Construction of functional neuronal circuitry in the olfactory bulb

Seminars in Cell and Developmental Biology

Volumn 35, Issue , 2014, Pages 180-188

  Imai, Takeshi ^a,b  

^a RIKEN Center for Biosystems Dynamics Research   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Development; Glomerulus; Lateral inhibition; Olfactory bulb; Plasticity; Temporal coding

Indexed keywords

PARVALBUMIN;

BRAIN CORTEX; CELLS; CODING; FEEDBACK SYSTEM; GAMMA OSCILLATION; GLOMERULUS; GRANULE CELL; HUMAN; INFORMATION PROCESSING; INHIBITION KINETICS; INTERNEURON; MITRAL CELL; NERVE CELL PLASTICITY; NERVE FIBER; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM PARAMETERS; NEUROMODULATION; NEURONAL CIRCUITRY; NONHUMAN; ODOR; OLFACTORY BULB; OSCILLATION; PRESYNAPTIC INHIBITION; REVIEW; SYNAPTIC TRANSMISSION; TUFTED CELL; ANATOMY AND HISTOLOGY; ANIMAL; BIOLOGICAL MODEL; CYTOLOGY; NERVE CELL; NERVE CELL NETWORK; OLFACTORY SYSTEM; PHYSIOLOGY;

ANIMALS; HUMANS; MODELS, NEUROLOGICAL; NERVE NET; NEURONAL PLASTICITY; NEURONS; ODORS; OLFACTORY BULB; OLFACTORY PATHWAYS; SMELL;

EID: 84908668396     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2014.07.012     Document Type: Review

References (141)

1. Shepherd G.M., Greer C.A., Mazzarello P., Sassoe-Pognetto M. The first images of nerve cells: Golgi on the olfactory bulb 1875. Brain Res Rev 2011, 66:92-105.
2. Buck L., Axel R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 1991, 65:175-187.
3. Mombaerts P., Wang F., Dulac C., Chao S., Nemes A., Mendelsohn M., et al. Visualizing an olfactory sensory map. Cell 1996, 87:675-686.
4. Imai T., Sakano H. Odorant receptor-mediated signaling in the mouse. Curr Opin Neurobiol 2008, 18:251-260.
5. Imai T., Sakano H. Axon-axon interactions in neuronal circuit assembly: lessons from olfactory map formation. Eur J Neurosci 2011, 34:1647-1654.
6. Imai T., Sakano H., Vosshall L.B. Topographic mapping - the olfactory system. Cold Spring Harb Perspect Biol 2010, 2:a001776.
7. Isaacson J.S. Odor representations in mammalian cortical circuits. Curr Opin Neurobiol 2010, 20:328-331.
8. Giessel A.J., Datta S.R. Olfactory maps, circuits and computations. Curr Opin Neurobiol 2014, 24C:120-132.
9. Sosulski D.L., Bloom M.L., Cutforth T., Axel R., Datta S.R. Distinct representations of olfactory information in different cortical centres. Nature 2011, 472:213-216.
10. Ke M.T., Fujimoto S., Imai T. SeeDB: a simple and morphology-preserving optical clearing agent for neuronal circuit reconstruction. Nat Neurosci 2013, 16:1154-1161.
11. Murphy G.J., Darcy D.P., Isaacson J.S. Intraglomerular inhibition: signaling mechanisms of an olfactory microcircuit. Nat Neurosci 2005, 8:354-364.
12. Aroniadou-Anderjaska V., Zhou F.M., Priest C.A., Ennis M., Shipley M.T. Tonic and synaptically evoked presynaptic inhibition of sensory input to the rat olfactory bulb via GABA(B) heteroreceptors. J Neurophysiol 2000, 84:1194-1203.
13. Hsia A.Y., Vincent J.D., Lledo P.M. Dopamine depresses synaptic inputs into the olfactory bulb. J Neurophysiol 1999, 82:1082-1085.
14. Wachowiak M., McGann J.P., Heyward P.M., Shao Z., Puche A.C., Shipley M.T. Inhibition [corrected] of olfactory receptor neuron input to olfactory bulb glomeruli mediated by suppression of presynaptic calcium influx. J Neurophysiol 2005, 94:2700-2712.
15. Olsen S.R., Wilson R.I. Lateral presynaptic inhibition mediates gain control in an olfactory circuit. Nature 2008, 452:956-960.
16. McGann J.P., Pirez N., Gainey M.A., Muratore C., Elias A.S., Wachowiak M. Odorant representations are modulated by intra- but not interglomerular presynaptic inhibition of olfactory sensory neurons. Neuron 2005, 48:1039-1053.
17. Vucinic D., Cohen L.B., Kosmidis E.K. Interglomerular center-surround inhibition shapes odorant-evoked input to the mouse olfactory bulb in vivo. J Neurophysiol 2006, 95:1881-1887.
18. Fleischmann A., Shykind B.M., Sosulski D.L., Franks K.M., Glinka M.E., Mei D.F., et al. Mice with a monoclonal nose: perturbations in an olfactory map impair odor discrimination. Neuron 2008, 60:1068-1081.
19. Schoppa N.E., Westbrook G.L. Glomerulus-specific synchronization of mitral cells in the olfactory bulb. Neuron 2001, 31:639-651.
20. Christie J.M., Bark C., Hormuzdi S.G., Helbig I., Monyer H., Westbrook G.L. Connexin36 mediates spike synchrony in olfactory bulb glomeruli. Neuron 2005, 46:761-772.
21. Hayar A., Shipley M.T., Ennis M. Olfactory bulb external tufted cells are synchronized by multiple intraglomerular mechanisms. J Neurosci 2005, 25:8197-8208.
22. Dhawale A.K., Hagiwara A., Bhalla U.S., Murthy V.N., Albeanu D.F. Non-redundant odor coding by sister mitral cells revealed by light addressable glomeruli in the mouse. Nat Neurosci 2010, 13:1404-1412.
23. Kikuta S., Fletcher M.L., Homma R., Yamasoba T., Nagayama S. Odorant response properties of individual neurons in an olfactory glomerular module. Neuron 2013, 77:1122-1135.
24. Willhite D.C., Nguyen K.T., Masurkar A.V., Greer C.A., Shepherd G.M., Chen W.R. Viral tracing identifies distributed columnar organization in the olfactory bulb. Proc Natl Acad Sci U S A 2006, 103:12592-12597.
25. Kim D.H., Phillips M.E., Chang A.Y., Patel H.K., Nguyen K.T., Willhite D.C. Lateral connectivity in the olfactory bulb is sparse and segregated. Front Neural Circuits 2011, 5:5.
26. Miyamichi K., Amat F., Moussavi F., Wang C., Wickersham I., Wall N.R., et al. Cortical representations of olfactory input by trans-synaptic tracing. Nature 2011, 472:191-196.
27. Ghosh S., Larson S.D., Hefzi H., Marnoy Z., Cutforth T., Dokka K., et al. Sensory maps in the olfactory cortex defined by long-range viral tracing of single neurons. Nature 2011, 472:217-220.
28. 2 avoidance responses in Drosophila. Science 2013, 340:1338-1341.
29. Padmanabhan K., Urban N.N. Intrinsic biophysical diversity decorrelates neuronal firing while increasing information content. Nat Neurosci 2010, 13:1276-1282.
30. Nagayama S., Takahashi Y.K., Yoshihara Y., Mori K. Mitral and tufted cells differ in the decoding manner of odor maps in the rat olfactory bulb. J Neurophysiol 2004, 91:2532-2540.
31. Igarashi K.M., Ieki N., An M., Yamaguchi Y., Nagayama S., Kobayakawa K., et al. Parallel mitral and tufted cell pathways route distinct odor information to different targets in the olfactory cortex. J Neurosci 2012, 32:7970-7985.
32. Gire D.H., Franks K.M., Zak J.D., Tanaka K.F., Whitesell J.D., Mulligan A.A., et al. Mitral cells in the olfactory bulb are mainly excited through a multistep signaling path. J Neurosci 2012, 32:2964-2975.
33. Fukunaga I., Berning M., Kollo M., Schmaltz A., Schaefer A.T. Two distinct channels of olfactory bulb output. Neuron 2012, 75:320-329.
34. De Saint Jan D., Hirnet D., Westbrook G.L., Charpak S. External tufted cells drive the output of olfactory bulb glomeruli. J Neurosci 2009, 29:2043-2052.
35. Hong W., Luo L. Genetic control of wiring specificity in the fly olfactory system. Genetics 2014, 196:17-29.
36. Imamura F., Ayoub A.E., Rakic P., Greer C.A. Timing of neurogenesis is a determinant of olfactory circuitry. Nat Neurosci 2011, 14:331-337.
37. Gao P., Sultan K.T., Zhang X.J., Shi S.H. Lineage-dependent circuit assembly in the neocortex. Development 2013, 140:2645-2655.
38. Ohtsuki G., Nishiyama M., Yoshida T., Murakami T., Histed M., Lois C., et al. Similarity of visual selectivity among clonally related neurons in visual cortex. Neuron 2012, 75:65-72.
39. Li Y., Lu H., Cheng P.L., Ge S., Xu H., Shi S.H., et al. Clonally related visual cortical neurons show similar stimulus feature selectivity. Nature 2012, 486:118-121.
40. Xu H.T., Han Z., Gao P., He S., Li Z., Shi W., et al. Distinct lineage-dependent structural and functional organization of the hippocampus. Cell 2014, 157:1552-1564.
41. Couper Leo J.M., Brunjes P.C. Neonatal focal denervation of the rat olfactory bulb alters cell structure and survival: a Golgi, Nissl and confocal study. Brain Res Dev Brain Res 2003, 140:277-286.
42. Kobayakawa K., Kobayakawa R., Matsumoto H., Oka Y., Imai T., Ikawa M., et al. Innate versus learned odour processing in the mouse olfactory bulb. Nature 2007, 450:503-508.
43. Belluscio L., Lodovichi C., Feinstein P., Mombaerts P., Katz L.C. Odorant receptors instruct functional circuitry in the mouse olfactory bulb. Nature 2002, 419:296-300.
44. Malun D., Brunjes P.C. Development of olfactory glomeruli: temporal and spatial interactions between olfactory receptor axons and mitral cells in opossums and rats. J Comp Neurol 1996, 368:1-16.
45. Matsutani S., Yamamoto N. Differentiation of mitral cell dendrites in the developing main olfactory bulbs of normal and naris-occluded rats. J Comp Neurol 2000, 418:402-410.
46. Lin D.M., Wang F., Lowe G., Gold G.H., Axel R., Ngai J., et al. Formation of precise connections in the olfactory bulb occurs in the absence of odorant-evoked neuronal activity. Neuron 2000, 26:69-80.
47. Maher B.J., McGinley M.J., Westbrook G.L. Experience-dependent maturation of the glomerular microcircuit. Proc Natl Acad Sci U S A 2009, 106:16865-16870.
48. Angelo K., Rancz E.A., Pimentel D., Hundahl C., Hannibal J., Fleischmann A., et al. A biophysical signature of network affiliation and sensory processing in mitral cells. Nature 2012, 488:375-378.
49. Su C.Y., Menuz K., Reisert J., Carlson J.R. Non-synaptic inhibition between grouped neurons in an olfactory circuit. Nature 2012, 492:66-71.
50. Bokil H., Laaris N., Blinder K., Ennis M., Keller A. Ephaptic interactions in the mammalian olfactory system. J Neurosci 2001, 21:RC173.
51. 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.
52. Kosaka T., Kosaka K. Tyrosine hydroxylase-positive GABAergic juxtaglomerular neurons are the main source of the interglomerular connections in the mouse main olfactory bulb. Neurosci Res 2008, 60:349-354.
53. Kiyokage E., Pan Y.Z., Shao Z., Kobayashi K., Szabo G., Yanagawa Y., et al. Molecular identity of periglomerular and short axon cells. J Neurosci 2010, 30:1185-1196.
54. Brill M.S., Ninkovic J., Winpenny E., Hodge R.D., Ozen I., Yang R., et al. Adult generation of glutamatergic olfactory bulb interneurons. Nat Neurosci 2009, 12:1524-1533.
55. Aungst J.L., Heyward P.M., Puche A.C., Karnup S.V., Hayar A., Szabo G., et al. Centre-surround inhibition among olfactory bulb glomeruli. Nature 2003, 426:623-629.
56. Whitesell J.D., Sorensen K.A., Jarvie B.C., Hentges S.T., Schoppa N.E. Interglomerular lateral inhibition targeted on external tufted cells in the olfactory bulb. J Neurosci 2013, 33:1552-1563.
57. Wachowiak M., Economo M.N., Diaz-Quesada M., Brunert D., Wesson D.W., White J.A., et al. Optical dissection of odor information processing in vivo using GCaMPs expressed in specified cell types of the olfactory bulb. J Neurosci 2013, 33:5285-5300.
58. Homma R., Kovalchuk Y., Konnerth A., Cohen L.B., Garaschuk O. In vivo functional properties of juxtaglomerular neurons in the mouse olfactory bulb. Front Neural Circuits 2013, 7:23.
59. Merkle F.T., Fuentealba L.C., Sanders T.A., Magno L., Kessaris N., Alvarez-Buylla A. Adult neural stem cells in distinct microdomains generate previously unknown interneuron types. Nat Neurosci 2014, 17:207-214.
60. Isaacson J.S., Strowbridge B.W. Olfactory reciprocal synapses: dendritic signaling in the CNS. Neuron 1998, 20:749-761.
61. Halabisky B., Friedman D., Radojicic M., Strowbridge B.W. Calcium influx through NMDA receptors directly evokes GABA release in olfactory bulb granule cells. J Neurosci 2000, 20:5124-5134.
62. Chen W.R., Xiong W., Shepherd G.M. Analysis of relations between NMDA receptors and GABA release at olfactory bulb reciprocal synapses. Neuron 2000, 25:625-633.
63. Egger V., Svoboda K., Mainen Z.F. Mechanisms of lateral inhibition in the olfactory bulb: efficiency and modulation of spike-evoked calcium influx into granule cells. J Neurosci 2003, 23:7551-7558.
64. Kato H.K., Gillet S.N., Peters A.J., Isaacson J.S., Komiyama T. Parvalbumin-expressing interneurons linearly control olfactory bulb output. Neuron 2013, 80:1218-1231.
65. Fantana A.L., Soucy E.R., Meister M. Rat olfactory bulb mitral cells receive sparse glomerular inputs. Neuron 2008, 59:802-814.
66. 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.
67. Miyamichi K., Shlomai-Fuchs Y., Shu M., Weissbourd B.C., Luo L., Mizrahi A. Dissecting local circuits: parvalbumin interneurons underlie broad feedback control of olfactory bulb output. Neuron 2013, 80:1232-1245.
68. Huang L., Garcia I., Jen H.I., Arenkiel B.R. Reciprocal connectivity between mitral cells and external plexiform layer interneurons in the mouse olfactory bulb. Front Neural Circuits 2013, 7:32.
69. Lodovichi C., Belluscio L., Katz L.C. Functional topography of connections linking mirror-symmetric maps in the mouse olfactory bulb. Neuron 2003, 38:265-276.
70. Mori K., Sakano H. How is the olfactory map formed and interpreted in the mammalian brain?. Annu Rev Neurosci 2011, 34:467-499. 10.1146/annurev-neuro-112210-112917.
71. Zhou Z., Belluscio L. Coding odorant concentration through activation timing between the medial and lateral olfactory bulb. Cell Rep 2012, 2:1143-1150.
72. Zhou Z., Belluscio L. Intrabulbar projecting external tufted cells mediate a timing-based mechanism that dynamically gates olfactory bulb output. J Neurosci 2008, 28:9920-9928.
73. Marks C.A., Cheng K., Cummings D.M., Belluscio L. Activity-dependent plasticity in the olfactory intrabulbar map. J Neurosci 2006, 26:11257-11266.
74. Batista-Brito R., Close J., Machold R., Fishell G. The distinct temporal origins of olfactory bulb interneuron subtypes. J Neurosci 2008, 28:3966-3975.
75. Lledo P.M., Merkle F.T., Alvarez-Buylla A. Origin and function of olfactory bulb interneuron diversity. Trends Neurosci 2008, 31:392-400.
76. Merkle F.T., Mirzadeh Z., Alvarez-Buylla A. Mosaic organization of neural stem cells in the adult brain. Science 2007, 317:381-384.
77. Hansen D.V., Lui J.H., Flandin P., Yoshikawa K., Rubenstein J.L., Alvarez-Buylla A., et al. Non-epithelial stem cells and cortical interneuron production in the human ganglionic eminences. Nat Neurosci 2013, 16:1576-1587.
78. Loulier K., Barry R., Mahou P., Le Franc Y., Supatto W., Matho K.S., et al. Multiplex cell and lineage tracking with combinatorial labels. Neuron 2014, 81:505-520.
79. Nagayama S., Enerva A., Fletcher M.L., Masurkar A.V., Igarashi K.M., Mori K., et al. Differential axonal projection of mitral and tufted cells in the mouse main olfactory system. Front Neural Circuits 2010, 4.
80. Arenkiel B.R., Peca J., Davison I.G., Feliciano C., Deisseroth K., Augustine G.J., et al. In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2. Neuron 2007, 54:205-218.
81. Apicella A., Yuan Q., Scanziani M., Isaacson J.S. Pyramidal cells in piriform cortex receive convergent input from distinct olfactory bulb glomeruli. J Neurosci 2010, 30:14255-14260.
82. Stettler D.D., Axel R. Representations of odor in the piriform cortex. Neuron 2009, 63:854-864.
83. Choi G.B., Stettler D.D., Kallman B.R., Bhaskar S.T., Fleischmann A., Axel R. Driving opposing behaviors with ensembles of piriform neurons. Cell 2011, 146:1004-1015.
84. Yan Z.Q., Tan J., Qin C., Lu Y., Ding C., Luo M.M. Precise circuitry links bilaterally symmetric olfactory maps. Neuron 2008, 58:613-624.
85. 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.
86. Rajan R., Clement J.P., Bhalla U.S. Rats smell in stereo. Science 2006, 311:666-670.
87. Imai T., Sakano H. Interhemispheric olfactory circuit and the memory beyond. Neuron 2008, 58:465-467.
88. Caron S.J., Ruta V., Abbott L.F., Axel R. Random convergence of olfactory inputs in the Drosophila mushroom body. Nature 2013, 497:113-117.
89. Jefferis G.S., Potter C.J., Chan A.M., Marin E.C., Rohlfing T., Maurer C.R., et al. Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation. Cell 2007, 128:1187-1203.
90. Miyasaka N., Arganda-Carreras I., Wakisaka N., Masuda M., Sumbul U., Seung H.S., et al. Olfactory projectome in the zebrafish forebrain revealed by genetic single-neuron labelling. Nat Commun 2014, 5:3639.
91. Dhande O.S., Huberman A.D. Retinal ganglion cell maps in the brain: implications for visual processing. Curr Opin Neurobiol 2014, 24C:133-142.
92. 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.
93. Boyd A.M., Sturgill J.F., Poo C., Isaacson J.S. Cortical feedback control of olfactory bulb circuits. Neuron 2012, 76:1161-1174.
94. Fletcher M.L., Chen W.R. Neural correlates of olfactory learning: critical role of centrifugal neuromodulation. Learn Mem 2010, 17:561-570.
95. Niedworok C.J., Schwarz I., Ledderose J., Giese G., Conzelmann K.K., Schwarz M.K. Charting monosynaptic connectivity maps by two-color light-sheet fluorescence microscopy. Cell Rep 2012, 2:1375-1386.
96. 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.
97. Castillo P.E., Carleton A., Vincent J.D., Lledo P.M. Multiple and opposing roles of cholinergic transmission in the main olfactory bulb. J Neurosci 1999, 19:9180-9191.
98. Rothermel M., Carey R.M., Puche A., Shipley M.T., Wachowiak M. Cholinergic inputs from Basal forebrain add an excitatory bias to odor coding in the olfactory bulb. J Neurosci 2014, 34:4654-4664.
99. 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.
100. Inagaki H.K., Ben-Tabou de-Leon S., Wong A.M., Jagadish S., Ishimoto H., Barnea G., et al. Visualizing neuromodulation in vivo: TANGO-mapping of dopamine signaling reveals appetite control of sugar sensing. Cell 2012, 148:583-595.
101. Bozza T., Vassalli A., Fuss S., Zhang J.J., Weiland B., Pacifico R., et al. Mapping of class I and class II odorant receptors to glomerular domains by two distinct types of olfactory sensory neurons in the mouse. Neuron 2009, 61:220-233.
102. Pacifico R., Dewan A., Cawley D., Guo C., Bozza T. An olfactory subsystem that mediates high-sensitivity detection of volatile amines. Cell Rep 2012, 2:76-88.
103. 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.
104. Ma L., Qiu Q., Gradwohl S., Scott A., Yu E.Q., Alexander R., et al. Distributed representation of chemical features and tunotopic organization of glomeruli in the mouse olfactory bulb. Proc Natl Acad Sci U S A 2012, 109:5481-5486.
105. Oka Y., Takai Y., Touhara K. Nasal airflow rate affects the sensitivity and pattern of glomerular odorant responses in the mouse olfactory bulb. J Neurosci 2009, 29:12070-12078.
106. 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.
107. Blauvelt D.G., Sato T.F., Wienisch M., Knopfel T., Murthy V.N. Distinct spatiotemporal activity in principal neurons of the mouse olfactory bulb in anesthetized and awake states. Front Neural Circuits 2013, 7:46.
108. Rinberg D., Koulakov A., Gelperin A. Sparse odor coding in awake behaving mice. J Neurosci 2006, 26:8857-8865.
109. 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.
110. Uchida N., Poo C., Haddad R. Coding and transformations in the olfactory system. Annu Rev Neurosci 2014, 37:363-385. 10.1146/annurev-neuro-071013-013941.
111. Spors H., Grinvald A. Spatio-temporal dynamics of odor representations in the mammalian olfactory bulb. Neuron 2002, 34:301-315.
112. 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.
113. Shusterman R., Smear M.C., Koulakov A.A., Rinberg D. Precise olfactory responses tile the sniff cycle. Nat Neurosci 2011, 14:1039-1044.
114. Cury K.M., Uchida N. Robust odor coding via inhalation-coupled transient activity in the mammalian olfactory bulb. Neuron 2010, 68:570-585.
115. Kepecs A., Uchida N., Mainen Z.F. The sniff as a unit of olfactory processing. Chem Senses 2006, 31:167-179.
116. Smear M., Shusterman R., O'Connor R., Bozza T., Rinberg D. Perception of sniff phase in mouse olfaction. Nature 2011, 479:397-400.
117. Smear M., Resulaj A., Zhang J., Bozza T., Rinberg D. Multiple perceptible signals from a single olfactory glomerulus. Nat Neurosci 2013, 16:1687-1691.
118. Buzsaki G., Draguhn A. Neuronal oscillations in cortical networks. Science 2004, 304:1926-1929.
119. Huxter J., Burgess N., O'Keefe J. Independent rate and temporal coding in hippocampal pyramidal cells. Nature 2003, 425:828-832.
120. Miura K., Mainen Z.F., Uchida N. Odor representations in olfactory cortex: distributed rate coding and decorrelated population activity. Neuron 2012, 74:1087-1098.
121. Niessing J., Friedrich R.W. Olfactory pattern classification by discrete neuronal network states. Nature 2010, 465:47-52.
122. Friedrich R.W. Neuronal computations in the olfactory system of zebrafish. Annu Rev Neurosci 2013, 36:383-402.
123. Uchida N., Mainen Z.F. Speed and accuracy of olfactory discrimination in the rat. Nat Neurosci 2003, 6:1224-1229.
124. 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.
125. 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.
126. Fukunaga I., Herb J.T., Kollo M., Boyden E.S., Schaefer A.T. Independent control of gamma and theta activity by distinct interneuron networks in the olfactory bulb. Nat Neurosci 2014, [Epub ahead of print]. 10.1038/nn.3760.
127. Lepousez G., Lledo P.M. Odor discrimination requires proper olfactory fast oscillations in awake mice. Neuron 2013, 80:1010-1024.
128. Igarashi K.M., Lu L., Colgin L.L., Moser M.B., Moser E.I. Coordination of entorhinal-hippocampal ensemble activity during associative learning. Nature 2014, 510:143-147. 10.1038/nature13162.
129. Kass M.D., Rosenthal M.C., Pottackal J., McGann J.P. Fear learning enhances neural responses to threat-predictive sensory stimuli. Science 2013, 342:1389-1392.
130. Mizrahi A., Katz L.C. Dendritic stability in the adult olfactory bulb. Nat Neurosci 2003, 6:1201-1207.
131. Mizrahi A., Lu J., Irving R., Feng G., Katz L.C. In vivo imaging of juxtaglomerular neuron turnover in the mouse olfactory bulb. Proc Natl Acad Sci U S A 2006, 103:1912-1917.
132. Mizrahi A. Dendritic development and plasticity of adult-born neurons in the mouse olfactory bulb. Nat Neurosci 2007, 10:444-452.
133. Lledo P.M., Alonso M., Grubb M.S. Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci 2006, 7:179-193.
134. Petreanu L., Alvarez-Buylla A. Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J Neurosci 2002, 22:6106-6113.
135. Yamaguchi M., Mori K. Critical period for sensory experience-dependent survival of newly generated granule cells in the adult mouse olfactory bulb. Proc Natl Acad Sci U S A 2005, 102:9697-9702.
136. Yokoyama T.K., Mochimaru D., Murata K., Manabe H., Kobayakawa K., Kobayakawa R., et al. Elimination of adult-born neurons in the olfactory bulb is promoted during the postprandial period. Neuron 2011, 71:883-897.
137. Yamaguchi M., Manabe H., Murata K., Mori K. Reorganization of neuronal circuits of the central olfactory system during postprandial sleep. Front Neural Circuits 2013, 7:132.
138. Manabe H., Kusumoto-Yoshida I., Ota M., Mori K. Olfactory cortex generates synchronized top-down inputs to the olfactory bulb during slow-wave sleep. J Neurosci 2011, 31:8123-8133.
139. Imayoshi I., Sakamoto M., Ohtsuka T., Takao K., Miyakawa T., Yamaguchi M., et al. Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci 2008, 11:1153-1161.
140. Sakamoto M., Imayoshi I., Ohtsuka T., Yamaguchi M., Mori K., Kageyama R. Continuous neurogenesis in the adult forebrain is required for innate olfactory responses. Proc Natl Acad Sci U S A 2011, 108:8479-8484.
141. Lazarini F., Lledo P.M. Is adult neurogenesis essential for olfaction. Trends Neurosci 2011, 34:20-30.