Coding odor identity and odor value in awake rodents

Progress in Brain Research

Volumn 208, Issue , 2014, Pages 205-222

  Nunez Parra, Alexia ^a   Li, Anan ^a,b   Restrepo, Diego ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b Wuhan National Laboratory for Optoelectronics   (China)

Author keywords

Anesthetized; Awake behaving; Olfaction; Olfactory bulb; Piriform cortex; Sniff

Indexed keywords

AFTERIMAGE; ARTICLE; BREATHING RATE; CODING; GRANULE CELL; MITRAL CELL; NONHUMAN; ODOR IDENTITY; ODOR VALUE; OLFACTORY BULB; OLFACTORY DISCRIMINATION; OLFACTORY SENSORY NEURON; PREFRONTAL CORTEX; PRIORITY JOURNAL; PYRIFORM CORTEX; SENSORY NERVE CELL; SIGNAL PROCESSING; SMELL AND TASTE PARAMETERS; SMELLING; SNIFFING; WAKEFULNESS; ACTION POTENTIAL; ANIMAL; CYTOLOGY; NERVE CELL NETWORK; ODOR; OLFACTORY SYSTEM; PHYSIOLOGY; RODENT;

ACTION POTENTIALS; ANIMALS; NERVE NET; ODORS; OLFACTORY BULB; OLFACTORY PATHWAYS; RODENTIA; SENSORY RECEPTOR CELLS; SMELL; WAKEFULNESS;

EID: 84899102804     PISSN: 00796123     EISSN: 18757855     Source Type: Book Series    
DOI: 10.1016/B978-0-444-63350-7.00008-5     Document Type: Chapter

References (85)

1. Araneda R.C., Firestein S. Adrenergic enhancement of inhibitory transmission in the accessory olfactory bulb. J. Neurosci. 2006, 26:3292-3298.
2. Balu R., Pressler R.T., Strowbridge B.W. Multiple modes of synaptic excitation of olfactory bulb granule cells. J. Neurosci. 2007, 27:5621-5632.
3. Bathellier B., Buhl D.L., Accolla R., Carleton A. Dynamic ensemble odor coding in the mammalian olfactory bulb: sensory information at different timescales. Neuron 2008, 57:586-598.
4. Bathellier B., Gschwend O., Carleton A. Temporal coding in olfaction. The Neurobiology of Olfaction 2010, CRC Press/Taylor & Francis, Boca Raton, FL. A. Menini (Ed.).
5. Beshel J., Kopell N., Kay L.M. Olfactory bulb gamma oscillations are enhanced with task demands. J. Neurosci. 2007, 27:8358-8365.
6. Boyd A.M., Sturgill J.F., Poo C., Isaacson J.S. Cortical feedback control of olfactory bulb circuits. Neuron 2012, 76:1161-1174.
7. Buonviso N., Amat C., Litaudon P., Roux S., Royet J.P., Farget V., Sicard G. Rhythm sequence through the olfactory bulb layers during the time window of a respiratory cycle. Eur. J. Neurosci. 2003, 17:1811-1819.
8. Buzsaki G., Watson B.O. Brain rhythms and neural syntax: implications for efficient coding of cognitive content and neuropsychiatric disease. Dialogues Clin. Neurosci. 2012, 14:345-367.
9. Cang J., Isaacson J.S. In vivo whole-cell recording of odor-evoked synaptic transmission in the rat olfactory bulb. J. Neurosci. 2003, 23:4108-4116.
10. Carey R.M., Verhagen J.V., Wesson D.W., Pirez N., Wachowiak M. Temporal structure of receptor neuron input to the olfactory bulb imaged in behaving rats. J. Neurophysiol. 2009, 101:1073-1088.
11. Cenier T., David F., Litaudon P., Garcia S., Amat C., Buonviso N. Respiration-gated formation of gamma and beta neural assemblies in the mammalian olfactory bulb. Eur. J. Neurosci. 2009, 29:921-930.
12. Cury K.M., Uchida N. Robust odor coding via inhalation-coupled transient activity in the mammalian olfactory bulb. Neuron 2010, 68:570-585.
13. Davison I.G., Katz L.C. Sparse and selective odor coding by mitral/tufted neurons in the main olfactory bulb. J. Neurosci. 2007, 27:2091-2101.
14. Devore S., Linster C. Noradrenergic and cholinergic modulation of olfactory bulb sensory processing. Front. Behav. Neurosci. 2012, 6:52.
15. Doucette W., Restrepo D. Profound context-dependent plasticity of mitral cell responses in olfactory bulb. PLoS Biol. 2008, 6:e258.
16. Doucette W., Gire D.H., Whitesell J., Carmean V., Lucero M.T., Restrepo D. Associative cortex features in the first olfactory brain relay station. Neuron 2011, 69:1176-1187.
17. Fletcher M.L., Masurkar A.V., Xing J., Imamura F., Xiong W., Nagayama S., Mutoh H., Greer C.A., Knopfel T., Chen W.R. Optical imaging of postsynaptic odor representation in the glomerular layer of the mouse olfactory bulb. J. Neurophysiol. 2009, 102:817-830.
18. Fukunaga I., Berning M., Kollo M., Schmaltz A., Schaefer A.T. Two distinct channels of olfactory bulb output. Neuron 2012, 75:320-329.
19. Gelperin A., Ghatpande A. Neural basis of olfactory perception. Ann. N. Y. Acad. Sci. 2009, 1170:277-285.
20. Gervais R., Buonviso N., Martin C., Ravel N. What do electrophysiological studies tell us about processing at the olfactory bulb level?. J. Physiol. Paris 2007, 101:40-45.
21. Gire D.H., Whitesell J.D., Doucette W., Restrepo D. Information for decision-making and stimulus identification is multiplexed in sensory cortex. Nat. Neurosci. 2013, 16:991-993.
22. Grosmaitre X., Santarelli L.C., Tan J., Luo M., Ma M. Dual functions of mammalian olfactory sensory neurons as odor detectors and mechanical sensors. Nat. Neurosci. 2007, 10:348-354.
23. Gschwend O., Beroud J., Carleton A. Encoding odorant identity by spiking packets of rate-invariant neurons in awake mice. PLoS One 2012, 7:e30155.
24. Haddad R., Lanjuin A., Madisen L., Zeng H., Murthy V.N., Uchida N. Olfactory cortical neurons read out a relative time code in the olfactory bulb. Nat. Neurosci. 2013, 16:949-957.
25. Igarashi K.M., Ieki N., An M., Yamaguchi Y., Nagayama S., Kobayakawa K., Kobayakawa R., Tanifuji M., Sakano H., Chen W.R., Mori K. Parallel mitral and tufted cell pathways route distinct odor information to different targets in the olfactory cortex. J. Neurosci. 2012, 32:7970-7985.
26. Imamura K., Mataga N., Mori K. Coding of odor molecules by mitral/tufted cells in rabbit olfactory bulb. I. Aliphatic compounds. J. Neurophysiol. 1992, 68:1986-2002.
27. Isaacson J.S., Strowbridge B.W. Olfactory reciprocal synapses: dendritic signaling in the CNS. Neuron 1998, 20:749-761.
28. Jahr C.E., Nicoll R.A. An intracellular analysis of dendrodendritic inhibition in the turtle in vitro olfactory bulb. J. Physiol. 1982, 326:213-234.
29. Jahr C.E., Nicoll R.A. Noradrenergic modulation of dendrodendritic inhibition in the olfactory bulb. Nature 1982, 297:227-229.
30. Johnson B.A., Leon M. Modular representations of odorants in the glomerular layer of the rat olfactory bulb and the effects of stimulus concentration. J. Comp. Neurol. 2000, 422:496-509.
31. Johnson B.A., Leon M. Chemotopic odorant coding in a mammalian olfactory system. J. Comp. Neurol. 2007, 503:1-34.
32. Kato H.K., Chu M.W., Isaacson J.S., Komiyama T. Dynamic sensory representations in the olfactory bulb: modulation by wakefulness and experience. Neuron 2012, 76:962-975.
33. Kay L.M. Theta oscillations and sensorimotor performance. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:3863-3868.
34. Kay L.M., Laurent G. Odor- and context-dependent modulation of mitral cell activity in behaving rats. Nat. Neurosci. 1999, 2:1003-1009.
35. Kay L.M., Beshel J., Brea J., Martin C., Rojas-Libano D., Kopell N. Olfactory oscillations: the what, how and what for. Trends Neurosci. 2009, 32:207-214.
36. Kepecs A., Uchida N., Mainen Z.F. The sniff as a unit of olfactory processing. Chem. Senses 2006, 31:167-179.
37. Kepecs A., Uchida N., Mainen Z.F. Rapid and precise control of sniffing during olfactory discrimination in rats. J. Neurophysiol. 2007, 98:205-213.
38. Khan A.G., Sarangi M., Bhalla U.S. Rats track odour trails accurately using a multi-layered strategy with near-optimal sampling. Nat. Commun. 2012, 3:703.
39. Kikuta S., Kashiwadani H., Mori K. Compensatory rapid switching of binasal inputs in the olfactory cortex. J. Neurosci. 2008, 28:11989-11997.
40. Kikuta S., Sato K., Kashiwadani H., Tsunoda K., Yamasoba T., Mori K. From the cover: neurons in the anterior olfactory nucleus pars externa detect right or left localization of odor sources. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:12363-12368.
41. Koulakov A.A., Rinberg D. Sparse incomplete representations: a potential role of olfactory granule cells. Neuron 2011, 72:124-136.
42. Lagier S., Panzanelli P., Russo R.E., Nissant A., Bathellier B., Sassoe-Pognetto M., Fritschy J.M., Lledo P.M. GABAergic inhibition at dendrodendritic synapses tunes gamma oscillations in the olfactory bulb. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:7259-7264.
43. Linster C., Cleland T.A. Glomerular microcircuits in the olfactory bulb. Neural Netw. 2009, 22:1169-1173.
44. Litaudon P., Garcia S., Buonviso N. Strong coupling between pyramidal cell activity and network oscillations in the olfactory cortex. Neuroscience 2008, 156:781-787.
45. Lowe G. Electrical signaling in the olfactory bulb. Curr. Opin. Neurobiol. 2003, 13:476-481.
46. Ma M., Luo M. Optogenetic activation of basal forebrain cholinergic neurons modulates neuronal excitability and sensory responses in the main olfactory bulb. J. Neurosci. 2012, 32:10105-10116.
47. Malnic B., Hirono J., Sato T., Buck L.B. Combinatorial receptor codes for odors. Cell 1999, 96:713-723.
48. Manabe H., Mori K. Sniff rhythm-paced fast and slow gamma-oscillations in the olfactory bulb: relation to tufted and mitral cells and behavioral states. J. Neurophysiol. 2013, 110:1593-1599.
49. Markopoulos F., Rokni D., Gire D.H., Murthy V.N. Functional properties of cortical feedback projections to the olfactory bulb. Neuron 2012, 76:1175-1188.
50. Martin C., Gervais R., Chabaud P., Messaoudi B., Ravel N. Learning-induced modulation of oscillatory activities in the mammalian olfactory system: the role of the centrifugal fibres. J. Physiol. Paris 2004, 98:467-478.
51. Matsutani S. Trajectory and terminal distribution of single centrifugal axons from olfactory cortical areas in the rat olfactory bulb. Neuroscience 2010, 169:436-448.
52. Miura K., Mainen Z.F., Uchida N. Odor representations in olfactory cortex: distributed rate coding and decorrelated population activity. Neuron 2012, 74:1087-1098.
53. Mombaerts P. Axonal wiring in the mouse olfactory system. Annu. Rev. Cell Dev. Biol. 2006, 22:713-737.
54. Mombaerts P., Wang F., Dulac C., Chao S.K., Nemes A., Mendelsohn M., Edmondson J., Axel R. Visualizing an olfactory sensory map. Cell 1996, 87:675-686.
55. Mori K., Nagao H., Yoshihara Y. The olfactory bulb: coding and processing of odor molecule information. Science 1999, 286:711-715.
56. Mori K., Takahashi Y.K., Igarashi K.M., Yamaguchi M. Maps of odorant molecular features in the Mammalian olfactory bulb. Physiol. Rev. 2006, 86:409-433.
57. Nagayama S., Enerva A., Fletcher M.L., Masurkar A.V., Igarashi K.M., Mori K., Chen W.R. Differential axonal projection of mitral and tufted cells in the mouse main olfactory system. Front. Neural Circuits 2010, 4:1-7.
58. Nara K., Saraiva L.R., Ye X., Buck L.B. A large-scale analysis of odor coding in the olfactory epithelium. J. Neurosci. 2011, 31:9179-9191.
59. Nunez-Parra A., Maurer R.K., Krahe K., Smith R.S., Araneda R.C. Disruption of centrifugal inhibition to olfactory bulb granule cells impairs olfactory discrimination. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:14777-14782.
60. Pain F., L'Heureux B., Gurden H. Visualizing odor representation in the brain: a review of imaging techniques for the mapping of sensory activity in the olfactory glomeruli. Cell. Mol. Life Sci. 2011, 68:2689-2709.
61. Patterson M.A., Lagier S., Carleton A. Odor representations in the olfactory bulb evolve after the first breath and persist as an odor afterimage. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:E3340-E3349.
62. Rinberg D., Gelperin A. Olfactory neuronal dynamics in behaving animals. Semin. Cell Dev. Biol. 2006, 17:454-461.
63. Rinberg D., Koulakov A., Gelperin A. Sparse odor coding in awake behaving mice. J. Neurosci. 2006, 26:8857-8865.
64. Rosero M.A., Aylwin M.L. Sniffing shapes the dynamics of olfactory bulb gamma oscillations in awake behaving rats. Eur. J. Neurosci. 2011, 34:787-799.
65. Schaefer M.L., Young D.A., Restrepo D. Olfactory fingerprints for major histocompatibility complex-determined body odors. J. Neurosci. 2001, 21:2481-2487.
66. Schoppa N.E., Kinzie J.M., Sahara Y., Segerson T.P., Westbrook G.L. Dendrodendritic inhibition in the olfactory bulb is driven by NMDA receptors. J. Neurosci. 1998, 18:6790-6802.
67. Serizawa S., Ishii T., Nakatani H., Tsuboi A., Nagawa F., Asano M., Sudo K., Sakagami J., Sakano H., Ijiri T., Matsuda Y., Suzuki M., Yamamori T., Iwakura Y. Mutually exclusive expression of odorant receptor transgenes. Nat. Neurosci. 2000, 3:687-693.
68. Shepherd G.M., Chen W.R., Greer C.A. Olfactory bulb. The Synaptic Organization of the Brain 2004, Oxford University Press, New York. G.M. Shepherd (Ed.).
69. Shusterman R., Smear M.C., Koulakov A.A., Rinberg D. Precise olfactory responses tile the sniff cycle. Nat. Neurosci. 2011, 14:1039-1044.
70. Smear M., Shusterman R., O'Connor R., Bozza T., Rinberg D. Perception of sniff phase in mouse olfaction. Nature 2011, 479:397-400.
71. Smith R.S., Araneda R.C. Cholinergic modulation of neuronal excitability in the accessory olfactory bulb. J. Neurophysiol. 2010, 104:2963-2974.
72. Spors H., Grinvald A. Spatio-temporal dynamics of odor representations in the mammalian olfactory bulb. Neuron 2002, 34:301-315.
73. Spors H., Wachowiak M., Cohen L.B., Friedrich R.W. Temporal dynamics and latency patterns of receptor neuron input to the olfactory bulb. J. Neurosci. 2006, 26:1247-1259.
74. Spors H., Albeanu D.F., Murthy V.N., Rinberg D., Uchida N., Wachowiak M., Friedrich R.W. Illuminating vertebrate olfactory processing. J. Neurosci. 2012, 32:14102-14108.
75. Verhagen J.V., Wesson D.W., Netoff T.I., White J.A., Wachowiak M. Sniffing controls an adaptive filter of sensory input to the olfactory bulb. Nat. Neurosci. 2007, 10:631-639.
76. Wachowiak M. Active sensing in olfaction. Neurobiology of Olfaction 2010, CRC Press, Boca Raton, FL, (Chapter 12). A. Menini (Ed.).
77. Wachowiak M. All in a sniff: olfaction as a model for active sensing. Neuron 2011, 71:962-973.
78. Wachowiak M., Cohen L.B. Representation of odorants by receptor neuron input to the mouse olfactory bulb. Neuron 2001, 32:723-735.
79. Wachowiak M., Shipley M.T. Coding and synaptic processing of sensory information in the glomerular layer of the olfactory bulb. Semin. Cell Dev. Biol. 2006, 17:411-423.
80. Wellis D.P., Scott J.W., Harrison T.A. Discrimination among odorants by single neurons of the rat olfactory bulb. J. Neurophysiol. 1989, 61:1161-1177.
81. Wesson D.W., Carey R.M., Verhagen J.V., Wachowiak M. Rapid encoding and perception of novel odors in the rat. PLoS Biol. 2008, 6:e82.
82. Wesson D.W., Donahou T.N., Johnson M.O., Wachowiak M. Sniffing behavior of mice during performance in odor-guided tasks. Chem. Senses 2008, 33:581-596.
83. Wesson D.W., Verhagen J.V., Wachowiak M. Why sniff fast? The relationship between sniff frequency, odor discrimination, and receptor neuron activation in the rat. J. Neurophysiol. 2009, 101:1089-1102.
84. Yokoi M., Mori K., Nakanishi S. Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:3371-3375.
85. Zhan C., Luo M. Diverse patterns of odor representation by neurons in the anterior piriform cortex of awake mice. J. Neurosci. 2010, 30:16662-16672.