1932

Abstract

Olfaction is fundamentally distinct from other sensory modalities. Natural odor stimuli are complex mixtures of volatile chemicals that interact in the nose with a receptor array that, in rodents, is built from more than 1,000 unique receptors. These interactions dictate a peripheral olfactory code, which in the brain is transformed and reformatted as it is broadcast across a set of highly interconnected olfactory regions. Here we discuss the problems of characterizing peripheral population codes for olfactory stimuli, of inferring the specific functions of different higher olfactory areas given their extensive recurrence, and of ultimately understanding how odor representations are linked to perception and action. We argue that, despite the differences between olfaction and other sensory modalities, addressing these specific questions will reveal general principles underlying brain function.

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2020-07-08
2024-04-13
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Literature Cited

  1. Abraham NM, Spors H, Carleton A, Margrie TW, Kuner T, Schaefer AT 2004. Maintaining accuracy at the expense of speed: Stimulus similarity defines odor discrimination time in mice. Neuron 44:865–76
    [Google Scholar]
  2. Adrian ED 1942. Olfactory reactions in the brain of the hedgehog. J. Physiol. 100:459–73
    [Google Scholar]
  3. Apfelbach R, Parsons M, Soini H, Novotny M 2015. Are single odorous components of a predator sufficient to elicit defensive behaviors in prey species. ? Front. Neurosci. 9:263
    [Google Scholar]
  4. Apicella A, Yuan Q, Scanziani M, Isaacson JS 2010. Pyramidal cells in piriform cortex receive convergent input from distinct olfactory bulb glomeruli. J. Neurosci. 30:14255–60
    [Google Scholar]
  5. Araneda RC, Kini AD, Firestein S 2000. The molecular receptive range of an odorant receptor. Nat. Neurosci. 3:1248–55
    [Google Scholar]
  6. Babadi B, Sompolinsky H 2014. Sparseness and expansion in sensory representations. Neuron 83:1213–26
    [Google Scholar]
  7. Baker KL, Dickinson M, Findley TM, Gire DH, Louis M et al. 2018. Algorithms for olfactory search across species. J. Neurosci. 38:9383–89
    [Google Scholar]
  8. Bao X, Raguet LL, Cole SM, Howard JD, Gottfried JA 2016. The role of piriform associative connections in odor categorization. eLife 5:e13732
    [Google Scholar]
  9. Bathellier B, Buhl DL, Accolla R, Carleton A 2008. Dynamic ensemble odor coding in the mammalian olfactory bulb: sensory information at different timescales. Neuron 57:586–98
    [Google Scholar]
  10. Bear DM, Lassance J-M, Hoekstra HE, Datta SR 2016. The evolving neural and genetic architecture of vertebrate olfaction. Curr. Biol. 26:R1039–49
    [Google Scholar]
  11. Bekkers JM, Suzuki N 2013. Neurons and circuits for odor processing in the piriform cortex. Trends Neurosci 36:429–38
    [Google Scholar]
  12. Bhattacharjee AS, Konakamchi S, Turaev D, Vincis R, Nunes D et al. 2019. Similarity and strength of glomerular odor representations define a neural metric of sniff-invariant discrimination time. Cell Rep 28:2966–78.e5
    [Google Scholar]
  13. Bolding KA, Franks KM 2017. Complementary codes for odor identity and intensity in olfactory cortex. eLife 6:e22630
    [Google Scholar]
  14. Bolding KA, Franks KM 2018. Recurrent cortical circuits implement concentration-invariant odor coding. Science 361:eaat6904
    [Google Scholar]
  15. Boyd AM, Sturgill JF, Poo C, Isaacson JS 2012. Cortical feedback control of olfactory bulb circuits. Neuron 76:1161–74
    [Google Scholar]
  16. Buck L, Axel R 1991. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175–87
    [Google Scholar]
  17. Burton SD 2017. Inhibitory circuits of the mammalian main olfactory bulb. J. Neurophysiol. 118:2034–51
    [Google Scholar]
  18. Burton SD, Wipfel M, Guo M, Eiting TP, Wachowiak M 2019. A novel olfactometer for efficient and flexible odorant delivery. Chem. Senses 44:173–88
    [Google Scholar]
  19. Butterwick JA, Del Marmol J, Kim KH, Kahlson MA, Rogow JA et al. 2018. Cryo-EM structure of the insect olfactory receptor Orco. Nature 560:447–52
    [Google Scholar]
  20. Chae H, Kepple DR, Bast WG, Murthy VN, Koulakov AA, Albeanu DF 2019. Mosaic representations of odors in the input and output layers of the mouse olfactory bulb. Nat. Neurosci. 22:1306–17
    [Google Scholar]
  21. Chapuis J, Wilson DA 2012. Bidirectional plasticity of cortical pattern recognition and behavioral sensory acuity. Nat. Neurosci. 15:155–61
    [Google Scholar]
  22. Chapuis J, Wilson DA 2013. Cholinergic modulation of olfactory pattern separation. Neurosci. Lett. 545:50–53
    [Google Scholar]
  23. Chen C-FF, Zou D-J, Altomare CG, Xu L, Greer CA, Firestein SJ 2014. Nonsensory target-dependent organization of piriform cortex. PNAS 111:16931–36
    [Google Scholar]
  24. Choi GB, Stettler DD, Kallman BR, Bhaskar ST, Fleischmann A, Axel R 2011. Driving opposing behaviors with ensembles of piriform neurons. Cell 146:1004–15
    [Google Scholar]
  25. Chu MW, Li WL, Komiyama T 2016. Balancing the robustness and efficiency of odor representations during learning. Neuron 92:174–86
    [Google Scholar]
  26. Cury KM, Uchida N 2010. Robust odor coding via inhalation-coupled transient activity in the mammalian olfactory bulb. Neuron 68:570–85
    [Google Scholar]
  27. Datta SR, Anderson DJ, Branson K, Perona P, Leifer A 2019. Computational neuroethology: a call to action. Neuron 104:11–24
    [Google Scholar]
  28. Davison IG, Ehlers MD 2011. Neural circuit mechanisms for pattern detection and feature combination in olfactory cortex. Neuron 70:82–94
    [Google Scholar]
  29. DeMaria S, Ngai J 2010. The cell biology of smell. J. Cell Biol. 191:443–52
    [Google Scholar]
  30. Dewan A, Cichy A, Zhang J, Miguel K, Feinstein P et al. 2018. Single olfactory receptors set odor detection thresholds. Nat. Commun. 9:2887
    [Google Scholar]
  31. Dewan A, Pacifico R, Zhan R, Rinberg D, Bozza T 2013. Non-redundant coding of aversive odours in the main olfactory pathway. Nature 497:486–89
    [Google Scholar]
  32. Dey S, Chamero P, Pru JK, Chien MS, Ibarra-Soria X et al. 2015. Cyclic regulation of sensory perception by a female hormone alters behavior. Cell 161:1334–44
    [Google Scholar]
  33. DiCarlo JJ, Zoccolan D, Rust NC 2012. How does the brain solve visual object recognition. ? Neuron 73:415–34
    [Google Scholar]
  34. Diodato A, Ruinart de Brimont M, Yim YS, Derian N, Perrin S et al. 2016. Molecular signatures of neural connectivity in the olfactory cortex. Nat. Commun. 7:12238
    [Google Scholar]
  35. Erskine A, Ackels T, Dasgupta D, Fukunaga I, Schaefer AT 2019. Mammalian olfaction is a high temporal bandwidth sense. bioRxiv 570689. https://doi.org/10.1101/570689
    [Crossref]
  36. Felleman DJ, Van Essen DC 1991. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1:1–47
    [Google Scholar]
  37. Ferrero DM, Lemon JK, Fluegge D, Pashkovski SL, Korzan WJ et al. 2011. Detection and avoidance of a carnivore odor by prey. PNAS 108:11235–40
    [Google Scholar]
  38. Fletcher ML, Chen WR 2010. Neural correlates of olfactory learning: critical role of centrifugal neuromodulation. Learn. Mem. 17:561–70
    [Google Scholar]
  39. Fournier J, Müller CM, Laurent G 2015. Looking for the roots of cortical sensory computation in three-layered cortices. Curr. Opin. Neurobiol. 31:119–26
    [Google Scholar]
  40. Franks KM, Russo MJ, Sosulski DL, Mulligan AA, Siegelbaum SA, Axel R 2011. Recurrent circuitry dynamically shapes the activation of piriform cortex. Neuron 72:49–56
    [Google Scholar]
  41. Friedrich RW 2013. Neuronal computations in the olfactory system of zebrafish. Annu. Rev. Neurosci. 36:383–402
    [Google Scholar]
  42. Fukunaga I, Berning M, Kollo M, Schmaltz A, Schaefer AT 2012. Two distinct channels of olfactory bulb output. Neuron 75:320–29
    [Google Scholar]
  43. Fusi S, Miller EK, Rigotti M 2016. Why neurons mix: high dimensionality for higher cognition. Curr. Opin. Neurobiol. 37:66–74
    [Google Scholar]
  44. Gadziola MA, Tylicki KA, Christian DL, Wesson DW 2015. The olfactory tubercle encodes odor valence in behaving mice. J. Neurosci. 35:4515–27
    [Google Scholar]
  45. Gainetdinov RR, Premont RT, Bohn LM, Lefkowitz RJ, Caron MG 2004. Desensitization of G protein–coupled receptors and neuronal functions. Annu. Rev. Neurosci. 27:107–44
    [Google Scholar]
  46. Ghosh S, Larson SD, Hefzi H, Marnoy Z, Cutforth T et al. 2011. Sensory maps in the olfactory cortex defined by long-range viral tracing of single neurons. Nature 472:217–20
    [Google Scholar]
  47. Giessel AJ, Datta SR 2014. Olfactory maps, circuits and computations. Curr. Opin. Neurobiol. 24:120–32
    [Google Scholar]
  48. Gilbert CD, Li W 2013. Top-down influences on visual processing. Nat. Rev. Neurosci. 14:350–63
    [Google Scholar]
  49. Gire DH, Kapoor V, Arrighi-Allisan A, Seminara A, Murthy VN 2016. Mice develop efficient strategies for foraging and navigation using complex natural stimuli. Curr. Biol. 26:1261–73
    [Google Scholar]
  50. Gire DH, Restrepo D, Sejnowski TJ, Greer C, De Carlos JA, Lopez-Mascaraque L 2013. Temporal processing in the olfactory system: Can we see a smell?. Neuron 78:416–32
    [Google Scholar]
  51. Gomez-Marin A, Ghazanfar AA 2019. The life of behavior. Neuron 104:25–36
    [Google Scholar]
  52. Gottfried JA 2010. Central mechanisms of odour object perception. Nat. Rev. Neurosci. 11:628–41
    [Google Scholar]
  53. Grabska-Barwińska A, Barthelmé S, Beck J, Mainen ZF, Pouget A, Latham PE 2016. A probabilistic approach to demixing odors. Nat. Neurosci. 20:98–106
    [Google Scholar]
  54. Haberly LB 2001. Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. Chem. Senses 26:551–76
    [Google Scholar]
  55. Haddad R, Khan R, Takahashi YK, Mori K, Harel D, Sobel N 2008. A metric for odorant comparison. Nat. Methods 5:425–29
    [Google Scholar]
  56. Haddad R, Lanjuin A, Madisen L, Zeng H, Murthy VN, Uchida N 2013. Olfactory cortical neurons read out a relative time code in the olfactory bulb. Nat. Neurosci. 16:949–57
    [Google Scholar]
  57. Hallem EA, Carlson JR 2006. Coding of odors by a receptor repertoire. Cell 125:143–60
    [Google Scholar]
  58. Handler A, Graham TGW, Cohn R, Morantte I, Siliciano AF et al. 2019. Distinct dopamine receptor pathways underlie the temporal sensitivity of associative learning. Cell 178:60–75.e19
    [Google Scholar]
  59. Hasselmo M, Wilson M, Anderson B, Bower J 1990. Associative memory function in piriform (olfactory) cortex: computational modeling and neuropharmacology Paper presented at the Cold Spring Harbor Symposia on Quantitative Biology Cold Spring Harbor, NY Summer:1990
  60. Hernandez-Nunez L, Belina J, Klein M, Si G, Claus L et al. 2015. Reverse-correlation analysis of navigation dynamics in Drosophila larva using optogenetics. eLife 4:e06225
    [Google Scholar]
  61. Horio N, Murata K, Yoshikawa K, Yoshihara Y, Touhara K 2019. Contribution of individual olfactory receptors to odor-induced attractive or aversive behavior in mice. Nat. Commun. 10:209
    [Google Scholar]
  62. Huang Y, Thathiah A 2015. Regulation of neuronal communication by G protein–coupled receptors. FEBS Lett 589:1607–19
    [Google Scholar]
  63. Illig KR, Haberly LB 2003. Odor-evoked activity is spatially distributed in piriform cortex. J. Comp. Neurol. 457:361–73
    [Google Scholar]
  64. Imamura F, Ayoub AE, Rakic P, Greer CA 2011. Timing of neurogenesis is a determinant of olfactory circuitry. Nat. Neurosci. 14:331–37
    [Google Scholar]
  65. Inokuchi K, Imamura F, Takeuchi H, Kim R, Okuno H et al. 2017. Nrp2 is sufficient to instruct circuit formation of mitral-cells to mediate odour-induced attractive social responses. Nat. Commun. 8:15977
    [Google Scholar]
  66. Iurilli G, Datta SR 2017. Population coding in an innately relevant olfactory area. Neuron 93:1180–97.e7
    [Google Scholar]
  67. Jaeger SR, McRae JF, Bava CM, Beresford MK, Hunter D et al. 2013. A Mendelian trait for olfactory sensitivity affects odor experience and food selection. Curr. Biol. 23:1601–5
    [Google Scholar]
  68. Jazayeri M, Afraz A 2017. Navigating the neural space in search of the neural code. Neuron 93:1003–14
    [Google Scholar]
  69. Jiang Y, Gong NN, Hu XS, Ni MJ, Pasi R, Matsunami H 2015. Molecular profiling of activated olfactory neurons identifies odorant receptors for odors in vivo. Nat. Neurosci. 18:1446–54
    [Google Scholar]
  70. Johnson BA, Leon M 2007. Chemotopic odorant coding in a mammalian olfactory system. J. Comp. Neurol. 503:1–34
    [Google Scholar]
  71. Jordan R, Fukunaga I, Kollo M, Schaefer AT 2018. Active sampling state dynamically enhances olfactory bulb odor representation. Neuron 98:1214–28.e5
    [Google Scholar]
  72. Kar K, Kubilius J, Schmidt K, Issa EB, DiCarlo JJ 2019. Evidence that recurrent circuits are critical to the ventral stream's execution of core object recognition behavior. Nat. Neurosci. 22:974–83
    [Google Scholar]
  73. Katada S, Hirokawa T, Oka Y, Suwa M, Touhara K 2005. Structural basis for a broad but selective ligand spectrum of a mouse olfactory receptor: mapping the odorant-binding site. J. Neurosci. 25:1806–15
    [Google Scholar]
  74. Kato HK, Chu MW, Isaacson JS, Komiyama T 2012. Dynamic sensory representations in the olfactory bulb: modulation by wakefulness and experience. Neuron 76:962–75
    [Google Scholar]
  75. Kell AJE, Yamins DLK, Shook EN, Norman-Haignere SV, McDermott JH 2018. A task-optimized neural network replicates human auditory behavior, predicts brain responses, and reveals a cortical processing hierarchy. Neuron 98:630–44.e16
    [Google Scholar]
  76. Keller A, Gerkin RC, Guan Y, Dhurandhar A, Turu G et al. 2017. Predicting human olfactory perception from chemical features of odor molecules. Science 355:6327820–26
    [Google Scholar]
  77. Keller A, Zhuang H, Chi Q, Vosshall LB, Matsunami H 2007. Genetic variation in a human odorant receptor alters odour perception. Nature 449:468–72
    [Google Scholar]
  78. Keller GB, Mrsic-Flogel TD 2018. Predictive processing: a canonical cortical computation. Neuron 100:424–35
    [Google Scholar]
  79. Khan RM, Luk C-H, Flinker A, Aggarwal A, Lapid H et al. 2007. Predicting odor pleasantness from odorant structure: pleasantness as a reflection of the physical world. J. Neurosci. 27:10015–23
    [Google Scholar]
  80. Kikuta S, Sato K, Kashiwadani H, Tsunoda K, Yamasoba T, Mori K 2010. Neurons in the anterior olfactory nucleus pars externa detect right or left localization of odor sources. PNAS 107:12363–68
    [Google Scholar]
  81. Koldaeva A, Schaefer AT, Fukunaga I 2019. Rapid task-dependent tuning of the mouse olfactory bulb. eLife 8:e43558
    [Google Scholar]
  82. Krakauer JW, Ghazanfar AA, Gomez-Marin A, MacIver MA, Poeppel D 2017. Neuroscience needs behavior: correcting a reductionist bias. Neuron 93:480–90
    [Google Scholar]
  83. Lamme VA, Roelfsema PR 2000. The distinct modes of vision offered by feedforward and recurrent processing. Trends Neurosci 23:571–79
    [Google Scholar]
  84. Large AM, Vogler NW, Canto-Bustos M, Friason FK, Schick P, Oswald A-MM 2018. Differential inhibition of pyramidal cells and inhibitory interneurons along the rostrocaudal axis of anterior piriform cortex. PNAS 115:E8067–76
    [Google Scholar]
  85. Laurent G 2002. Olfactory network dynamics and the coding of multidimensional signals. Nat. Rev. Neurosci. 3:884–95
    [Google Scholar]
  86. Leitner FC, Melzer S, Lütcke H, Pinna R, Seeburg PH et al. 2016. Spatially segregated feedforward and feedback neurons support differential odor processing in the lateral entorhinal cortex. Nat. Neurosci. 19:935–44
    [Google Scholar]
  87. Lepousez G, Valley MT, Lledo P-M 2013. The impact of adult neurogenesis on olfactory bulb circuits and computations. Annu. Rev. Physiol. 75:339–63
    [Google Scholar]
  88. Lerman GM, Gill JV, Rinberg D, Shoham S 2018. Precise optical probing of perceptual detection. bioRxiv 456764. https://doi.org/10.1101/456764
    [Crossref]
  89. Lewicki MS 2002. Efficient coding of natural sounds. Nat. Neurosci. 5:356–63
    [Google Scholar]
  90. Lin D, Shea SD, Katz LC 2006. Representation of natural stimuli in the rodent main olfactory bulb. Neuron 50:937–49
    [Google Scholar]
  91. Linster C, Cleland TA 2016. Neuromodulation of olfactory transformations. Curr. Opin. Neurobiol. 40:170–77
    [Google Scholar]
  92. Linster C, Hasselmo ME 2001. Neuromodulation and the functional dynamics of piriform cortex. Chem. Senses 26:585–94
    [Google Scholar]
  93. Litwin-Kumar A, Harris KD, Axel R, Sompolinsky H, Abbott LF 2017. Optimal degrees of synaptic connectivity. Neuron 93:1153–64.e7
    [Google Scholar]
  94. Lucero MT 2013. Peripheral modulation of smell: fact or fiction?. Semin. Cell Dev. Biol. 24:58–70
    [Google Scholar]
  95. Luskin MB, Price JL 1983. The topographic organization of associational fibers of the olfactory system in the rat, including centrifugal fibers to the olfactory bulb. J. Comp. Neurol. 216:264–91
    [Google Scholar]
  96. Ma L, Qiu Q, Gradwohl S, Scott A, Yu EQ et al. 2012. Distributed representation of chemical features and tunotopic organization of glomeruli in the mouse olfactory bulb. PNAS 109:5481–86
    [Google Scholar]
  97. Mainland JD, Keller A, Li YR, Zhou T, Trimmer C et al. 2014. The missense of smell: functional variability in the human odorant receptor repertoire. Nat. Neurosci. 17:114–20
    [Google Scholar]
  98. Malnic B, Hirono J, Sato T, Buck LB 1999. Combinatorial receptor codes for odors. Cell 96:713–23
    [Google Scholar]
  99. Markopoulos F, Rokni D, Gire DH, Murthy VN 2012. Functional properties of cortical feedback projections to the olfactory bulb. Neuron 76:1175–88
    [Google Scholar]
  100. Mathew D, Martelli C, Kelley-Swift E, Brusalis C, Gershow M et al. 2013. Functional diversity among sensory receptors in a Drosophila olfactory circuit. PNAS 110:E2134–43
    [Google Scholar]
  101. Mathis A, Mamidanna P, Cury KM, Abe T, Murthy VN et al. 2018. DeepLabCut: markerless pose estimation of user-defined body parts with deep learning. Nat. Neurosci. 21:1281–89
    [Google Scholar]
  102. Mathis A, Rokni D, Kapoor V, Bethge M, Murthy VN 2016. Reading out olfactory receptors: Feedforward circuits detect odors in mixtures without demixing. Neuron 91:1110–23
    [Google Scholar]
  103. Mendonça AG, Drugowitsch J, Inês Vicente M, DeWitt E, Pouget A, Mainen ZF 2018. The impact of learning on perceptual decisions and its implication for speed-accuracy tradeoffs. bioRxiv 501858. https://doi.org/10.1101/501858
    [Crossref]
  104. Millhouse O, Heimer L 1984. Cell configurations in the olfactory tubercle of the rat. J. Comp. Neurol. 228:571–97
    [Google Scholar]
  105. Millman DJ, Murthy VN 2020. Rapid learning of odor–value association in the olfactory striatum. J. Neurosci 22:JN-RM-2604-19
    [Google Scholar]
  106. Miura K, Mainen ZF, Uchida N 2012. Odor representations in olfactory cortex: distributed rate coding and decorrelated population activity. Neuron 74:1087–98
    [Google Scholar]
  107. Miyamichi K, Amat F, Moussavi F, Wang C, Wickersham I et al. 2011. Cortical representations of olfactory input by trans-synaptic tracing. Nature 472:191–96
    [Google Scholar]
  108. Monahan K, Lomvardas S 2015. Monoallelic expression of olfactory receptors. Annu. Rev. Cell Dev. Biol. 31:721–40
    [Google Scholar]
  109. Mori K, Sakano H 2011. How is the olfactory map formed and interpreted in the mammalian brain?. Annu. Rev. Neurosci. 34:467–99
    [Google Scholar]
  110. Mori K, Takahashi YK, Igarashi KM, Yamaguchi M 2006. Maps of odorant molecular features in the mammalian olfactory bulb. Physiol. Rev. 86:409–33
    [Google Scholar]
  111. Murata K, Kanno M, Ieki N, Mori K, Yamaguchi M 2015. Mapping of learned odor-induced motivated behaviors in the mouse olfactory tubercle. J. Neurosci. 35:10581–99
    [Google Scholar]
  112. Murthy VN 2011. Olfactory maps in the brain. Annu. Rev. Neurosci. 34:233–58
    [Google Scholar]
  113. Nagayama S, Homma R, Imamura F 2014. Neuronal organization of olfactory bulb circuits. Front. Neural Circuits 8:98
    [Google Scholar]
  114. Nagel KI, Wilson RI 2011. Biophysical mechanisms underlying olfactory receptor neuron dynamics. Nat. Neurosci. 14:208–16
    [Google Scholar]
  115. Nakashima A, Ihara N, Shigeta M, Kiyonari H, Ikegaya Y, Takeuchi H 2019. Structured spike series specify gene expression patterns for olfactory circuit formation. Science 365:eaaw5030
    [Google Scholar]
  116. Nara K, Saraiva LR, Ye X, Buck LB 2011. A large-scale analysis of odor coding in the olfactory epithelium. J. Neurosci. 31:9179–91
    [Google Scholar]
  117. Neville K, Haberly L. 2004. Olfactory cortex. The Synaptic Organization of the Brain G Shepherd 415–54 New York: Oxford Univ. Press
    [Google Scholar]
  118. Oka Y, Katada S, Omura M, Suwa M, Yoshihara Y, Touhara K 2006. Odorant receptor map in the mouse olfactory bulb: in vivo sensitivity and specificity of receptor-defined glomeruli. Neuron 52:857–69
    [Google Scholar]
  119. Oka Y, Nakamura A, Watanabe H, Touhara K 2004. An odorant derivative as an antagonist for an olfactory receptor. Chem. Senses 29:815–22
    [Google Scholar]
  120. Otazu GH, Chae H, Davis MB, Albeanu DF 2015. Cortical feedback decorrelates olfactory bulb output in awake mice. Neuron 86:1461–77
    [Google Scholar]
  121. Pacifico R, Dewan A, Cawley D, Guo C, Bozza T 2012. An olfactory subsystem that mediates high-sensitivity detection of volatile amines. Cell Rep 2:76–88
    [Google Scholar]
  122. Panzeri S, Harvey CD, Piasini E, Latham PE, Fellin T 2017. Cracking the neural code for sensory perception by combining statistics, intervention, and behavior. Neuron 93:491–507
    [Google Scholar]
  123. Payton CA, Wilson DA, Wesson DW 2012. Parallel odor processing by two anatomically distinct olfactory bulb target structures. PLOS ONE 7:e34926
    [Google Scholar]
  124. Peron S, Pancholi R, Voelcker B, Wittenbach JD, Ólafsdóttir HF et al. 2020. Recurrent interactions in local cortical circuits. Nature 579:256–59
    [Google Scholar]
  125. Pfister P, Smith BC, Evans BJ, Brann JH, Trimmer C et al. 2019. Odorant receptor inhibition is fundamental to odor encoding. bioRxiv 760033. https://doi.org/10.1101/760033
    [Crossref]
  126. Poivet E, Peterlin Z, Tahirova N, Xu L, Altomare C et al. 2016. Applying medicinal chemistry strategies to understand odorant discrimination. Nat. Commun. 7:11157
    [Google Scholar]
  127. Poo C, Isaacson JS 2011. A major role for intracortical circuits in the strength and tuning of odor-evoked excitation in olfactory cortex. Neuron 72:41–48
    [Google Scholar]
  128. Qu LP, Kahnt T, Cole SM, Gottfried JA 2016. De novo emergence of odor category representations in the human brain. J. Neurosci. 36:468–78
    [Google Scholar]
  129. Rabell JE, Mutlu K, Noutel J, Del Olmo PM, Haesler S 2017. Spontaneous rapid odor source localization behavior requires interhemispheric communication. Curr. Biol. 27:1542–48.e4
    [Google Scholar]
  130. Reddy G, Zak JD, Vergassola M, Murthy VN 2018. Antagonism in olfactory receptor neurons and its implications for the perception of odor mixtures. eLife 7:e34958
    [Google Scholar]
  131. Rennaker RL, Chen C-FF, Ruyle AM, Sloan AM, Wilson DA 2007. Spatial and temporal distribution of odorant-evoked activity in the piriform cortex. J. Neurosci. 27:1534–42
    [Google Scholar]
  132. Resulaj A, Rinberg D. 2015. Novel behavioral paradigm reveals lower temporal limits on mouse olfactory decisions. J. Neurosci. 35:11667–73
    [Google Scholar]
  133. Rinberg D, Koulakov A, Gelperin A 2006. Speed-accuracy tradeoff in olfaction. Neuron 51:351–58
    [Google Scholar]
  134. Roland B, Deneux T, Franks KM, Bathellier B, Fleischmann A 2017. Odor identity coding by distributed ensembles of neurons in the mouse olfactory cortex. eLife 6:e26337
    [Google Scholar]
  135. Root CM, Denny CA, Hen R, Axel R 2014. The participation of cortical amygdala in innate, odour-driven behaviour. Nature 515:269–73
    [Google Scholar]
  136. Rospars JP, Lansky P, Chaput M, Duchamp-Viret P 2008. Competitive and noncompetitive odorant interactions in the early neural coding of odorant mixtures. J. Neurosci. 28:2659–66
    [Google Scholar]
  137. Russell LE, Yang Z, Tan PL, Fişek M, Packer AM et al. 2019. The influence of visual cortex on perception is modulated by behavioural state. bioRxiv 706010. https://doi.org/10.1101/706010
    [Crossref]
  138. Saito H, Chi Q, Zhuang H, Matsunami H, Mainland JD 2009. Odor coding by a mammalian receptor repertoire. Sci. Signal. 2:ra9
    [Google Scholar]
  139. Santoro SW, Dulac C 2012. The activity-dependent histone variant H2BE modulates the life span of olfactory neurons. eLife 1:e00070
    [Google Scholar]
  140. Schaffer ES, Stettler DD, Kato D, Choi GB, Axel R, Abbott LF 2018. Odor perception on the two sides of the brain: consistency despite randomness. Neuron 98:736–42.e3
    [Google Scholar]
  141. Schoppa NE, Urban NN 2003. Dendritic processing within olfactory bulb circuits. Trends Neurosci 26:501–6
    [Google Scholar]
  142. Semedo JD, Zandvakili A, Machens CK, Yu BM, Kohn A 2019. Cortical areas interact through a communication subspace. Neuron 102:249–59.e4
    [Google Scholar]
  143. Shirasu M, Yoshikawa K, Takai Y, Nakashima A, Takeuchi H et al. 2014. Olfactory receptor and neural pathway responsible for highly selective sensing of musk odors. Neuron 81:165–78
    [Google Scholar]
  144. Simoncelli EP, Olshausen BA 2001. Natural image statistics and neural representation. Annu. Rev. Neurosci. 24:1193–216
    [Google Scholar]
  145. Smear M, Resulaj A, Zhang J, Bozza T, Rinberg D 2013. Multiple perceptible signals from a single olfactory glomerulus. Nat. Neurosci. 16:1687–91
    [Google Scholar]
  146. Snitz K, Yablonka A, Weiss T, Frumin I, Khan RM, Sobel N 2013. Predicting odor perceptual similarity from odor structure. PLOS Comput. Biol. 9:e1003184
    [Google Scholar]
  147. Sosulski DL, Bloom ML, Cutforth T, Axel R, Datta SR 2011. Distinct representations of olfactory information in different cortical centres. Nature 472:213–16
    [Google Scholar]
  148. Soucy ER, Albeanu DF, Fantana AL, Murthy VN, Meister M 2009. Precision and diversity in an odor map on the olfactory bulb. Nat. Neurosci. 12:210–20
    [Google Scholar]
  149. Stern M, Bolding KA, Abbott LF, Franks KM 2018. A transformation from temporal to ensemble coding in a model of piriform cortex. eLife 7:e34831
    [Google Scholar]
  150. Stettler DD, Axel R. 2009. Representations of odor in the piriform cortex. Neuron 63:854–64
    [Google Scholar]
  151. Stringer C, Pachitariu M, Steinmetz N, Carandini M, Harris KD 2019. High-dimensional geometry of population responses in visual cortex. Nature 571:361–65
    [Google Scholar]
  152. Su C-Y, Menuz K, Carlson JR 2009. Olfactory perception: receptors, cells, and circuits. Cell 139:45–59
    [Google Scholar]
  153. Suzuki N, Bekkers JM 2012. Microcircuits mediating feedforward and feedback synaptic inhibition in the piriform cortex. J. Neurosci. 32:919–31
    [Google Scholar]
  154. Takeuchi H, Ishida H, Hikichi S, Kurahashi T 2009. Mechanism of olfactory masking in the sensory cilia. J. Gen. Physiol. 133:583–601
    [Google Scholar]
  155. Takeuchi H, Sakano H 2014. Neural map formation in the mouse olfactory system. Cell. Mol. Life Sci. 71:3049–57
    [Google Scholar]
  156. Uchida N, Mainen ZF 2003. Speed and accuracy of olfactory discrimination in the rat. Nat. Neurosci. 6:1224–29
    [Google Scholar]
  157. Uchida N, Poo C, Haddad R 2014. Coding and transformations in the olfactory system. Annu. Rev. Neurosci. 37:363–85
    [Google Scholar]
  158. Urs NM, Nicholls PJ, Caron MG 2014. Integrated approaches to understanding antipsychotic drug action at GPCRs. Curr. Opin. Cell Biol. 27:56–62
    [Google Scholar]
  159. Vickers NJ 2000. Mechanisms of animal navigation in odor plumes. Biol. Bull. 198:203–12
    [Google Scholar]
  160. Vincis R, Gschwend O, Bhaukaurally K, Beroud J, Carleton A 2012. Dense representation of natural odorants in the mouse olfactory bulb. Nat. Neurosci. 15:537–39
    [Google Scholar]
  161. von der Weid B, Rossier D, Lindup M, Tuberosa J, Widmer A et al. 2015. Large-scale transcriptional profiling of chemosensory neurons identifies receptor-ligand pairs in vivo. Nat. Neurosci. 18:1455–63
    [Google Scholar]
  162. Wachowiak M 2011. All in a sniff: olfaction as a model for active sensing. Neuron 71:962–73
    [Google Scholar]
  163. Wachowiak M, Shipley MT 2006. Coding and synaptic processing of sensory information in the glomerular layer of the olfactory bulb. Semin. Cell Dev. Biol. 17:411–23
    [Google Scholar]
  164. Wang PY, Boboila C, Shamash P, Wu Z, Stein NP et al. 2019. The imposition of value on odor: transient and persistent representations of odor value in prefrontal cortex. bioRxiv 753426. https://doi.org/10.1101/753426
    [Crossref]
  165. Weiss T, Snitz K, Yablonka A, Khan RM, Gafsou D et al. 2012. Perceptual convergence of multi-component mixtures in olfaction implies an olfactory white. PNAS 109:19959–64
    [Google Scholar]
  166. Wesson DW, Carey RM, Verhagen JV, Wachowiak M 2008. Rapid encoding and perception of novel odors in the rat. PLOS Biol 6:e82
    [Google Scholar]
  167. Wesson DW, Wilson DA 2010. Smelling sounds: olfactory–auditory sensory convergence in the olfactory tubercle. J. Neurosci. 30:3013–21
    [Google Scholar]
  168. Wesson DW, Wilson DA 2011. Sniffing out the contributions of the olfactory tubercle to the sense of smell: hedonics, sensory integration, and more. ? Neurosci. Biobehav. Rev. 35:655–68
    [Google Scholar]
  169. Wilson CD, Serrano GO, Koulakov AA, Rinberg D 2017. A primacy code for odor identity. Nat. Commun. 8:1477
    [Google Scholar]
  170. Wilson DA, Sullivan RM 2011. Cortical processing of odor objects. Neuron 72:506–19
    [Google Scholar]
  171. Wilson RI 2013. Early olfactory processing in Drosophila: mechanisms and principles. Annu. Rev. Neurosci. 36:217–41
    [Google Scholar]
  172. Wilson RI, Mainen ZF 2006. Early events in olfactory processing. Annu. Rev. Neurosci. 29:163–201
    [Google Scholar]
  173. Wiltschko AB, Johnson MJ, Iurilli G, Peterson RE, Katon JM et al. 2015. Mapping sub-second structure in mouse behavior. Neuron 88:1121–35
    [Google Scholar]
  174. Wojcik PT, Sirotin YB 2014. Single scale for odor intensity in rat olfaction. Curr. Biol. 24:568–73
    [Google Scholar]
  175. Xu L, Li W, Voleti V, Zou D-J, Hillman EMC, Firestein S 2020. Widespread receptor-driven modulation in peripheral olfactory coding. Science 368:eaaz5390
    [Google Scholar]
  176. Xu PS, Lee D, Holy TE 2016. Experience-dependent plasticity drives individual differences in pheromone-sensing neurons. Neuron 91:878–92
    [Google Scholar]
  177. Yamada Y, Bhaukaurally K, Madarász TJ, Pouget A, Rodriguez I, Carleton A 2017. Context-and output layer-dependent long-term ensemble plasticity in a sensory circuit. Neuron 93:1198–212.e5
    [Google Scholar]
  178. Yamins DLK, Hong H, Cadieu CF, Solomon EA, Seibert D, DiCarlo JJ 2014. Performance-optimized hierarchical models predict neural responses in higher visual cortex. PNAS 111:8619–24
    [Google Scholar]
  179. Yeshurun Y, Sobel N 2009. An odor is not worth a thousand words: from multidimensional odors to unidimensional odor objects. Annu. Rev. Psychol. 61:219–41
    [Google Scholar]
  180. Yu Y, de March CA, Ni MJ, Adipietro KA, Golebiowski J et al. 2015. Responsiveness of G protein–coupled odorant receptors is partially attributed to the activation mechanism. PNAS 112:14966–71
    [Google Scholar]
  181. Zariwala HA, Kepecs A, Uchida N, Hirokawa J, Mainen ZF 2013. The limits of deliberation in a perceptual decision task. Neuron 78:339–51
    [Google Scholar]
  182. Zelano C, Mohanty A, Gottfried JA 2011. Olfactory predictive codes and stimulus templates in piriform cortex. Neuron 72:178–87
    [Google Scholar]
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