Sparse Distributed Representation of Odors in a Large-scale Olfactory Bulb Circuit

PLoS Computational Biology

Volumn 9, Issue 3, 2013, Pages

  Yu, Yuguo ^a,b   McTavish, Thomas S ^b   Hines, Michael L ^b   Shepherd, Gordon M ^b   Valenti, Cesare ^c   Migliore, Michele ^b,d  

^a FUDAN UNIVERSITY   (China)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PALERMO   (Italy)

^d CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; CYTOLOGY; GRANULATION; TIMING CIRCUITS;

'CURRENT; CELL NETWORK; CRITICAL STEPS; DISTRIBUTED REPRESENTATION; EXPERIMENTAL TECHNIQUES; GRANULE CELLS; LARGE-SCALES; LATERAL INHIBITION; OLFACTORY BULBS; SPIKING PATTERNS;

ODORS;

ARTICLE; ARTIFICIAL NEURAL NETWORK; CELL ACTIVATION; CELL INTERACTION; CELL NETWORK SELF ORGANIZATION; CELLULAR PARAMETERS; CONNECTOME; CONTROLLED STUDY; DENDRODENDRITIC SYNAPSE; EXCITATORY POSTSYNAPTIC POTENTIAL; GRANULE CELL; IMAGE RECONSTRUCTION; INHIBITORY POSTSYNAPTIC POTENTIAL; LARGE SCALE PRODUCTION; LATERAL INHIBITION; MITRAL CELL; MOLECULAR DYNAMICS; NEGATIVE FEEDBACK; NERVE CELL INHIBITION; NERVE CELL PLASTICITY; NEUROMODULATION; OLFACTORY BULB; OLFACTORY DISCRIMINATION; OSCILLATION; POSITIVE FEEDBACK; SENSORY STIMULATION; SYNAPSE; THREE DIMENSIONAL IMAGING;

EID: 84876010321     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003014     Document Type: Article

References (83)

1. Hartline HK, Wagner HG, Ratliff F, (1956) Inhibition in the eye of Limulus. J Gen Physiol 39: 651-73.
2. Smear M, Shusterman R, O'Connor R, Bozza T, Rinberg D, (2011) Perception of sniff phase in mouse olfaction. Nature 479: 397-400.
3. Kuffler SW, (1953) Discharge patterns and functional organization of mammalian retina. J Neurophysiol 16: 37-68.
4. Oswald AM, Schiff ML, Reyes AD, (2006) Synaptic mechanisms underlying auditory processing. Curr Opin Neurobiol 16: 371-6.
5. Fuchs JL, Brown PB, (1984) Two-point discriminability: Relation to properties of the somatosensory system. Somatosensory Research 2: 163-169.
6. Rall W, Shepherd GM, (1968) Theoretical reconstruction of field potentials and dendrodendritic synaptic interactions in olfactory bulb. J Neurophysiol 31: 884-915.
7. Yokoi M, Mori K, Nakanishi S, (1995) Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proc Natl Acad Sci USA 92: 3371-5.
8. Pinching AJ, (1970) Synaptic connexions in the glomerular layer of the olfactory bulb. J Physiol 210: 14P-15P.
9. Egger V, Urban NN, (2006) Dynamic connectivity in the mitral cell-granule cell microcircuit Semin. Cell Dev Biol 17: 424-32.
10. Willhite DC, Nguyen KT, Masurkar AV, Greer CA, Shepherd GM, et al. (2006) Viral tracing identifies distributed columnar organization in the olfactory bulb. Proc Nat Acad Sci USA 103: 12592-12597.
11. Jia C, Chen WR, Shepherd GM, (1999) Synaptic organization and neurotransmitters in the rat accessory olfactory bulb. J Neurophysiol 81: 345-55.
12. Tan J, Savigner A, Ma M, Luo M, (2010) Odor information processing by the olfactory bulb analyzed in gene-targeted mice. Neuron 65: 912-26.
13. Nikonov AA, Caprio J, (2005) Processing of odor information in the olfactory bulb and cerebral lobes. Chem Senses 30 Suppl 1: i317-8.
14. Mori K, Nagao H, Yoshihara Y, (1999) The olfactory bulb: coding and processing of odor molecule information. Science 286: 711-5.
15. Mori K, Takahashi YK, Igarashi KM, Yamaguchi M, (2006) Maps of odorant molecular features in the Mammalian olfactory bulb. Physiol Rev 86: 409-33.
16. Shusterman R, Smear MC, Koulakov AA, Rinberg D, (2011) Precise olfactory responses tile the sniff cycle. Nat Neurosci 14: 1039-44.
17. Kim DH, Phillips ME, Chang AY, Patel HK, Nguyen KT, et al. (2011) Lateral Connectivity in the Olfactory Bulb is Sparse and Segregated. Front Neural Circuits 5: 5.
18. Migliore M, Hines ML, McTavish TS, Shepherd GM, (2010) Functional roles of distributed synaptic clusters in the mitral-granule cell network of the olfactory bulb. Front Integr Neurosci 4: 122.
19. Stewart WB, Kauer JS, Shepherd GM, (1979) Functional organization of rat olfactory bulb analysed by the 2-deoxyglucose method. J Comp Neurol 185: 715-34.
20. Xu F, Liu N, Kida I, Rothman DL, Hyder F, et al. (2003) Odor maps of aldehydes and esters revealed by functional MRI in the glomerular layer of the mouse olfactory bulb. Proc Natl Acad Sci USA 100: 11029-34.
21. Linster C, Cleland TA, (2009) Glomerular microcircuits in the olfactory bulb. Neur Netw 22: 1169-1173.
22. Royet JP, Distel H, Hudson R, Gervais R, (1998) A re-estimation of the number of glomeruli and mitral cells in the olfactory bulb of rabbit. Brain Res 788: 35-42.
23. Shepherd GM, Chen WR, Greer CA (1998) Olfactory bulb. In: G.MShepherd, editors. The Synaptic Organization of the Brain. New York, USA: Oxford University Press). pp. 159-204.
24. Migliore M, Shepherd GM, (2008) Dendritic action potentials connect distributed dendrodendritic microcircuits. J Comput Neurosci 24: 207-221.
25. Xiong W, Chen WR, (2002) Dynamic gating of spike propagation in the mitral cell lateral dendrites. Neuron 34: 115-26.
26. Mandairon N, Linster C, (2009) Odor perception and olfactory bulb plasticity in adult mammals. J Neurophysiol 101: 2204-9.
27. Otsuka T, Kawaguchi Y, (2009) Cortical inhibitory cell types differentially form intralaminar and interlaminar subnetworks with excitatory neurons. J Neurosci 29: 10533-40.
28. Migliore M, Inzirillo C, Shepherd GM, (2007) Learning mechanism for column formation in the olfactory bulb. Front Integr Neurosci 1: 12.
29. Nawroth JC, Greer CA, Chen WR, Laughlin SB, Shepherd GM, (2007) An energy budget for the olfactory glomerulus. J Neurosci 27: 9790-800.
30. McTavish TS, Migliore M, Shepherd GM, Hines ML, (2012) Mitral cell spike synchrony modulated by dendrodendritic synapse location. Front Comput Neurosci 6: 3.
31. Junek S, Kludt E, Wolf F, Schild D, (2010) Olfactory coding with patterns of response latencies. Neuron 67: 872-84.
32. Kapoor V, Urban NN, (2006) Glomerulus-specific, long-latency activity in the olfactory bulb granule cell network. J Neurosci 26: 11709-19.
33. Guthrie KM, Anderson AJ, Leon M, Gall C, (1993) Odor-induced increases in c-fos mRNA expression reveal an anatomical "unit" for odor processing in olfactory bulb. Proc Natl Acad Sci USA 90: 3329-33.
34. Lowe G, (2002) Inhibition of backpropagating action potentials in mitral cell secondary dendrites. J Neurophysiol 88: 64-85.
35. Mori K, Nowycky MC, Shepherd GM, (1981) Analysis of a long-duration inhibitory potential in mitral cells in the isolated turtle olfactory bulb. J Physiol 314: 311-20.
36. Wilson DA, Sullivan RM, Gall CM, Guthrie KM, (1996) NMDA-receptor modulation of lateral inhibition and c-fos expression in olfactory bulb. Brain Res 719: 62-71.
37. Christie JM, Schoppa NE, Westbrook GL, (2001) Tufted cell dendrodendritic inhibition in the olfactory bulb is dependent on NMDA receptor activity. J Neurophysiol 85: 169-73.
38. Egger V, Svoboda K, Mainen ZF, (2003) Mechanisms of lateral inhibition in the olfactory bulb: efficiency and modulation of spike-evoked calcium influx into granule cells. J Neurosci 23: 7551-8.
39. David F, Linster C, Cleland TA, (2008) Lateral dendritic shunt inhibition can regularize mitral cell spike patterning. J Comput Neurosci 25: 25-38.
40. Fantana AL, Soucy ER, Meister M, (2008) Rat olfactory bulb mitral cells receive sparse glomerular inputs. Neuron 59: 802-14.
41. Giridhar S, Doiron B, Urban NN, (2011) Timescale-dependent shaping of correlation by olfactory bulb lateral inhibition. Proc Natl Acad Sci USA 108: 5843-8.
42. Davison AP, Feng J, Brown D, (2003) Dendrodendritic inhibition and simulated odor responses in a detailed olfactory bulb network model. J Neurophysiol 90: 1921-35.
43. Arevian AC, Kapoor V, Urban NN, (2008) Activity-dependent gating of lateral nhibition in the mouse olfactory bulb. Nat Neurosci 11: 80-7.
44. Chow SF, Wick SD, Riecke H, (2012) Neurogenesis drives stimulus decorrelation in a model of the olfactory bulb. PLoS Comput Biol 8: e1002398.
45. Nissant A, Bardy C, Katagiri H, Murray K, Lledo PM, (2009) Adult neurogenesis promotes synaptic plasticity in the olfactory bulb. Nat Neurosci 12: 728-730.
46. Phillips CG, Powell TPS, Shepherd GM, (1963) Responses of mitral cells to stimulation of the lateral olfactory tract in the rabbit. J Physiol 168: 65-88.
47. Margrie TW, Sakmann B, Urban NN, (2001) Action potential propagation in mitral cell lateral dendrites is decremental and controls recurrent and lateral inhibition in the mammalian olfactory bulb. Proc Natl Acad Sci USA 98: 319-24.
48. Vincis R, Gschwend O, Bhaukaurally K, Beroud J, Carleton A, (2012) Dense representation of natural odorants in the mouse olfactory bulb. Nat Neurosci 15: 537-9.
49. Koulakov AA, Rinberg D, (2011) Sparse incomplete representations: a potential role of olfactory granule cells. Neuron 72: 124-36.
50. Dhawale AK, Hagiwara A, Bhalla US, Murthy VN, Albeanu DF, (2010) Non-redundant odor coding by sister mitral cells revealed by light addressable glomeruli in the mouse. Nat Neurosci 13: 1404-12.
51. Gschwend O, Beroud J, Carleton A, (2012) Encoding odorant identity by spiking packets of rate-invariant neurons in awake mice. PLoS One 7: e30155.
52. Carey RM, Wachowiak M, (2011) Effect of sniffing on the temporal structure of mitral/tufted cell output from the olfactory bulb. J Neurosci 31: 10615-26.
53. Kato Hiroyuki K, Chu Monica W, Isaacson Jeffry S, Komiyama T, (2012) Dynamic Sensory Representations in the Olfactory Bulb: Modulation by Wakefulness and Experience. Neuron 76: 962-975.
54. Kepecs A, Uchida N, Mainen ZF, (2007) Rapid and precise control of sniffing during olfactory discrimination in rats. J Neurophysiol 98: 205-213.
55. Luo SX, Axel R, Abbott LF, (2010) Generating sparse and selective third-order responses in the olfactory system of the fly. Proc Natl Acad Sci USA 107: 10713-8.
56. Assisi C, Stopfer M, Laurent G, Bazhenov M, (2007) Adaptive regulation of sparseness by feedforward inhibition. Nat Neurosci 10: 1176-84.
57. Olsen SR, Bhandawat V, Wilson RI, (2010) Divisive normalization in olfactory population codes. Neuron 66: 287-99.
58. Ennis M, Linster C, Aroniadou-Anderjaska V, Ciombor K, Shipley MT, (1998) Glutamate and synaptic plasticity at mammalian primary olfactory synapses. Ann N Y Acad Sci 855: 457-66.
59. Ma TF, Zhao XL, Cai L, Zhang N, Ren SQ, et al. (2012) Regulation of spike timing-dependent plasticity of olfactory inputs in mitral cells in the rat olfactory bulb. PLoS One 7: e35001.
60. Gao Y, Strowbridge BW, (2009) Long-term plasticity of excitatory inputs to granule cells in the rat olfactory bulb. Nat Neurosci 12: 731-3.
61. Patneau DK, Stripling JS, (1992) Functional correlates of selective long-term potentiation in the olfactory cortex and olfactory bulb. Brain Res 585: 219-28.
62. Arenkiel BR, Hasegawa H, Yi JJ, Larsen RS, Wallace ML, et al. (2011) Activity-induced remodeling of olfactory bulb microcircuits revealed by monosynaptic tracing. PLoS One 6: e29423.
63. Shepherd GM, Chen WR, Willhite D, Migliore M, Greer CA, (2007) The olfactory granule cell: from classical enigma to central role in olfactory processing. Brain Res Rev 55: 373-82.
64. Migliore M, Hines ML, Shepherd GM, (2005) The role of distal dendritic gap junctions in synchronization of mitral cell axonal output,. J Comput Neurosci 18: 151-161.
65. Bischofberger J, Jonas P, (1997) Action potential propagation into the presynaptic dendrites of rat mitral cells. J Physiol 504: 359-365.
66. Migliore M, Hoffman DA, Magee JC, Johnston D, (1999) Role of an A-type K+ conductance in the back-propagation of action potentials in the dendrites of hippocampal pyramidal neurons. J Comput Neurosci 7: 5-16.
67. Wang XY, McKenzie JS, Kemm RE, (1996) Whole-cell K+ currents in identified olfactory bulb output neurones of rats. J Physiol 490: 63-77.
68. Debarbieux F, Audinat E, Charpak S, (2003) Action potential propagation in dendrites of rat mitral cells in vivo. J Neurosci 23: 5553-60.
69. Chen WR, Shen GY, Shepherd GM, Hines ML, Midtgaard J, (2002) Multiple modes of action potential initiation and propagation in mitral cell primary dendrite. J Neurophysiol 88: 2755-64.
70. Schoppa NE, Westbrook GL, (1999) Regulation of synaptic timing in the olfactory bulb by an A-type potassium current. Nat Neurosci 2: 1106-13.
71. Pinato G, Midtgaard J, (2004) Dendritic sodium spikelets and low-threshold calcium spikes in turtle olfactory bulb granule cells. J Neurophysiol 93: 1285-94.
72. Zelles Y, Boyd JD, Hardy AB, Delaney KR, (2006) Branch-specific Ca2+ influx from Na+-dependent dendritic spikes in olfactory granule cells. J Neurosci 26: 30-40.
73. Wellis DP, Kauer JS, (1994) GABAergic and glutamatergic synaptic input to identified granule cells in salamander olfactory bulb. J Physiol 475: 419-30.
74. Cang J, Isaacson JS, (2003) In vivo whole-cell recording of odor-evoked synaptic transmission in the rat olfactory bulb. J Neurosci 23: 4108-16.
75. Destexhe A, Mainen ZF, Sejnowski TJ, (1994) An efficient method for computing synaptic conductances based on a kinetic model of receptor binding. Neural Comp 6: 10-14.
76. Jahr CE, Stevens CF, (1990) A quantitative description of NMDA receptor-channel kinetic behavior. J Neurosci 10: 1830-7.
77. Jahr CE, Stevens CF, (1990b) Voltage dependence of NMDA-activated macroscopic conductances predicted by single-channel kinetics. J Neurosci 10: 3178-82.
78. Schoppa NE, Kinzie JM, Sahara Y, Segerson TP, Westbrook GL, (1998) Dendrodendritic inhibition in the olfactory bulb is driven by NMDA receptors. J Neurosci 18: 6790-802.
79. Isaacson JS, (2001) Mechanisms governing dendritic gamma-aminobutyric acid (GABA) release in the rat olfactory bulb. Proc Natl Acad Sci USA 98: 337-42.
80. Bienenstock EL, Cooper LN, Munro PW, (1982) Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci 2: 32-48.
81. Stanton PK, (1996) LTD, LTP, and the sliding threshold for long-term synaptic plasticity. Hippocampus 6: 35-42.
82. Haykin S (1994) Neural Networks: A Comprehensive Foundation. New York: Macmillan Publishing.
83. Hines M, Carnevale NT, (1997) The NEURON simulation environment. Neural Comp 9: 1179-1209.