Functional Properties of Cortical Feedback Projections to the Olfactory Bulb

Neuron

Volumn 76, Issue 6, 2012, Pages 1175-1188

  Markopoulos, Foivos ^a,b   Rokni, Dan ^a   Gire, David H ^a   Murthy, Venkatesh N ^a  

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CHANNELRHODOPSIN 2; RHODOPSIN; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; DENDRITIC SPINE; EXCITATORY POSTSYNAPTIC POTENTIAL; IN VIVO STUDY; MEMBRANE POTENTIAL; MITRAL CELL; NERVE FIBER; NONHUMAN; OLFACTORY BULB; OLFACTORY NUCLEUS; OPTOGENETICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SENSORY FEEDBACK; SYNAPSE; SYNAPTIC TRANSMISSION;

ANIMALS; AXONS; CEREBRAL CORTEX; EVOKED POTENTIALS; FEEDBACK, PHYSIOLOGICAL; INTERNEURONS; NERVE NET; OLFACTORY BULB; OLFACTORY PATHWAYS; OLFACTORY PERCEPTION; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; RATS, TRANSGENIC;

EID: 84871382462     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2012.10.028     Document Type: Article

References (73)

1. Albeanu D.F., Soucy E., Sato T.F., Meister M., Murthy V.N. LED arrays as cost effective and efficient light sources for widefield microscopy. PLoS ONE 2008, 3:e2146.
2. Balu R., Strowbridge B.W. Opposing inward and outward conductances regulate rebound discharges in olfactory mitral cells. J. Neurophysiol. 2007, 97:1959-1968.
3. Balu R., Pressler R.T., Strowbridge B.W. Multiple modes of synaptic excitation of olfactory bulb granule cells. J. Neurosci. 2007, 27:5621-5632.
4. Baluch F., Itti L. Mechanisms of top-down attention. Trends Neurosci. 2011, 34:210-224.
5. Bardy C., Alonso M., Bouthour W., Lledo P.M. How, when, and where new inhibitory neurons release neurotransmitters in the adult olfactory bulb. J. Neurosci. 2010, 30:17023-17034.
6. Boyd A.M., Sturgill J.F., Poo C., Isaacson J.S. Cortical feedback control of olfactory bulb circuits. Neuron 2012, 76:1161-1174. this issue.
7. Brunjes P.C., Illig K.R., Meyer E.A. A field guide to the anterior olfactory nucleus (cortex). Brain Res. Rev. 2005, 50:305-335.
8. Cardin J.A., Carlén M., Meletis K., Knoblich U., Zhang F., Deisseroth K., Tsai L.-H., Moore C.I. Targeted optogenetic stimulation and recording of neurons in vivo using cell-type-specific expression of Channelrhodopsin-2. Nat. Protoc. 2010, 5:247-254.
9. Carlson G.C., Shipley M.T., Keller A. Long-lasting depolarizations in mitral cells of the rat olfactory bulb. J. Neurosci. 2000, 20:2011-2021.
10. Christie J.M., Westbrook G.L. Lateral excitation within the olfactory bulb. J. Neurosci. 2006, 26:2269-2277.
11. Cury K.M., Uchida N. Robust odor coding via inhalation-coupled transient activity in the mammalian olfactory bulb. Neuron 2010, 68:570-585.
12. Davis B.J., Macrides F. The organization of centrifugal projections from the anterior olfactory nucleus, ventral hippocampal rudiment, and piriform cortex to the main olfactory bulb in the hamster: an autoradiographic study. J. Comp. Neurol. 1981, 203:475-493.
13. Davis B.J., Macrides F., Youngs W.M., Schneider S.P., Rosene D.L. Efferents and centrifugal afferents of the main and accessory olfactory bulbs in the hamster. Brain Res. Bull. 1978, 3:59-72.
14. Davison I.G., Ehlers M.D. Neural circuit mechanisms for pattern detection and feature combination in olfactory cortex. Neuron 2011, 70:82-94.
15. de Olmos J., Hardy H., Heimer L. The afferent connections of the main and the accessory olfactory bulb formations in the rat: an experimental HRP-study. J. Comp. Neurol. 1978, 181:213-244.
16. 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.
17. Deisseroth K. Optogenetics. Nat. Methods 2011, 8:26-29.
18. 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.
19. 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.
20. Egger V., Urban N.N. Dynamic connectivity in the mitral cell-granule cell microcircuit. Semin. Cell Dev. Biol. 2006, 17:424-432.
21. Fontanini A., Katz D.B. Behavioral modulation of gustatory cortical activity. Ann. N Y Acad. Sci. 2009, 1170:403-406.
22. Gire D.H., Schoppa N.E. Control of on/off glomerular signaling by a local GABAergic microcircuit in the olfactory bulb. J. Neurosci. 2009, 29:13454-13464.
23. Gire D.H., Franks K.M., Zak J.D., Tanaka K.F., Whitesell J.D., Mulligan A.A., Hen R., Schoppa N.E. Mitral cells in the olfactory bulb are mainly excited through a multistep signaling path. J. Neurosci. 2012, 32:2964-2975.
24. Hagiwara A., Pal S.K., Sato T.F., Wienisch M., Murthy V.N. Optophysiological analysis of associational circuits in the olfactory cortex. Front Neural Circuits 2012, 6:18.
25. Han X. Optogenetics in the nonhuman primate. Prog. Brain Res. 2012, 196:215-233.
26. Hayar A., Karnup S., Ennis M., Shipley M.T. External tufted cells: a major excitatory element that coordinates glomerular activity. J. Neurosci. 2004, 24:6676-6685.
27. Hurley L.M., Devilbiss D.M., Waterhouse B.D. A matter of focus: monoaminergic modulation of stimulus coding in mammalian sensory networks. Curr. Opin. Neurobiol. 2004, 14:488-495.
28. Illig K.R., Eudy J.D. Contralateral projections of the rat anterior olfactory nucleus. J. Comp. Neurol. 2009, 512:115-123.
29. Isaacson J.S. Odor representations in mammalian cortical circuits. Curr. Opin. Neurobiol. 2010, 20:328-331.
30. Isaacson J.S., Strowbridge B.W. Olfactory reciprocal synapses: dendritic signaling in the CNS. Neuron 1998, 20:749-761.
31. Isaacson J.S., Scanziani M. How inhibition shapes cortical activity. Neuron 2011, 72:231-243.
32. Kapoor V., Urban N.N. Glomerulus-specific, long-latency activity in the olfactory bulb granule cell network. J. Neurosci. 2006, 26:11709-11719.
33. Kashiwadani H., Sasaki Y.F., Uchida N., Mori K. Synchronized oscillatory discharges of mitral/tufted cells with different molecular receptive ranges in the rabbit olfactory bulb. J. Neurophysiol. 1999, 82:1786-1792.
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. Kikuta S., Kashiwadani H., Mori K. Compensatory rapid switching of binasal inputs in the olfactory cortex. J. Neurosci. 2008, 28:11989-11997.
36. 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. USA 2010, 107:12363-12368.
37. Kiselycznyk C.L., Zhang S., Linster C. Role of centrifugal projections to the olfactory bulb in olfactory processing. Learn. Mem. 2006, 13:575-579.
38. Knudsen E.I. Fundamental components of attention. Annu. Rev. Neurosci. 2007, 30:57-78.
39. Lei H., Mooney R., Katz L.C. Synaptic integration of olfactory information in mouse anterior olfactory nucleus. J. Neurosci. 2006, 26:12023-12032.
40. Luna V.M., Schoppa N.E. GABAergic circuits control input-spike coupling in the piriform cortex. J. Neurosci. 2008, 28:8851-8859.
41. Macrides F., Chorover S.L. Olfactory bulb units: activity correlated with inhalation cycles and odor quality. Science 1972, 175:84-87.
42. Matsutani S., Yamamoto N. Centrifugal innervation of the mammalian olfactory bulb. Anat. Sci. Int. 2008, 83:218-227.
43. Miesenböck G. The optogenetic catechism. Science 2009, 326:395-399.
44. 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.
45. 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.
46. Najac M., De Saint Jan D., Reguero L., Grandes P., Charpak S. Monosynaptic and polysynaptic feed-forward inputs to mitral cells from olfactory sensory neurons. J. Neurosci. 2011, 31:8722-8729.
47. Nicoll R.A., Jahr C.E. Self-excitation of olfactory bulb neurones. Nature 1982, 296:441-444.
48. Nissant A., Bardy C., Katagiri H., Murray K., Lledo P.M. Adult neurogenesis promotes synaptic plasticity in the olfactory bulb. Nat. Neurosci. 2009, 12:728-730.
49. Noudoost B., Chang M.H., Steinmetz N.A., Moore T. Top-down control of visual attention. Curr. Opin. Neurobiol. 2010, 20:183-190.
50. Orona E., Rainer E.C., Scott J.W. Dendritic and axonal organization of mitral and tufted cells in the rat olfactory bulb. J. Comp. Neurol. 1984, 226:346-356.
51. Petreanu L., Huber D., Sobczyk A., Svoboda K. Channelrhodopsin-2-assisted circuit mapping of long-range callosal projections. Nat. Neurosci. 2007, 10:663-668.
52. Petzold G.C., Hagiwara A., Murthy V.N. Serotonergic modulation of odor input to the mammalian olfactory bulb. Nat. Neurosci. 2009, 12:784-791.
53. Pimentel D.O., Margrie T.W. Glutamatergic transmission and plasticity between olfactory bulb mitral cells. J. Physiol. 2008, 586:2107-2119.
54. Pinching A.J., Powell T.P. The termination of centrifugal fibres in the glomerular layer of the olfactory bulb. J. Cell Sci. 1972, 10:621-635.
55. Pírez N., Wachowiak M. In vivo modulation of sensory input to the olfactory bulb by tonic and activity-dependent presynaptic inhibition of receptor neurons. J. Neurosci. 2008, 28:6360-6371.
56. Pouille F., Scanziani M. Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 2001, 293:1159-1163.
57. Powell T.P., Cowan W.M., Raisman G. The central olfactory connexions. J. Anat. 1965, 99:791-813.
58. Price J.L., Powell T.P. An experimental study of the origin and the course of the centrifugal fibres to the olfactory bulb in the rat. J. Anat. 1970, 107:215-237.
59. Rennaker R.L., Chen C.F., Ruyle A.M., Sloan A.M., Wilson D.A. Spatial and temporal distribution of odorant-evoked activity in the piriform cortex. J. Neurosci. 2007, 27:1534-1542.
60. Restrepo D., Doucette W., Whitesell J.D., McTavish T.S., Salcedo E. From the top down: flexible reading of a fragmented odor map. Trends Neurosci. 2009, 32:525-531.
61. Reyher C.K., Schwerdtfeger W.K., Baumgarten H.G. Interbulbar axonal collateralization and morphology of anterior olfactory nucleus neurons in the rat. Brain Res. Bull. 1988, 20:549-566.
62. Rinberg D., Koulakov A., Gelperin A. Sparse odor coding in awake behaving mice. J. Neurosci. 2006, 26:8857-8865.
63. Schneider S.P., Scott J.W. Orthodromic response properties of rat olfactory bulb mitral and tufted cells correlate with their projection patterns. J. Neurophysiol. 1983, 50:358-378.
64. 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.
65. Scott J.W., Ranier E.C., Pemberton J.L., Orona E., Mouradian L.E. Pattern of rat olfactory bulb mitral and tufted cell connections to the anterior olfactory nucleus pars externa. J. Comp. Neurol. 1985, 242:415-424.
66. Shao Z., Puche A.C., Kiyokage E., Szabo G., Shipley M.T. Two GABAergic intraglomerular circuits differentially regulate tonic and phasic presynaptic inhibition of olfactory nerve terminals. J. Neurophysiol. 2009, 101:1988-2001.
67. Shao Z., Puche A.C., Liu S., Shipley M.T. Intraglomerular inhibition shapes the strength and temporal structure of glomerular output. J. Neurophysiol. 2012, 108:782-793.
68. Shepherd G.M., Chen W.R., Greer C.A. Olfactory bulb. The Synaptic Organization of the Brain 2004, 165-216. Oxford University Press, New York. G.M. Shepherd (Ed.).
69. Shipley M.T., Adamek G.D. The connections of the mouse olfactory bulb: a study using orthograde and retrograde transport of wheat germ agglutinin conjugated to horseradish peroxidase. Brain Res. Bull. 1984, 12:669-688.
70. Shusterman R., Smear M.C., Koulakov A.A., Rinberg D. Precise olfactory responses tile the sniff cycle. Nat. Neurosci. 2011, 14:1039-1044.
71. Stettler D.D., Axel R. Representations of odor in the piriform cortex. Neuron 2009, 63:854-864.
72. Strowbridge B.W. Role of cortical feedback in regulating inhibitory microcircuits. Ann. N Y Acad. Sci. 2009, 1170:270-274.
73. Tyler W.J., Petzold G.C., Pal S.K., Murthy V.N. Experience-dependent modification of primary sensory synapses in the mammalian olfactory bulb. J. Neurosci. 2007, 27:9427-9438.