Spike timing and neural codes for odors

Spike Timing: Mechanisms and Function

Volumn , Issue , 2013, Pages 273-297

  Reiter, Sam ^a   Stopfer, Mark ^b  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84908174214     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1201/b14859     Document Type: Chapter

References (111)

1. Araneda, R. C., Kini, A. D., and Firestein, S. 2000. The molecular receptive range of an odor-ant receptor. Nature Neuroscience 3, 1248-55.
2. Assisi, C., Stopfer, M., and Bazhenov, M. 2012. Balanced excitation and inhibition optimize odor processing in insect olfactory system. PLoS Computational Biology 8(7), e1002563.
3. Assisi, C., Stopfer, M., Laurent, G., and Bazhenov, M. 2007. Adaptive regulation of sparseness by feedforward inhibition. Nature Neuroscience 10, 1176-84.
4. Bathellier, B., Buhl, D. L., Accolla, R., and Carleton, A. 2008. Dynamic ensemble odor coding in the mammalian olfactory bulb: Sensory information at different timescales. Neuron 57, 586-98.
5. Bazhenov, M., Stopfer, M., Rabinovich, M., Huerta, R., Abarbanel, H. D., Sejnowski, T. J., and Laurent, G. 2001a. Model of transient oscillatory synchronization in the locust antennal lobe Neuron 30, 553-67.
6. Bazhenov, M., Stopfer, M., Rabinovich, M., Huerta, R., Abarbanel, H. D., Sejnowski, T. J., and Laurent, G. 2001b. Model of cellular and network mechanisms for odor-evoked temporal patterning in the locust antennal lobe Neuron 30, 569-81.
7. Bazhenov, M., Stopfer, M., Sejnowski, T. J., and Laurent, G. 2005. Fast odor learning improves reliability of odor responses in the locust antennal lobe. Neuron 46, 483-92.
8. Bhandawat, V., Olsen, S. R., Gouwens, N. W., Schlief, M. L., and Wilson, R. I. 2007. Sensory processing in the Drosophila antennal lobe increases reliability and separability of ensemble odor representations. Nature Neuroscience 10, 1474-82.
9. Bozza, T., Feinstein, P., Zheng, C., and Mombaerts, P. 2002. Odorant receptor expression defines functional units in the mouse olfactory system. Journal of Neuroscience 22, 3033-43.
10. Broome, B. M., Jayaraman, V., and Laurent, G. 2006. Encoding and decoding of overlapping odor sequences. Neuron 51(4), 467-82.
11. Brown, S. L., Joseph, J., and Stopfer, M. 2005. Encoding a temporally structured stimulus with a temporally structured neural representation. Nature Neuroscience 8, 1568-76.
12. Buck, L. B. 1996. Information coding in the vertebrate olfactory system. Annual Reviews Neuroscience 19, 517-44.
13. Cassenaer, S. and Laurent, G. 2007. Hebbian STDP in mushroom bodies facilitates the syn-chronous flow of olfactory information in locusts. Nature 448, 709-13.
14. Cassenaer, S. and Laurent, G. 2012. Conditional modulation of spike-timing-dependent plas-ticity for olfactory learning. Nature 482, 47-52.
15. Clyne, P. J., Warr, C. G., Freeman, M. R., Lessing, D., Kim, J., and Carlson, J. R. 1999. A novel family of divergent seven-transmembrane proteins: Candidate odorant receptors in Drosophila. Neuron 22, 327-38.
16. Couto, A., Alenius, M., and Dickson, B. J. 2005. Molecular, anatomical, and functional orga-nization of the Drosophila olfactory system. Current Biology 15, 1535-47.
17. Cury, K. M. and Uchida, N. 2010. Robust odor coding via inhalation-coupled transient activity in the mammalian olfactory bulb. Neuron 68, 570-85.
18. de Bruyne, M., Foster, K., and Carlson, J. R. 2001. Odor coding in the Drosophila antenna. Neuron 30, 537-52.
19. Demmer H. and Kloppenburg, P. 2009. Intrinsic membrane properties and inhibitory synaptic input of Kenyon cells as mechanisms for sparse coding? Journal of Neurophysiology 102.3, 1538-50.
20. Dhawale, A. K., Hagiwara, A., Bhalla, U. S., Murthy, V. N., and Albeanu, D. F. 2010. Non-redundant odor coding by sister mitral cells revealed by light addressable glomeruli in the mouse. Nature Neuroscience 13, 1404-12.
21. Dobritsa, A. A., Der Goes Van Naters, W. van, Warr, Coral G., Steinbrecht, R. A., and Carlson, J. R. 2003. Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron 37, 827-41.
22. Dubnau, J., Grady, L., Kitamoto, T., and Tully, T. 2001. Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory. Nature 411, 476-80.
23. Duchamp-Viret, P. 1999. Odor response properties of rat olfactory receptor neurons. Science 284, 2171-4.
24. Egger, V. and Urban, N. N. 2006. Dynamic connectivity in the mitral cell-granule cell micro-circuit. Seminars in Cell & Developmental Biology 17, 424-32.
25. Erber, J., Masuhr, T., and Menzel, R. 1980. Localization of short-term memory in the brain of the bee, Apis mellifera. Physiological Entomology 5, 343-58.
26. Esslen, J. and Kaissling, K. E. 1976. Zahl und Verteilung antennaler Sensillen bei der Honigbiene (Apis mellifera L.). Zoomorphologie 83, 227-51.
27. Firestein, S., Picco, C., and Menini, A. 1993. The relation between stimulus and response in olfactory receptor cells of the tiger salamander. The Journal of Physiology 468, 1-10.
28. Fishilevich, E. and Vosshall, L. B. 2005. Genetic and functional subdivision of the Drosophila antennal lobe. Current Biology 15, 1548-53.
29. Friedrich, R. W. and Laurent, G. 2001. Dynamic optimization of odor representations by slow temporal patterning of mitral cell activity. Science 291, 889-94.
30. Gupta, N. and Stopfer, M. 2012. Functional analysis of a higher olfactory center, the lateral horn. Journal of Neuroscience 32, 8138-48.
31. Hallem, E. A. and Carlson, J. R. 2006. Coding of odors by a receptor repertoire. Cell 125, 143-60.
32. Hartline, H. K. 1956. Inhibition in the eye of the limulus. The Journal of General Physiology 39, 651-73.
33. Heisenberg, M. 2003. Mushroom body memoir: From maps to models. Nature Reviews. Neuroscience 4, 266-75.
34. Heisenberg, M., Borst, A., Wagner, S., and Byers, D. 1985. Drosophila mushroom body mutants are deficient in olfactory learning. Journal of Neurogenetics 2, 1-30.
35. Hildebrand, J. G. and Shepherd, G. M. 1997. Mechanisms of olfactory discrimination: Converging evidence for common principles across phyla. Annual Review of Neuroscience 20, 595-631.
36. Homberg, U., Christensen, T. A., and Hildebrand, J. G. 1989. Structure and function of the deutocerebrum in insects. Annual Review of Entomology 34, 477-501.
37. Hopfield, J. J. 1995. Pattern recognition computation using action potential timing for stimulus representation. Nature 376, 33-6.
38. Hosler, J. S. and Smith, B. H. 2000. Blocking and the detection of odor components in blends. The Journal of Experimental Biology 203, 2797-806.
39. Huang, J., Zhang, W., Qiao, W., Hu, A., and Wang, Z. 2010. Functional connectivity and selec-tive odor responses of excitatory local interneurons in Drosophila antennal lobe. Neuron 67, 1021-33.
40. Hummel, T., Sekinger, B., Wolf, S. R., Pauli, E., and Kobal, G. 1997. “Sniffin” sticks: Olfactory performance assessed by the combined testing of odour identification, odor discrimina-tion and olfactory threshold. Chemical Senses 22, 39-52.
41. Ito, I., Bazhenov, M., Ong, R. C., Raman, B., and Stopfer, M. 2009. Frequency transitions in odor-evoked neural oscillations. Neuron 64, 692-706.
42. Ito, I., Ong, R. C.-Y., Raman, B., and Stopfer, M. 2008. Sparse odor representation and olfac-tory learning. Nature Neuroscience 11, 1177-84.
43. Jacquin-Joly, E. and Merlin, C. 2004. Insect olfactory receptors: Contributions of molecular biology to chemical ecology. Journal of Chemical Ecology 30, 2359-97.
44. Jayaraman, V. and Laurent, G. 2007. Evaluating a genetically encoded optical sensor of neural activity using electrophysiology in intact adult fruit flies. Frontiers in Neural Circuits 1, 3.
45. Jortner, R. A., Farivar, S. S., and Laurent, G. 2007. A simple connectivity scheme for sparse coding in an olfactory system. The Journal of Neuroscience 27, 1659-69.
46. Joseph, J., Dunn, F. A., and Stopfer, M. 2012. Spontaneous olfactory receptor neuron activity determines follower cell response properties. The Journal of Neuroscience 32, 2900-10.
47. Kaupp, U. B. 2010. Olfactory signalling in vertebrates and insects: Differences and common-alities. Nature Reviews. Neuroscience 11, 188-200.
48. Kay, L. M., Beshel, J., Brea, J., Martin, C., Rojas-Líbano, D., and Kopell, N. 2009. Olfactory oscillations: The what, how and what for. Trends in Neurosciences 32, 207-14.
49. Kay, L. M. and Stopfer, M. 2006. Information processing in the olfactory systems of insects and vertebrates. Seminars in Cell & Developmental Biology 17, 433-42.
50. Kleene, S. J. 2008. The electrochemical basis of odor transduction in vertebrate olfactory cilia. Chemical Senses 33, 839-59.
51. Krashes, M. J., DasGupta, S., Vreede, A., White, B., Armstrong, J. D., and Waddell, S. 2009. A neural circuit mechanism integrating motivational state with memory expression in Drosophila. Cell 139, 416-27.
52. Krashes, M. J., Keene, A. C., Leung, B., Armstrong, J. D., and Waddell, S. 2007. Sequential use of mushroom body neuron subsets during Drosophila odor memory processing. Neuron 53, 103-15.
53. Kuffler, S. W. 1953. Discharge patterns and functional organization of mammalian retina. Journal of Neurophysiology 16, 37-68.
54. Laurent, G. 2002. Olfactory network dynamics and the coding of multidimensional signals. Nature Reviews. Neuroscience 3, 884-95.
55. Laurent, G. and Davidowitz, H. 1994. Encoding of olfactory information with oscillating neu-ral assemblies. Science 265, 1872-5.
56. Laurent, G. and Naraghi, M. 1994. Odorant-induced oscillations in the mushroom bodies of the locust. The Journal of Neuroscience 14, 2993-3004.
57. Lei, H., Christensen, T. A., and Hildebrand, J. G. 2002. Local inhibition modulates odor-evoked synchronization of glomerulus-specific output neurons. Nature Neuroscience 5, 557-65.
58. MacLeod, K. M. and Carr, C. E. 2007. Beyond timing in the auditory brainstem: Intensity coding in the avian cochlear nucleus angularis. In: Computational Neuroscience: Theoretical Insights Into Brain Function. Eds: P. Cisek, T. Drew, and J.F. Kalaska. Elsevier, Amsterdam.
59. MacLeod, K. and Laurent, G. 1996. Distinct mechanisms for synchronization and temporal patterning of odor-encoding neural assemblies. Science 274, 976-9.
60. Malnic, B., Hirono, J., Sato, T., and Buck, L. B. 1999. Combinatorial receptor codes for odors. Cell 96, 713-23.
61. Mazor, O. and Laurent, G. 2005. Transient dynamics versus fixed points in odor representa-tions by locust antennal lobe projection neurons. Neuron 48, 661-73.
62. McGuire, S. E., Le, P. T., and Davis, R. L. 2001. The role of Drosophila mushroom body sig-naling in olfactory memory. Science 293, 1330-3.
63. Michel, W. C. and Ache, B. W. 1994. Odor-evoked inhibition in primary olfactory receptor neurons. Chemical Senses 19, 11-24.
64. Mombaerts, P. 2004. Odorant receptor gene choice in olfactory sensory neurons: The one receptor-one neuron hypothesis revisited. Current Opinion in Neurobiology 14, 31-6.
65. Mombaerts, P., Wang, F., Dulac, C., Chao, S. K., Nemes, A., Mendelsohn, M., Edmondson, J., and Axel, R. 1996. Visualizing an olfactory sensory map. Cell 87, 675-86.
66. Neville, K. R. and Haberly, L. B. 2003. Beta and gamma oscillations in the olfactory system of the urethane-anesthetized rat. Journal of Neurophysiology, 90(6), 3921-30.
67. Ng, M., Roorda, R. D., Lima, S. Q., Zemelman, B. V., Morcillo, P., and Miesenböck, G. 2002. Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron 36, 463-74.
68. Olsen, S. R., Bhandawat, V., and Wilson, R. I. 2007. Excitatory interactions between olfactory processing channels in the Drosophila antennal lobe. Neuron 54, 89-103.
69. Papadopoulou, M., Cassenaer, S., Nowotny, T., and Laurent, G. 2011. Normalization for sparse encoding of odors by a wide field interneuron. Science 332, 721-5.
70. Perez-Orive, J., Mazor, O., Turner, G. C., Cassenaer, S., Wilson, R. I., and Laurent, G. 2002. Oscillations and sparsening of odor representations in the mushroom body. Science 297, 359-65.
71. Pomeroy, S., LaMantia, A., and Purves, D. 1990. Postnatal construction of neural circuitry in the mouse olfactory bulb. The Journal of Neuroscience 10, 1952-66.
72. Poo, C. and Isaacson, J. S. 2009. Odor representations in olfactory cortex: “Sparse” coding, global inhibition, and oscillations. Neuron 62, 850-61.
73. Pouget, A., Dayan, P., and Zemel, R. 2000. Information processing with population codes. Nature Reviews. Neuroscience 1, 125-32.
74. Raman, B., Joseph, J., Tang, J., and Stopfer, M. 2010. Temporally diverse firing patterns in olfactory receptor neurons underlie spatiotemporal neural codes for odors. The Journal of Neuroscience 30, 1994-2006.
75. Ressler, K. 1993. A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell 73, 597-609.
76. Rinberg, D., Koulakov, A., and Gelperin, A. 2006. Speed-accuracy tradeoff in olfaction. Neuron 51, 351-8.
77. Roweis, S. T. and Saul, L. K. 2000. Nonlinear dimensionality reduction by locally linear embedding. Science 290, 2323-6.
78. Rützler, M. and Zwiebel, L. J. 2005. Molecular biology of insect olfaction: Recent progress and conceptual models. Journal of Comparative Physiology. A 191, 777-90.
79. Sato, K., Pellegrino, M., Nakagawa, T., Nakagawa, T., Vosshall, L. B., and Touhara, K. 2008. Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452, 1002-6.
80. Schoppa, N. 2003. Dendritic processing within olfactory bulb circuits. Trends in Neurosciences 26, 501-6.
81. Schwaerzel, M., Heisenberg, M., and Zars, T. 2002. Extinction antagonizes olfactory memory at the subcellular level. Neuron 35, 951-60.
82. Shang, Y., Claridge-Chang, A., Sjulson, L., Pypaert, M., and Miesenböck, G. 2007. Excitatory local circuits and their implications for olfactory processing in the fly antennal lobe. Cell 128, 601-12.
83. Sobel, N., Prabhakaran, V., Desmond, J. E., Glover, G. H., Goode, R. L., Sullivan, E. V., and Gabrieli, J. D. 1998. Sniffing and smelling: Separate subsystems in the human olfactory cortex. Nature 392, 282-6.
84. Spors, H. and Grinvald, A. 2002. Spatio-temporal dynamics of odor representations in the mammalian olfactory bulb. Neuron 34, 301-15.
85. Spors, H., Wachowiak, M., Cohen, L. B., and Friedrich, R. W. 2006. Temporal dynam-ics and latency patterns of receptor neuron input to the olfactory bulb. The Journal of Neuroscience 26, 1247-59.
86. Stocker, R. F. 1994. The organization of the chemosensory system in Drosophila melanogas-ter: A review. Cell and Tissue Research 275, 3-26.
87. Stokes, C. C. A. and Isaacson, J. S. 2010. From dendrite to soma: Dynamic routing of inhibition by complementary interneuron microcircuits in olfactory cortex. Neuron 67, 452-65.
88. Stopfer, M., Bhagavan, S., Smith, B. H., and Laurent, G. 1997. Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 390, 70-4.
89. Stopfer, M., Jayaraman, V., and Laurent, G. 2003. Intensity versus identity coding in an olfac-tory system. Neuron 39, 991-1004.
90. Stopfer, M. and Laurent, G. 1999. Short-term memory in olfactory network dynamics. Nature 402, 664-8.
91. Su, C.-Y., Menuz, K., and Carlson, J. R. 2009. Olfactory perception: Receptors, cells, and circuits. Cell 139, 45-59.
92. Tanaka, N. K., Ito, K., and Stopfer, M. 2009. Odor-evoked neural oscillations in Drosophila are mediated by widely branching interneurons. The Journal of Neuroscience 29, 8595-603.
93. Tripathy, S. J., Peters, O. J., Staudacher, E. M., Kalwar, F. R., Hatfield, M. N., and Daly, K. C. 2010. Odors pulsed at wing beat frequencies are tracked by primary olfactory networks and enhance odor detection. Frontiers in Cellular Neuroscience 4, 1.
94. Turner, G. C., Bazhenov, M., and Laurent, G. 2008. Olfactory representations by Drosophila mushroom body neurons. Journal of Neurophysiology 99, 734-46.
95. Uchida, N., Takahashi, Y. K., Tanifuji, M., and Mori, K. 2000. Odor maps in the mamma-lian olfactory bulb: Domain organization and odorant structural features. Nature Neuroscience 3, 1035-43.
96. Vassar, R., Ngai, J., and Axel, R. 1993. Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium. Cell 74, 309-18.
97. 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. Nature Neuroscience 10, 631-9.
98. Vogt, R. G. and Riddiford, L. M. 1981. Pheromone binding and inactivation by moth antennae. Nature 293, 161-3.
99. Vosshall, L. B., Amrein, H., Morozov, P. S., Rzhetsky, A., and Axel, R. 1999. A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96, 725-36.
100. Vosshall, L. B., Wong, A. M., and Axel, R. 2000. An olfactory sensory map in the fly brain. Cell 102, 147-59.
101. Wachowiak, M. and Cohen, L. B. 2001. Representation of odorants by receptor neuron input to the mouse olfactory bulb. Neuron 32, 723-35.
102. Wachowiak, M. and Shipley, M. T. 2006. Coding and synaptic processing of sensory informa-tion in the glomerular layer of the olfactory bulb. Seminars in Cell & Developmental Biology 17, 411-23.
103. Waldrop, B., Christensen, T. A., and Hildebrand, J. G. 1987. GABA-mediated synaptic inhi-bition of projection neurons in the antennal lobes of the sphinx moth, Manduca sexta. Journal of Comparative Physiology A 161, 23-32.
104. Wang, J. W., Wong, A. M., Flores, J., Vosshall, L. B., and Axel, R. 2003. Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112, 271-82.
105. Wehr, M. and Laurent, G. 1996. Odour encoding by temporal sequences of firing in oscillating neural assemblies. Nature 384, 162-6.
106. Werblin, S. and Dowling, E. 1969. Organization of the retina of the mudpuppy, recording nec-turus macubsus. II. Intracellular. Journal of Neurophysiology 32, 339-55.
107. Wicher, D., Schäfer, R., Bauernfeind, R., Stensmyr, M. C., Heller, R., Heinemann, S. H., and Hansson, B. S. 2008. Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature 452, 1007-11.
108. Wilson, R. I. and Mainen, Z. F. 2006. Early events in olfactory processing. Annual Review of Neuroscience 29, 163-201.
109. Wilson, R. I., Turner G. C., and Laurent G. 2004. Transformation of olfactory representations in the Drosophila antennal lobe. Science 303(5656), 366-70.
110. Wright, G. A., Lutmerding, A., Dudareva, N., and Smith, Brian H 2005. Intensity and the ratios of compounds in the scent of snapdragon flowers affect scent discrimination by honeybees (Apis mellifera). Journal of Comparative Physiology. A 191, 105-14.
111. Yaksi, E. and Wilson, R. I. 2010. Electrical coupling between olfactory glomeruli. Neuron 67, 1034-47.