1932

Abstract

All an animal can do to infer the state of its environment is to observe the sensory-evoked activity of its own neurons. These inferences about the presence, quality, or similarity of objects are probabilistic and inform behavioral decisions that are often made in close to real time. Neural systems employ several strategies to facilitate sensory discrimination: Biophysical mechanisms separate the neuronal response distributions in coding space, compress their variances, and combine information from sequential observations. We review how these strategies are implemented in the olfactory system of the fruit fly. The emerging principles of odor discrimination likely apply to other neural circuits of similar architecture.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-052118-115655
2019-05-06
2024-06-24
Loading full text...

Full text loading...

/deliver/fulltext/biophys/48/1/annurev-biophys-052118-115655.html?itemId=/content/journals/10.1146/annurev-biophys-052118-115655&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Albus JS 1971. A theory of cerebellar function. Math. Biosci. 10:25–61
    [Google Scholar]
  2. 2.
    Aso Y, Hattori D, Yu Y, Johnston RM, Iyer NA et al. 2014. The neuronal architecture of the mushroom body provides a logic for associative learning. eLife 3:e04577
    [Google Scholar]
  3. 3.
    Aso Y, Sitaraman D, Ichinose T, Kaun KR, Vogt K et al. 2014. Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila. . eLife 4:e04580
    [Google Scholar]
  4. 4.
    Barlow HB 1961. Possible principles underlying the transformation of sensory messages. Sensory Communication WA Rosenblith 217–34 Cambridge, MA: MIT Press
    [Google Scholar]
  5. 5.
    Barnstedt O, Owald D, Felsenberg J, Brain R, Moszynski J-P et al. 2016. Memory-relevant mushroom body output synapses are cholinergic. Neuron 89:1237–47
    [Google Scholar]
  6. 6.
    Benton R, Vannice KS, Gomez-Diaz C, Vosshall LB 2009. Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. . Cell 136:149–62
    [Google Scholar]
  7. 7.
    Bhandawat V, Olsen SR, Gouwens NW, Schlief ML, Wilson RI 2007. Sensory processing in the Drosophila antennal lobe increases reliability and separability of ensemble odor representations. Nat. Neurosci. 10:1474–82
    [Google Scholar]
  8. 8.
    Bialek W 2012. Biophysics: Searching for Principles Princeton, NJ: Princeton Univ. Press
    [Google Scholar]
  9. 9.
    Bialek W, Rieke F, de Ruyter van Steveninck RR, Warland D 1991. Reading a neural code. Science 252:1854–57
    [Google Scholar]
  10. 10.
    Bogacz R, Brown E, Moehlis J, Holmes P, Cohen JD 2006. The physics of optimal decision making: a formal analysis of models of performance in two-alternative forced-choice tasks. Psychol. Rev. 113:700–65
    [Google Scholar]
  11. 11.
    Bolding KA, Franks KM 2017. Complementary codes for odor identity and intensity in olfactory cortex. eLife 6:e22630
    [Google Scholar]
  12. 12.
    Borst A 1983. Computation of olfactory signals in Drosophila melanogaster. J. Comp. Physiol. A 152:373–83
    [Google Scholar]
  13. 13.
    Britten KH, Shadlen MN, Newsome WT, Movshon JA 1992. The analysis of visual motion: a comparison of neuronal and psychophysical performance. J. Neurosci. 12:4745–65
    [Google Scholar]
  14. 14.
    Brunet LJ, Gold GH, Ngai J 1996. General anosmia caused by a targeted disruption of the mouse olfactory cyclic nucleotide-gated cation channel. Neuron 17:681–93
    [Google Scholar]
  15. 15.
    Brunton BW, Botvinick MM, Brody CD 2013. Rats and humans can optimally accumulate evidence for decision-making. Science 340:95–98
    [Google Scholar]
  16. 16.
    Burke CJ, Huetteroth W, Owald D, Perisse E, Krashes MJ et al. 2012. Layered reward signalling through octopamine and dopamine in Drosophila. . Nature 492:433–37
    [Google Scholar]
  17. 17.
    Butterwick JA, del Mármol 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]
  18. 18.
    Cai X, Liang CW, Muralidharan S, Kao JPY, Tang C-M et al. 2004. Unique roles of SK and Kv4.2 potassium channels in dendritic integration. Neuron 44:351–64
    [Google Scholar]
  19. 19.
    Campbell RAA, Honegger KS, Qin H, Li W, Demir E, Turner GC 2013. Imaging a population code for odor identity in the Drosophila mushroom body. J. Neurosci. 33:10568–81
    [Google Scholar]
  20. 20.
    Candès EJ, Wakin MB 2008. An introduction to compressive sampling: a sensing/sampling paradigm that goes against the common knowledge in data acquisition. IEEE Signal Process. Mag. 25:21–30
    [Google Scholar]
  21. 21.
    Cao L-H, Yang D, Wu W, Zeng X, Jing B-Y et al. 2017. Odor-evoked inhibition of olfactory sensory neurons drives olfactory perception in Drosophila. Nat. . Commun 8:1357
    [Google Scholar]
  22. 22.
    Caron SJC, Ruta V, Abbott LF, Axel R 2013. Random convergence of olfactory inputs in the Drosophila mushroom body. Nature 497:113–17
    [Google Scholar]
  23. 23.
    Cayco-Gajic NA, Clopath C, Silver RA 2017. Sparse synaptic connectivity is required for decorrelation and pattern separation in feedforward networks. Nat. Commun. 8:1116
    [Google Scholar]
  24. 24.
    Chou Y-H, Spletter ML, Yaksi E, Leong JCS, Wilson RI, Luo L 2010. Diversity and wiring variability of olfactory local interneurons in the Drosophila antennal lobe. Nat. Neurosci. 13:439–49
    [Google Scholar]
  25. 25.
    Claridge-Chang A, Roorda RD, Vrontou E, Sjulson L, Li H et al. 2009. Writing memories with light-addressable reinforcement circuitry. Cell 139:405–15
    [Google Scholar]
  26. 26.
    Clyne PJ, Warr CG, Freeman MR, Lessing D, Kim J, Carlson JR 1999. A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. . Neuron 22:327–38
    [Google Scholar]
  27. 27.
    Couto A, Alenius M, Dickson BJ 2005. Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr. Biol. 15:1535–47
    [Google Scholar]
  28. 28.
    Cover TM, Thomas JA 1991. Elements of Information Theory New York: Wiley
    [Google Scholar]
  29. 29.
    DasGupta S, Ferreira CH, Miesenböck G 2014. FoxP influences the speed and accuracy of a perceptual decision in Drosophila. . Science 344:901–4
    [Google Scholar]
  30. 30.
    DasGupta S, Waddell S 2008. Learned odor discrimination in Drosophila without combinatorial odor maps in the antennal lobe. Curr. Biol. 18:1668–74
    [Google Scholar]
  31. 31.
    de Bruyne M, Clyne PJ, Carlson JR 1999. Odor coding in a model olfactory organ: the Drosophila maxillary palp. J. Neurosci. 19:4520–32
    [Google Scholar]
  32. 32.
    de Bruyne M, Foster K, Carlson JR 2001. Odor coding in the Drosophila antenna. Neuron 30:537–52
    [Google Scholar]
  33. 33.
    Dobritsa AA, van der Goes van Naters W, Warr CG, Steinbrecht RA, Carlson JR 2003. Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron 37:827–41
    [Google Scholar]
  34. 34.
    Dolan M-J, Belliart-Guérin G, Bates AS, Frechter S, Lampin-Saint-Amaux A et al. 2018. Communication from learned to innate olfactory processing centers is required for memory retrieval in Drosophila. . Neuron 100:651–68
    [Google Scholar]
  35. 35.
    Dudai Y 1977. Properties of learning and memory in Drosophila melanogaster. J. Comp. Physiol. A 114:69–89
    [Google Scholar]
  36. 36.
    Evans DA, Stempel AV, Vale R, Ruehle S, Lefler Y, Branco T 2018. A synaptic threshold mechanism for computing escape decisions. Nature 558:590–94
    [Google Scholar]
  37. 37.
    Fairhall AL, Lewen GD, Bialek W, de Ruyter van Steveninck RR 2001. Efficiency and ambiguity in an adaptive neural code. Nature 412:787–92
    [Google Scholar]
  38. 38.
    Farris SM 2011. Are mushroom bodies cerebellum-like structures. ? Arthropod Struct. Dev. 40:368–79
    [Google Scholar]
  39. 39.
    Fişek M, Wilson RI 2014. Stereotyped connectivity and computations in higher-order olfactory neurons. Nat. Neurosci. 17:280–88
    [Google Scholar]
  40. 40.
    Fishilevich E, Vosshall LB 2005. Genetic and functional subdivision of the Drosophila antennal lobe. Curr. Biol. 15:1548–53
    [Google Scholar]
  41. 41.
    Frechter S, Bates AS, Tootoonian S, Dolan M-J, Manton JD et al. 2018. Functional and anatomical specificity in a higher olfactory centre. bioRxiv 336982 . https://doi.org/10.1101/336982
    [Crossref]
  42. 42.
    Friedrich RW, Laurent G 2001. Dynamic optimization of odor representations by slow temporal patterning of mitral cell activity. Science 291:889–94
    [Google Scholar]
  43. 43.
    Gammaitoni L, Hänggi P, Jung P, Marchesoni F 1998. Stochastic resonance. Rev. Mod. Phys. 70:223–87
    [Google Scholar]
  44. 44.
    Gao Q, Chess A 1999. Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. Genomics 60:31–39
    [Google Scholar]
  45. 45.
    Gao Q, Yuan B, Chess A 2000. Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe. Nat. Neurosci. 3:780–85
    [Google Scholar]
  46. 46.
    Gold JI, Shadlen MN 2001. Neural computations that underlie decisions about sensory stimuli. Trends Cogn. Sci. 5:10–16
    [Google Scholar]
  47. 47.
    Gold JI, Shadlen MN 2007. The neural basis of decision making. Annu. Rev. Neurosci. 30:535–74
    [Google Scholar]
  48. 48.
    Good IJ 1985. Weight of evidence: a brief survey. Bayesian Statistics 2 JM Bernardo, MH DeGroot, DV Lindley, AFM Smith 249–69 Amsterdam: Elsevier Sci.
    [Google Scholar]
  49. 49.
    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
    [Google Scholar]
  50. 50.
    Green DM, Swets JA 1966. Signal Detection Theory and Psychophysics New York: Wiley
    [Google Scholar]
  51. 51.
    Groschner LN, Chan Wah Hak L, Bogacz R, DasGupta S, Miesenböck G 2018. Dendritic integration of sensory evidence in perceptual decision-making. Cell 173:894–905.e13
    [Google Scholar]
  52. 52.
    Gruntman E, Turner GC 2013. Integration of the olfactory code across dendritic claws of single mushroom body neurons. Nat. Neurosci. 16:1821–29
    [Google Scholar]
  53. 53.
    Guo H, Kunwar K, Smith D 2017. Odorant receptor sensitivity modulation in Drosophila. J. Neurosci 37:9465–73
    [Google Scholar]
  54. 54.
    Hallem EA, Carlson JR 2006. Coding of odors by a receptor repertoire. Cell 125:143–60
    [Google Scholar]
  55. 55.
    Hallem EA, Ho MG, Carlson JR 2004. The molecular basis of odor coding in the Drosophila antenna. Cell 117:965–79
    [Google Scholar]
  56. 56.
    Hamming RW 1980. Coding and Information Theory Englewood Cliffs, NJ: Prentice-Hall
    [Google Scholar]
  57. 57.
    Hanes DP, Schall JD 1996. Neural control of voluntary movement initiation. Science 274:427–30
    [Google Scholar]
  58. 58.
    Harvey CD, Coen P, Tank DW 2012. Choice-specific sequences in parietal cortex during a virtual-navigation decision task. Nature 484:62–68
    [Google Scholar]
  59. 59.
    Heisenberg M, Borst A, Wagner S, Byers D 1985. Drosophila mushroom body mutants are deficient in olfactory learning. J. Neurogenet. 2:1–30
    [Google Scholar]
  60. 60.
    Hige T, Aso Y, Modi MN, Rubin GM, Turner GC 2015. Heterosynaptic plasticity underlies aversive olfactory learning in Drosophila. . Neuron 88:985–98
    [Google Scholar]
  61. 61.
    Hoffman DA, Magee JC, Colbert CM, Johnston D 1997. K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387:869–75
    [Google Scholar]
  62. 62.
    Honegger KS, Campbell RAA, Turner GC 2011. Cellular-resolution population imaging reveals robust sparse coding in the Drosophila mushroom body. J. Neurosci. 31:11772–85
    [Google Scholar]
  63. 63.
    Huang J, Zhang W, Qiao W, Hu A, Wang Z 2010. Functional connectivity and selective odor responses of excitatory local interneurons in Drosophila antennal lobe. Neuron 67:1021–33
    [Google Scholar]
  64. 64.
    Inada K, Tsuchimoto Y, Kazama H 2017. Origins of cell-type-specific olfactory processing in the Drosophila mushroom body circuit. Neuron 95:357–67.e4
    [Google Scholar]
  65. 65.
    Ito I, Ong RC-Y, Raman B, Stopfer M 2008. Sparse odor representation and olfactory learning. Nat. Neurosci. 11:1177–84
    [Google Scholar]
  66. 66.
    Ito K, Suzuki K, Estes P, Ramaswami M, Yamamoto D, Stausfeld NJ 1998. The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in the Drosophila melanogaster Meigen. Learn. Mem. 5:52–77
    [Google Scholar]
  67. 67.
    Jeanne JM, Fişek M, Wilson RI 2018. The organization of projections from olfactory glomeruli onto higher-order neurons. Neuron 98:1198–213.e6
    [Google Scholar]
  68. 68.
    Jeanne JM, Wilson RI 2015. Convergence, divergence, and reconvergence in a feedforward network improves neural speed and accuracy. Neuron 88:1014–26
    [Google Scholar]
  69. 69.
    Jefferis GS, Potter CJ, Chan AM, Marin EC, Rohlfing T et al. 2007. Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation. Cell 128:1187–203
    [Google Scholar]
  70. 70.
    Jefferis GSXE, Marin E, Stocker RF, Luo L 2001. Target neuron prespecification in the olfactory map of Drosophila. . Nature 414:204–8
    [Google Scholar]
  71. 71.
    Joseph J, Dunn FA, Stopfer M 2012. Spontaneous olfactory receptor neuron activity determines follower cell response properties. J. Neurosci. 32:2900–10
    [Google Scholar]
  72. 72.
    Kahneman D 2011. Thinking, Fast and Slow New York: Farrar, Strous and Giroux
    [Google Scholar]
  73. 73.
    Kanerva P 1988. Sparse Distributed Memory Cambridge, MA: MIT Press
    [Google Scholar]
  74. 74.
    Kazama H, Wilson RI 2008. Homeostatic matching and nonlinear amplification at identified central synapses. Neuron 58:401–13
    [Google Scholar]
  75. 75.
    Kazama H, Wilson RI 2009. Origins of correlated activity in an olfactory circuit. Nat. Neurosci. 12:1136–44
    [Google Scholar]
  76. 76.
    Kim AJ, Lazar AA, Slutskiy YB 2011. System identification of Drosophila olfactory sensory neurons. J. Comput. Neurosci. 30:143–61
    [Google Scholar]
  77. 77.
    Kim AJ, Lazar AA, Slutskiy YB 2015. Projection neurons in Drosophila antennal lobes signal the acceleration of odor concentrations. eLife 4:e06651
    [Google Scholar]
  78. 78.
    Kohl J, Ostrovsky AD, Frechter S, Jefferis GSXE 2013. A bidirectional circuit switch reroutes pheromone signals in male and female brains. Cell 155:1610–23
    [Google Scholar]
  79. 79.
    Krashes MJ, Keene AC, Leung B, Armstrong JD, Waddell S 2007. Sequential use of mushroom body neuron subsets during Drosophila odor memory processing. Neuron 53:103–15
    [Google Scholar]
  80. 80.
    Kreher SA, Mathew D, Kim J, Carlson JR 2008. Translation of sensory input into behavioral output via an olfactory system. Neuron 59:110–24
    [Google Scholar]
  81. 81.
    Kullback S 1959. Information Theory and Statistics New York: Wiley
    [Google Scholar]
  82. 82.
    Kurtovic A, Widmer A, Dickson BJ 2007. A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature 446:542–46
    [Google Scholar]
  83. 83.
    Larsson MC, Domingos AI, Jones WD, Chiappe ME, Amrein H, Vosshall LB 2004. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43:703–14
    [Google Scholar]
  84. 84.
    Latimer KW, Yates JL, Meister MLR, Huk AC, Pillow JW 2015. Single-trial spike trains in parietal cortex reveal discrete steps during decision-making. Science 349:184–87
    [Google Scholar]
  85. 85.
    Leiss F, Groh C, Butcher NJ, Meinertzhagen IA, Tavosanis G 2009. Synaptic organization in the adult Drosophila mushroom body calyx. J. Comp. Neurol. 517:808–24
    [Google Scholar]
  86. 86.
    Lima SQ, Miesenböck G 2005. Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121:141–52
    [Google Scholar]
  87. 87.
    Lin AC, Bygrave AM, de Calignon A, Lee T, Miesenböck G 2014. Sparse, decorrelated odor coding in the mushroom body enhances learned odor discrimination. Nat. Neurosci. 17:559–68
    [Google Scholar]
  88. 88.
    Litwin-Kumar A, Harris KD, Axel R, Sompolinsky H, Abbott LF 2017. Optimal degrees of synaptic connectivity. Neuron 93:1153–57
    [Google Scholar]
  89. 89.
    Liu C, Plaçais P-Y, Yamagata N, Pfeiffer BD, Aso Y et al. 2012. A subset of dopamine neurons signals reward for odour memory in Drosophila. . Nature 488:512–16
    [Google Scholar]
  90. 90.
    Luo SX, Axel R, Abbott LF 2010. Generating sparse and selective third-order responses in the olfactory system of the fly. PNAS 107:10713–18
    [Google Scholar]
  91. 91.
    Mao Z, Davis RL 2009. Eight different types of dopaminergic neurons innervate the Drosophila mushroom body neuropil: anatomical and physiological heterogeneity. Front. Neural Circuits 3:5
    [Google Scholar]
  92. 92.
    Marin EC, Jefferis GSXE, Komiyama T, Zhu H, Luo L 2002. Representation of the glomerular olfactory map in the Drosophila brain. Cell 109:243–55
    [Google Scholar]
  93. 93.
    Marr D 1969. A theory of cerebellar cortex. J. Physiol. 202:437–70
    [Google Scholar]
  94. 94.
    Masek P, Heisenberg M 2008. Distinct memories of odor intensity and quality in Drosophila. . PNAS 105:15985–90
    [Google Scholar]
  95. 95.
    Mazor O, Laurent G 2005. Transient dynamics versus fixed points in odor representations by locust antennal lobe projection neurons. Neuron 48:661–73
    [Google Scholar]
  96. 96.
    Miesenböck G 2009. The optogenetic catechism. Science 326:395–99
    [Google Scholar]
  97. 97.
    Mountcastle VB, Steinmetz MA, Romo R 1990. Frequency discrimination in the sense of flutter: psychophysical measurements correlated with postcentral events in behaving monkeys. J. Neurosci. 10:3032–44
    [Google Scholar]
  98. 98.
    Murthy M, Fiete I, Laurent G 2008. Testing odor response stereotypy in the Drosophila mushroom body. Neuron 59:1009–23
    [Google Scholar]
  99. 99.
    Nagel KI, Hong EJ, Wilson RI 2015. Synaptic and circuit mechanisms promoting broadband transmission of olfactory stimulus dynamics. Nat. Neurosci. 18:56–65
    [Google Scholar]
  100. 100.
    Nagel KI, Wilson RI 2011. Biophysical mechanisms underlying olfactory receptor neuron dynamics. Nat. Neurosci. 14:208–16
    [Google Scholar]
  101. 101.
    Newsome WT, Britten KH, Movshon JA 1989. Neuronal correlates of a perceptual decision. Nature 341:52–54
    [Google Scholar]
  102. 102.
    Ng M, Roorda RD, Lima SQ, Zemelman BV, Morcillo P, Miesenböck G 2002. Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron 36:463–74
    [Google Scholar]
  103. 103.
    Okada R, Awasaki T, Ito K 2009. Gamma-aminobutyric acid (GABA)-mediated neural connections in the Drosophila antennal lobe. J. Comp. Neurol. 514:74–91
    [Google Scholar]
  104. 104.
    Okada R, Rybak J, Manz G, Menzel R 2007. Learning-related plasticity in PE1 and other mushroom body-extrinsic neurons in the honeybee brain. J. Neurosci. 27:11736–47
    [Google Scholar]
  105. 105.
    Olsen SR, Bhandawat V, Wilson RI 2007. Excitatory interactions between olfactory processing channels in the Drosophila antennal lobe. Neuron 54:89–103
    [Google Scholar]
  106. 106.
    Olsen SR, Bhandawat V, Wilson RI 2010. Divisive normalization in olfactory population codes. Neuron 66:287–99
    [Google Scholar]
  107. 107.
    Olsen SR, Wilson RI 2008. Lateral presynaptic inhibition mediates gain control in an olfactory circuit. Nature 452:956–60
    [Google Scholar]
  108. 108.
    Owald D, Felsenberg J, Talbot CB, Das G, Perisse E et al. 2015. Activity of defined mushroom body output neurons underlies learned olfactory behavior in Drosophila. . Neuron 86:417–27
    [Google Scholar]
  109. 109.
    Papadopoulou M, Cassenaer S, Nowotny T, Laurent G 2011. Normalization for sparse encoding of odors by a wide-field interneuron. Science 332:721–25
    [Google Scholar]
  110. 110.
    Parnas M, Lin AC, Huetteroth W, Miesenböck G 2013. Odor discrimination in Drosophila: from neural population codes to behavior. Neuron 79:932–44
    [Google Scholar]
  111. 111.
    Perisse E, Owald D, Barnstedt O, Talbot CB, Huetteroth W, Waddell S 2016. Aversive learning and appetitive motivation toggle feed-forward inhibition in the Drosophila mushroom body. Neuron 90:1086–99
    [Google Scholar]
  112. 112.
    Pikielny CW, Hasan G, Rouyer F, Rosbash M 1994. Members of a family of Drosophila putative odorant-binding proteins are expressed in different subsets of olfactory hairs. Neuron 12:35–49
    [Google Scholar]
  113. 113.
    Ratcliff R 1978. Theory of memory retrieval. Psychol. Rev. 85:59–108
    [Google Scholar]
  114. 114.
    Resulaj A, Ruediger S, Olsen SR, Scanziani M 2018. First spikes in visual cortex enable perceptual discrimination. eLife 7:e34044
    [Google Scholar]
  115. 115.
    Rieke F, Warland D, de Ruyter van Steveninck R, Bialek W 1997. Spikes: Exploring the Neural Code Cambridge, MA: MIT Press
    [Google Scholar]
  116. 116.
    Roitman JD, Shadlen MN 2002. Response of neurons in the lateral intraparietal area during a combined visual discrimination reaction time task. J. Neurosci. 22:9475–89
    [Google Scholar]
  117. 117.
    Root CM, Masuyama K, Green DS, Enell LE, Nässel DR et al. 2008. A presynaptic gain control mechanism fine-tunes olfactory behavior. Neuron 59:311–21
    [Google Scholar]
  118. 118.
    Root CM, Semmelhack JL, Wong AM, Flores J, Wang JW 2007. Propagation of olfactory information in Drosophila. . PNAS 104:11826–31
    [Google Scholar]
  119. 119.
    Ruta V, Datta SR, Vasconcelos ML, Freeland J, Looger LL, Axel R 2010. A dimorphic pheromone circuit in Drosophila from sensory input to descending output. Nature 468:686–90
    [Google Scholar]
  120. 120.
    Sato K, Pellegrino M, Nakagawa T, Nakagawa T, Vosshall LB, Touhara K 2008. Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452:1002–6
    [Google Scholar]
  121. 121.
    Schuckel J, Torkkeli PH, French AS 2009. Two interacting olfactory transduction mechanisms have linked polarities and dynamics in Drosophila melanogaster antennal basiconic sensilla neurons. J. Neurophysiol. 102:214–23
    [Google Scholar]
  122. 122.
    Séjourné J, Plaçais P-Y, Aso Y, Siwanowicz I, Trannoy S et al. 2011. Mushroom body efferent neurons responsible for aversive olfactory memory retrieval in Drosophila. Nat. . Neurosci 14:903–10
    [Google Scholar]
  123. 123.
    Shadlen MN, Kiani R 2013. Decision making as a window on cognition. Neuron 80:791–806
    [Google Scholar]
  124. 124.
    Shadlen MN, Newsome WT 2001. Neural basis of a perceptual decision in the parietal cortex (area LIP) of the rhesus monkey. J. Neurophysiol. 86:1916–36
    [Google Scholar]
  125. 125.
    Shang Y, Claridge-Chang A, Sjulson L, Pypaert M, Miesenböck G 2007. Excitatory local circuits and their implications for olfactory processing in the fly antennal lobe. Cell 128:601–12
    [Google Scholar]
  126. 126.
    Shlens J 2014. Notes on Kullback-Leibler divergence and likelihood. arXiv 1404.2000[cs.IT]
  127. 127.
    Simoncelli EP, Olshausen BA 2001. Natural image statistics and neural representation. Annu. Rev. Neurosci. 24:1193–216
    [Google Scholar]
  128. 128.
    Stevens CF 2015. What the fly's nose tells the fly's brain. PNAS 112:9460–65
    [Google Scholar]
  129. 129.
    Stevens CF 2016. A statistical property of fly odor responses is conserved across odors. PNAS 113:6737–42
    [Google Scholar]
  130. 130.
    Stocker RF 1994. The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res 275:3–26
    [Google Scholar]
  131. 131.
    Stopfer M, Jayaraman V, Laurent G 2003. Intensity versus identity coding in an olfactory system. Neuron 39:991–1004
    [Google Scholar]
  132. 132.
    Störtkuhl KF, Hovemann BT, Carlson JR 1999. Olfactory adaptation depends on the Trp Ca2+ channel in Drosophila. J. Neurosci 19:4839–46
    [Google Scholar]
  133. 133.
    Strausfeld NJ, Hansen L, Li Y, Gomez RS, Ito K 1998. Evolution, discovery, and interpretations of arthropod mushroom bodies. Learn Mem 5:11–37
    [Google Scholar]
  134. 134.
    Suh GS, Wong AM, Hergarden AC, Wang JW, Simon AF et al. 2004. A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. . Nature 431:854–59
    [Google Scholar]
  135. 135.
    Szyszka P, Gerkin RC, Galizia CG, Smith BH 2014. High-speed odor transduction and pulse tracking by insect olfactory receptor neurons. PNAS 111:16925–30
    [Google Scholar]
  136. 136.
    Takemura S-Y, Aso Y, Hige T, Wong A, Lu Z et al. 2017. A connectome of a learning and memory center in the adult Drosophila brain. eLife 6:e26975
    [Google Scholar]
  137. 137.
    Tanaka NK, Tanimoto H, Ito K 2008. Neuronal assemblies of the Drosophila mushroom body. J. Comp. Neurol. 508:711–55
    [Google Scholar]
  138. 138.
    Turner GC, Bazhenov M, Laurent G 2008. Olfactory representations by Drosophila mushroom body neurons. J. Neurophysiol. 99:734–46
    [Google Scholar]
  139. 139.
    Uchida N, Mainen ZF 2003. Speed and accuracy of olfactory discrimination in the rat. Nat. Neurosci. 6:1224–29
    [Google Scholar]
  140. 140.
    Vosshall LB, Amrein H, Morozov PS, Rzhetsky A, Axel R 1999. A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96:725–36
    [Google Scholar]
  141. 141.
    Vosshall LB, Wong AM, Axel R 2000. An olfactory sensory map in the fly brain. Cell 102:147–59
    [Google Scholar]
  142. 142.
    Wang JW, Wong AM, Flores J, Vosshall LB, Axel R 2003. Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112:271–82
    [Google Scholar]
  143. 143.
    Wei A, Covarrubias M, Butler A, Baker K, Pak M, Salkoff L 1990. K+ current diversity is produced by an extended gene family conserved in Drosophila and mouse. Science 248:599–603
    [Google Scholar]
  144. 144.
    Wicher D, Schäfer R, Bauernfeind R, Stensmyr MC, Heller R et al. 2008. Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature 452:1007–11
    [Google Scholar]
  145. 145.
    Wilson RI, Laurent G 2005. Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe. J. Neurosci. 25:9069–79
    [Google Scholar]
  146. 146.
    Wilson RI, Turner GC, Laurent G 2004. Transformation of olfactory representations in the Drosophila antennal lobe. Science 303:366–70
    [Google Scholar]
  147. 147.
    Wong AM, Wang JW, Axel R 2002. Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109:229–41
    [Google Scholar]
  148. 148.
    Yaksi E, Wilson RI 2010. Electrical coupling between olfactory glomeruli. Neuron 67:1034–47
    [Google Scholar]
  149. 149.
    Yasuyama K, Meinertzhagen IA, Schürmann FW 2002. Synaptic organization of the mushroom body calyx in Drosophila melanogaster. J. Comp. Neurol 445:211–26
    [Google Scholar]
  150. 150.
    Zheng Z, Lauritzen JS, Perlman E, Robinson CG, Nichols M et al. 2018. A complete electron microscopy volume of the brain of adult Drosophila melanogaster. Cell 174:730–43.e22
    [Google Scholar]
/content/journals/10.1146/annurev-biophys-052118-115655
Loading
/content/journals/10.1146/annurev-biophys-052118-115655
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error