his Diploma in Biology from RWTH Aachen University, where he also completed his PhD studies in 2015 in the Department of Chemosensation with Prof. Marc Spehr. His doctoral research mainly focused on signalling mechanisms in the olfactory system. Supported by a postdoctoral fellowship from the DFG, he moved to the laboratory of Prof. Andreas Schaefer at the Francis Crick Institute, where his interest lies in the investigation of how natural sensory stimuli are perceived and processed in the mammalian brain on the cellular and network level using physiological and behavioural techniques.

Acknowledgments

TA is thankful to A. Schaefer and A.C. Marin for valuable comments on an earlier version of this manuscript and all members of the Sensory Circuits and Neurotechnology Laboratory for fruitful discussions.

  1. Author contribution: The author has accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: This work was supported by the Francis Crick Institute which receives its core funding from Cancer Research UK (FC001153), the UK Medical Research Council (FC001153), and the Wellcome Trust (FC001153); a Wellcome Investigator Award to A. Schaefer (110174/Z/15/Z); the NeuroNex program “From Odor to Action” to A. Schaefer and a DFG postdoctoral fellowship to TA.

  3. Conflict of interest statement: The author declares no conflicts of interest.

References

Abraham, N.M., Spors, H., Carleton, A., Margrie, T.W., Kuner, T., and Schaefer, A.T. (2004). Maintaining accuracy at the expense of speed: stimulus similarity defines odor discrimination time in mice. Neuron 44, 865–876, https://doi.org/10.1016/s0896-6273(04)00753-6.Search in Google Scholar

Ackels, T., Erskine, A., Dasgupta, D., Marin, A.C., Warner, T.P.A., Tootoonian, S., Fukunaga, I., Harris, J.J., and Schaefer, A.T. (2021). Fast odour dynamics are encoded in the olfactory system and guide behaviour. Nature 593, 558–563, https://doi.org/10.1038/s41586-021-03514-2.Search in Google Scholar

Arakawa, H., Arakawa, K., Blanchard, D.C., and Blanchard, R.J. (2008). A new test paradigm for social recognition evidenced by urinary scent marking behavior in C57BL/6J mice. Behav. Brain Res. 190, 97–104, https://doi.org/10.1016/j.bbr.2008.02.009.Search in Google Scholar

Baker, K.L., Dickinson, M., Findley, T.M., Gire, D.H., Louis, M., Suver, M.P., Verhagen, J.V., Nagel, K.I., and Smear, M.C. (2018). Algorithms for olfactory search across species. J. Neurosci. 38, 9383–9389, https://doi.org/10.1523/jneurosci.1668-18.2018.Search in Google Scholar

Bekesy, G.von (1964). Olfactory analogue to directional hearing. J. Appl. Physiol. 19, 369–373, https://doi.org/10.1152/jappl.1964.19.3.369.Search in Google Scholar

Benhamou, S. (1989). An olfactory orientation model for mammals’ movements in their home ranges. J. Theor. Biol. 139, 379–388, https://doi.org/10.1016/s0022-5193(89)80216-4.Search in Google Scholar

Bhattacharyya, U. and Singh Bhalla, U. (2015). Robust and rapid air borne odor tracking without casting. ENeuro 2, https://doi.org/10.1523/eneuro.0102-15.2015.Search in Google Scholar

Boie, S.D., Connor, E.G., McHugh, M., Nagel, K.I., Ermentrout, G.B., Crimaldi, J.P., and Victor, J.D. (2018). Information-theoretic analysis of realistic odor plumes: what cues are useful for determining location? PLoS Comput. Biol. 14, 1–19, https://doi.org/10.1371/journal.pcbi.1006275.Search in Google Scholar PubMed PubMed Central

Bolding, K.A., and Franks, K.M. (2017). Complementary codes for odor identity and intensity in olfactory cortex. Elife 6, 1–26, https://doi.org/10.7554/elife.22630.Search in Google Scholar PubMed PubMed Central

Brown, S.L., Joseph, J., and Stopfer, M. (2005). Encoding a temporally structured stimulus with a temporally structured neural representation. Nat. Neurosci. 8, 1568–1576, https://doi.org/10.1038/nn1559.Search in Google Scholar PubMed

Cardé, R.T., and Willis, M.A. (2008). Navigational strategies used by insects to find distant, wind-borne sources of odor. J. Chem. Ecol. 34, 854–866, https://doi.org/10.1007/s10886-008-9484-5.Search in Google Scholar PubMed

Catania, K.C. (2013). Stereo and serial sniffing guide navigation to an odour source in a mammal. Nat. Commun. 4, 1441, https://doi.org/10.1038/ncomms2444.Search in Google Scholar PubMed

Celani, A., Villermaux, E., and Vergassola, M. (2014). Odor landscapes in turbulent environments. Phys. Rev. X 4, 041015, https://doi.org/10.1103/physrevx.4.041015.Search in Google Scholar

Chapman, P.D., Burkland, R., Bradley, S.P., Houot, B., Bullman, V., Dacks, A.M., and Daly, K.C. (2018). Flight motor networks modulate primary olfactory processing in the moth Manduca sexta. Proc. Natl. Acad. Sci. U. S. A. 115, 5588–5593, https://doi.org/10.1073/pnas.1722379115.Search in Google Scholar PubMed PubMed Central

Chong, E., Moroni, M., Wilson, C., Shoham, S., Panzeri, S., and Rinberg, D. (2020). Manipulating synthetic optogenetic odors reveals the coding logic of olfactory perception. Science 368, eaba2357, https://doi.org/10.1126/science.aba2357.Search in Google Scholar PubMed PubMed Central

Connor, E.G., McHugh, M.K., and Crimaldi, J.P. (2018). Quantification of airborne odor plumes using planar laser-induced fluorescence. Exp. Fluids 59, 0, https://doi.org/10.1007/s00348-018-2591-3.Search in Google Scholar

Crimaldi, J.P., and Koseff, J.R. (2001). High-resolution measurements of the spatial and temporal scalar structure of a turbulent plume. Exp. Fluids 31, 90–102, https://doi.org/10.1007/s003480000263.Search in Google Scholar

Crimaldi, J., Lei, H., Schaefer, A., Schmuker, M., Smith, B.H., True, A.C., Verhagen, J.V., and Victor, J.D. (2022). Active sensing in a dynamic olfactory world. J. Comput. Neurosci. 50, 1–6, https://doi.org/10.1007/s10827-021-00798-1.Search in Google Scholar PubMed

Cury, K.M., and Uchida, N. (2010). Robust odor coding via inhalation-coupled transient activity in the mammalian olfactory bulb. Neuron 68, 570–585, https://doi.org/10.1016/j.neuron.2010.09.040.Search in Google Scholar PubMed

Dasgupta, D., Warner, T.P.A., Erskine, A., and Schaefer, A.T. (2022). Coupling of mouse olfactory bulb projection neurons to fluctuating odour pulses. J. Neurosci. 42, 4278–4296, https://doi.org/10.1523/JNEUROSCI.1422-21.2022.Search in Google Scholar PubMed PubMed Central

Demir, M., Kadakia, N., Anderson, H.D., Clark, D.A., and Emonet, T. (2020). Walking Drosophila navigate complex plumes using stochastic decisions biased by the timing of odor encounters. Elife 9, 1–31, https://doi.org/10.7554/elife.57524.Search in Google Scholar

Devine, D.V., and Atema, J. (1982). Function of chemoreceptor organs in spatial orientation of the lobster, Homarus americanus: differences and overlap. Biol. Bull. 163, 144–153, https://doi.org/10.2307/1541504.Search in Google Scholar

Esquivelzeta Rabell, J., Mutlu, K., Noutel, J., Martin del Olmo, P., and Haesler, S. (2017). Spontaneous rapid odor source localization behavior requires interhemispheric communication. Curr. Biol. 27, 1542–1548.e4, https://doi.org/10.1016/j.cub.2017.04.027.Search in Google Scholar PubMed

Feldman, J.L., Del Negro, C.A., and Gray, P.A. (2013). Understanding the rhythm of breathing: so near, yet so far. Annu. Rev. Physiol. 75, 423–452, https://doi.org/10.1146/annurev-physiol-040510-130049.Search in Google Scholar PubMed PubMed Central

Findley, T.M., Wyrick, D.G., Cramer, J.L., Brown, M.A., Holcomb, B., Attey, R., Yeh, D., Monasevitch, E., Nouboussi, N., Cullen, I., et al.. (2021). Sniff-synchronized, gradient-guided olfactory search by freely moving mice. Elife 10, 1–39, https://doi.org/10.7554/elife.58523.Search in Google Scholar PubMed PubMed Central

Fischler-Ruiz, W., Clark, D., Joshi, N., Devi-Chou, V., Kitch, L., Schnitzer, M.J., Abbott, L.F., and Axel, R. (2021). Olfactory landmarks and path integration converge to form a cognitive spatial map. Neuron 109, 4036–4049.e5.10.1016/j.neuron.2021.09.055Search in Google Scholar

Geffen, M.N., Broome, B.M., Laurent, G., and Meister, M. (2009). Neural encoding of rapidly fluctuating odors. Neuron 61, 570–586, https://doi.org/10.1016/j.neuron.2009.01.021.Search in Google Scholar PubMed

Gire, D.H., Kapoor, V., Arrighi-Allisan, A., Seminara, A., and Murthy, V.N. (2016). Mice develop efficient strategies for foraging and navigation using complex natural stimuli. Curr. Biol. 26, 1261–1273, https://doi.org/10.1016/j.cub.2016.03.040.Search in Google Scholar PubMed PubMed Central

Grimaud, J., and Murthy, V.N. (2018). How to monitor breathing in laboratory rodents: a review of the current methods. J. Neurophysiol. 120, 624–632, https://doi.org/10.1152/jn.00708.2017.Search in Google Scholar PubMed PubMed Central

Gumaste, A., Coronas-Samano, G., Hengenius, J., Axman, R., Connor, E.G., Baker, K.L., Ermentrout, B., Crimaldi, J.P., and Verhagen, J.V. (2020). A comparison between mouse, in silico, and robot odor plume navigation reveals advantages of mouse odor tracking. eNeuro 7, https://doi.org/10.1523/ENEURO.0212-19.2019.Search in Google Scholar PubMed PubMed Central

Hepper, P.G., and Wells, D.L. (2005). How many footsteps do dogs need to determine the direction of an odour trail? Chem. Senses 30, 291–298, https://doi.org/10.1093/chemse/bji023.Search in Google Scholar PubMed

Hopfield, J.J. (1991). Olfactory computation and object perception. Proc. Natl. Acad. Sci. Unit. States Am. 88, 6462–6466, https://doi.org/10.1073/pnas.88.15.6462.Search in Google Scholar PubMed PubMed Central

Hurst, J.L., and Beynon, R.J. (2004). Scent wars: the chemobiology of competitive signalling in mice. BioEssays News Rev. Mol. Cell. Dev. Biol. 26, 1288–1298, https://doi.org/10.1002/bies.20147.Search in Google Scholar PubMed

Huston, S.J., Stopfer, M., Cassenaer, S., Aldworth, Z.N., and Laurent, G. (2015). Neural encoding of odors during active sampling and in turbulent plumes. Neuron 88, 403–418, https://doi.org/10.1016/j.neuron.2015.09.007.Search in Google Scholar PubMed PubMed Central

Jackson, B.J., Fatima, G.L., Oh, S., and Gire, D.H. (2020). Many paths to the same goal: balancing exploration and exploitation during probabilistic route planning. ENeuro 7, 1–11, https://doi.org/10.1523/eneuro.0536-19.2020.Search in Google Scholar PubMed PubMed Central

Jacobs, L.F., Arter, J., Cook, A., and Sulloway, F.J. (2015). Olfactory orientation and navigation in humans. PLoS One 10, 1–13, https://doi.org/10.1371/journal.pone.0129387.Search in Google Scholar PubMed PubMed Central

Jones, P.W. and Urban, N.N. (2018). Mice Follow Odor Trails Using Stereo Olfactory Cues and Rapid Sniff to Sniff Comparisons. bioRxiv 293746, https://doi.org/10.1101/293746.10.1101/293746Search in Google Scholar

Jordan, R., Fukunaga, I., Kollo, M., and Schaefer, A.T. (2018). Active sampling state dynamically enhances olfactory bulb odor representation. Neuron 98, 1214–1228, https://doi.org/10.1016/j.neuron.2018.05.016.Search in Google Scholar PubMed PubMed Central

Justus, K.A., Murlis, J., Jones, C., and Cardé, R.T. (2002). Measurement of odor-plume structure in a wind tunnel using a photoionization detector and a tracer gas. Environ. Fluid Mech. 2, 115–142, https://doi.org/10.1023/a:1016227601019.10.1023/A:1016227601019Search in Google Scholar

Kepecs, A., Uchida, N., and Mainen, Z.F. (2006). The sniff as a unit of olfactory processing. Chem. Senses 31, 167–179, https://doi.org/10.1093/chemse/bjj016.Search in Google Scholar PubMed

Khan, A.G., Sarangi, M., and Bhalla, U.S. (2012). Rats track odour trails accurately using a multi-layered strategy with near-optimal sampling. Nat. Commun. 3, 703, https://doi.org/10.1038/ncomms1712.Search in Google Scholar PubMed

Kim, A.J., Lazar, A.A., and Slutskiy, Y.B. (2011). System identification of Drosophila olfactory sensory neurons. J. Comput. Neurosci. 30, 143–161, https://doi.org/10.1007/s10827-010-0265-0.Search in Google Scholar PubMed PubMed Central

Lewis, S.M., Xu, L., Rigolli, N., Tariq, M.F., Stern, M., Seminara, A., and Gire, D.H. (2021). Plume dynamics structure the spatiotemporal activity of glomerular networks in the mouse olfactory bulb. Front. Cell. Neurosci. 15, 633757, https://doi.org/10.3389/fncel.2021.633757.Search in Google Scholar PubMed PubMed Central

Li, A., Gire, D.H., Bozza, T., and Restrepo, D. (2014). Precise detection of direct glomerular input duration by the olfactory bulb. J. Neurosci. 34, 16058–16064, https://doi.org/10.1523/jneurosci.3382-14.2014.Search in Google Scholar PubMed PubMed Central

Li, C., Dong, H., and Zhao, K. (2018). A balance between aerodynamic and olfactory performance during flight in Drosophila. Nat. Commun. 9, 1–8, https://doi.org/10.1038/s41467-018-05708-1.Search in Google Scholar PubMed PubMed Central

Liu, A., Papale, A.E., Hengenius, J., Patel, K., Ermentrout, B., and Urban, N.N. (2020). Mouse navigation strategies for odor source localization. Front. Neurosci. 14, 1–16, https://doi.org/10.3389/fnins.2020.00218.Search in Google Scholar PubMed PubMed Central

Mafra-Neto, A., and Cardé, R.T. (1994). Fine-scale structure of pheromone plumes modulates upwind orientation of flying moths. Nature 369, 142–144, https://doi.org/10.1038/369142a0.Search in Google Scholar

Marin, A.C., Schaefer, A.T., and Ackels, T. (2021). Spatial information from the odour environment in mammalian olfaction. Cell Tissue Res. 383, 473–483, https://doi.org/10.1007/s00441-020-03395-3.Search in Google Scholar PubMed PubMed Central

Mathis, A., Mamidanna, P., Cury, K.M., Abe, T., Murthy, V.N., Mathis, M.W., and Bethge, M. (2018). DeepLabCut: markerless pose estimation of user-defined body parts with deep learning. Nat. Neurosci. 21, 1281–1289, https://doi.org/10.1038/s41593-018-0209-y.Search in Google Scholar PubMed

McAfee, S.S., Ogg, M.C., Ross, J.M., Liu, Y., Fletcher, M.L., and Heck, D.H. (2016). Minimally invasive highly precise monitoring of respiratory rhythm in the mouse using an epithelial temperature probe. J. Neurosci. Methods 263, 89–94, https://doi.org/10.1016/j.jneumeth.2016.02.007.Search in Google Scholar PubMed PubMed Central

Meister, M. (2015). On the dimensionality of odor space. eLife, 4, e07865, pp. 1–12. https://doi.org/10.7554/eLife.07865.Search in Google Scholar PubMed PubMed Central

Moore, P., and Crimaldi, J. (2004). Odor landscapes and animal behavior: tracking odor plumes in different physical worlds. J. Mar. Syst. 49, 55–64, https://doi.org/10.1016/j.jmarsys.2003.05.005.Search in Google Scholar

Moore, P.A., and Atema, J. (1991). Spatial information in the three-dimensional fine structure of an aquatic odor plume. Biol. Bull. 181, 408–418, https://doi.org/10.2307/1542361.Search in Google Scholar PubMed

Mori, K., Nagao, H., and Yoshihara, Y. (1999). The olfactory bulb: coding and processing of odor molecule information. Science 286, 711–715, https://doi.org/10.1126/science.286.5440.711.Search in Google Scholar PubMed

Murlis, J., Elkington, J.S., and Carde, R.T. (1992). Odor plumes and how insects use them. Annu. Rev. Entomol. 37, 505–532, https://doi.org/10.1146/annurev.en.37.010192.002445.Search in Google Scholar

Murlis, J., Willis, M.A., and Cardé, R.T. (2000). Spatial and temporal structures of pheromone plumes in fields and forests. Physiol. Entomol. 25, 211–222, https://doi.org/10.1046/j.1365-3032.2000.00176.x.Search in Google Scholar

Mylne, K.R., and Mason, P.J. (1991). Concentration fluctuation measurements in a dispersing plume at a range of up to 1000m. Q. J. R. Meteorol. Soc. 117, 177–206, https://doi.org/10.1256/smsqj.49708.Search in Google Scholar

Parabucki, A., Bizer, A., Morris, G., Munoz, A.E., Bala, A.D.S., Smear, M., and Shusterman, R. (2019). Odor concentration change coding in the olfactory bulb. eNeuro. https://doi.org/10.1523/ENEURO.0396-18.2019.Search in Google Scholar PubMed PubMed Central

Poo, C., Agarwal, G., Bonacchi, N., and Mainen, Z.F. (2021). Spatial maps in piriform cortex during olfactory navigation. Nature 601, 595–599, https://doi.org/10.1038/s41586-021-04242-3.Search in Google Scholar PubMed

Porter, J., Craven, B., Khan, R.M., Chang, S.J., Kang, I., Judkewitz, B., Volpe, J., Settles, G., and Sobel, N. (2007). Mechanisms of scent-tracking in humans. Nat. Neurosci. 10, 27–29, https://doi.org/10.1038/nn1819.Search in Google Scholar PubMed

Radvansky, B.A., and Dombeck, D.A. (2018). An olfactory virtual reality system for mice. Nat. Commun. 9, 839, https://doi.org/10.1038/s41467-018-03262-4.Search in Google Scholar PubMed PubMed Central

Radvansky, B.A., Oh, J.Y., Climer, J.R., and Dombeck, D.A. (2021). Behavior determines the hippocampal spatial mapping of a multisensory environment. Cell Rep. 36, 109444, https://doi.org/10.1016/j.celrep.2021.109444.Search in Google Scholar PubMed PubMed Central

Raiser, G., Galizia, C.G., and Szyszka, P. (2017). A high-bandwidth dual-channel olfactory stimulator for studying temporal sensitivity of olfactory processing. Chem. Senses 42, 141–151, https://doi.org/10.1093/chemse/bjw114.Search in Google Scholar PubMed

Rajan, R., Clement, J., and Bhalla, U. (2006). Rats smell in stereo. Science 311, 666–670, https://doi.org/10.1126/science.1122096.Search in Google Scholar

Rebello, M.R., McTavish, T.S., Willhite, D.C., Short, S.M., Shepherd, G.M., and Verhagen, J.V. (2014). Perception of odors linked to precise timing in the olfactory system. PLoS Biol. 12, e1002021, https://doi.org/10.1371/journal.pbio.1002021.Search in Google Scholar

Reddy, G., Murthy, V.N., and Vergassola, M. (2022a). Olfactory sensing and navigation in turbulent environments. Annu. Rev. Condens. Matter Phys. 13, 191–213, https://doi.org/10.1146/annurev-conmatphys-031720-032754.Search in Google Scholar

Reddy, G., Shraiman, B.I., and Vergassola, M. (2022b). Sector search strategies for odor trail tracking. Proc. Natl. Acad. Sci. U. S. A. 119, 1–8, https://doi.org/10.1073/pnas.2107431118.Search in Google Scholar

Reeder, P.B., and Ache, B.W. (1980). Chemotaxis in the Florida spiny lobster, Panulirus argus. Anim. Behav. 28, 831–839, https://doi.org/10.1016/s0003-3472(80)80143-6.Search in Google Scholar

Reisert, J., Golden, G.J., Matsumura, K., Smear, M., Rinberg, D., and Gelperin, A. (2014). Comparing thoracic and intra-nasal pressure transients to monitor active odor sampling during odor-guided decision making in the mouse. J. Neurosci. Methods 221, 8–14, https://doi.org/10.1016/j.jneumeth.2013.09.006.Search in Google Scholar

Riffell, J.A., Sanders, E., Hinterwirth, A.J., Abrell, L., Shlizerman, E., Medina, B., and Kutz, J.N. (2014). Flower discrimination by pollinators in a dynamic chemical environment. Science 344, 1515–1518, https://doi.org/10.1126/science.1251041.Search in Google Scholar

van Rijzingen, I.M.S., Gispen, W.H., and Spruijt, B.M. (1995). Olfactory bulbectomy temporarily impairs Morris maze performance: an ACTH(4-9) analog accellerates return of function. Physiol. Behav. 58, 147–152, https://doi.org/10.1016/0031-9384(95)00032-e.Search in Google Scholar

Schmuker, M., Bahr, V., and Huerta, R. (2016). Exploiting plume structure to decode gas source distance using metal-oxide gas sensors. Sensor. Actuator. B Chem. 235, 636–646, https://doi.org/10.1016/j.snb.2016.05.098.Search in Google Scholar

Schwenk, K. (1994). Why snakes have forked tongues. Science 263, 1573–1577, https://doi.org/10.1126/science.263.5153.1573.Search in Google Scholar PubMed

Shraiman, B.I., Siggia, E.D., Shralman, B.I., and Siggia, E.D. (2000). Scalar turbulence. Nature 405, 639, https://doi.org/10.1038/35015000.Search in Google Scholar PubMed

Shusterman, R., Smear, M.C., Koulakov, A.A., and Rinberg, D. (2011). Precise olfactory responses tile the sniff cycle. Nat. Neurosci. 14, 1039–1044, https://doi.org/10.1038/nn.2877.Search in Google Scholar PubMed

Smear, M., Shusterman, R., O’Connor, R., Bozza, T., and Rinberg, D. (2011). Perception of sniff phase in mouse olfaction. Nature 479, 397–400, https://doi.org/10.1038/nature10521.Search in Google Scholar PubMed

Smear, M., Resulaj, A., Zhang, J., Bozza, T., and Rinberg, D. (2013). Multiple perceptible signals from a single olfactory glomerulus. Nat. Neurosci. 2013, 1687–1691, https://doi.org/10.1186/2044-7248-3-s1-o11.Search in Google Scholar

Stierle, J.S., Galizia, C.G., and Szyszka, P. (2013). Millisecond stimulus onset-asynchrony enhances information about components in an odor mixture. J. Neurosci. 33, 6060–6069, https://doi.org/10.1523/jneurosci.5838-12.2013.Search in Google Scholar PubMed PubMed Central

Szyszka, P., Stierle, J.S., Biergans, S., and Galizia, C.G. (2012). The speed of smell: odor-object segregation within milliseconds. PLoS One 7, 4–7, https://doi.org/10.1371/journal.pone.0036096.Search in Google Scholar PubMed PubMed Central

Szyszka, P., Gerkin, R.C., Galizia, C.G., and Smith, B.H. (2014). High-speed odor transduction and pulse tracking by insect olfactory receptor neurons. Proc. Natl. Acad. Sci. Unit. States Am. 111, 16925–16930, https://doi.org/10.1073/pnas.1412051111.Search in Google Scholar PubMed PubMed Central

Tariq, M.F., Lewis, S.M., Lowell, A., Moore, S., Miles, J.T., Perkel, D.J., and Gire, D.H. (2021). Using head-mounted ethanol sensors to monitor olfactory information and determine behavioral changes associated with ethanol-plume contact during mouse odor-guided navigation. eNeuro 8, https://doi.org/10.1523/ENEURO.0285-20.2020.Search in Google Scholar PubMed PubMed Central

Thesen, A., Steen, J.B., and Døving, K.B. (1993). Behaviour of dogs during olfactory tracking. J. Exp. Biol. 180, 247–251, https://doi.org/10.1242/jeb.180.1.247.Search in Google Scholar PubMed

Uchida, N., and Mainen, Z.F. (2003). Speed and accuracy of olfactory discrimination in the rat. Nat. Neurosci. 6, 1224–1229, https://doi.org/10.1038/nn1142.Search in Google Scholar PubMed

Vergassola, M., Villermaux, E., and Shraiman, B.I. (2007). “Infotaxis” as a strategy for searching without gradients. Nature 445, 406–409, https://doi.org/10.1038/nature05464.Search in Google Scholar

Verhagen, J.V., Wesson, D.W., Netoff, T.I., White, J.A., and Wachowiak, M. (2007). Sniffing controls an adaptive filter of sensory input to the olfactory bulb. Nat. Neurosci. 10, 631–639, https://doi.org/10.1038/nn1892.Search in Google Scholar

Vickers, N.J. (2000). Mechanisms of animal navigation in odor plumes. Biol. Bull. 198, 203–212, https://doi.org/10.2307/1542524.Search in Google Scholar

Wachowiak, M. (2011). All in a sniff: olfaction as a model for active sensing. Neuron 71, 962–973, https://doi.org/10.1016/j.neuron.2011.08.030.Search in Google Scholar

Wallace, D.G., Gorny, B., and Whishaw, I.Q. (2002). Rats can track odors, other rats, and themselves: implications for the study of spatial behavior. Behav. Brain Res. 131, 185–192, https://doi.org/10.1016/s0166-4328(01)00384-9.Search in Google Scholar

Weissburg, M.J., Dusenbery, D.B., Ishida, H., Janata, J., Keller, T., Roberts, P.J.W., and Webster, D.R. (2002). A multidisciplinary study of spatial and temporal scales containing information in turbulent chemical plume tracking. Environ. Fluid Mech. 2, 65–94, https://doi.org/10.1023/a:1016223500111.10.1023/A:1016223500111Search in Google Scholar

Welker, W.I. (1964). Analysis of sniffing of the albino rat. Behaviour 22, 223–244, https://doi.org/10.1163/156853964x00030.Search in Google Scholar

Wesson, D.W., Donahou, T.N., Johnson, M.O., and Wachowiak, M. (2008). Sniffing behavior of mice during performance in odor-guided tasks. Chem. Senses 33, 581–596, https://doi.org/10.1093/chemse/bjn029.Search in Google Scholar PubMed PubMed Central

Wu, Y., Chen, K., Ye, Y., Zhang, T., and Zhou, W. (2020). Humans navigate with stereo olfaction. Proc. Natl. Acad. Sci. U. S. A. 117, 16065–16071, https://doi.org/10.1073/pnas.2004642117.Search in Google Scholar PubMed PubMed Central

Published Online: 2022-06-14
Published in Print: 2022-08-26

© 2022 Walter de Gruyter GmbH, Berlin/Boston

Articles in the same Issue

  1. Frontmatter
  2. Editorial
  3. Editorial
  4. Review articles
  5. Perireceptor events and peripheral modulation of olfactory signals in the olfactory epithelium of vertebrates
  6. Mammalian social memory relies on neuromodulation in the olfactory bulb
  7. How the body rules the nose
  8. Information about space from time: how mammals navigate the odour landscape
  9. Functional role of the anterior olfactory nucleus in sensory information processing
  10. How the sense of smell influences cognition throughout life
  11. Presentation of scientific institutions
  12. The “MultiSensE” consortium
  13. Nachrichten aus der Gesellschaft
  14. Nachrichten aus der Gesellschaft
https://doi.org/10.1515/nf-2022-0006
Keywords for this article
active sampling; navigation; odour plume; olfaction; temporally complex structure

Articles in the same Issue

  1. Frontmatter
  2. Editorial
  3. Editorial
  4. Review articles
  5. Perireceptor events and peripheral modulation of olfactory signals in the olfactory epithelium of vertebrates
  6. Mammalian social memory relies on neuromodulation in the olfactory bulb
  7. How the body rules the nose
  8. Information about space from time: how mammals navigate the odour landscape
  9. Functional role of the anterior olfactory nucleus in sensory information processing
  10. How the sense of smell influences cognition throughout life
  11. Presentation of scientific institutions
  12. The “MultiSensE” consortium
  13. Nachrichten aus der Gesellschaft
  14. Nachrichten aus der Gesellschaft
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