Odor Discrimination Requires Proper Olfactory Fast Oscillations in Awake Mice

Neuron

Volumn 80, Issue 4, 2013, Pages 1010-1024

  Lepousez, Gabriel ^a,b   Lledo, Pierre Marie ^a,b  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; CARBENOXOLONE; DIZOCILPINE; KAINIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PICROTOXIN;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CONTROLLED STUDY; IN VIVO STUDY; INTERNEURON; MITRAL CELL; MOUSE; NERVE CELL STIMULATION; NONHUMAN; OLFACTORY BULB; OLFACTORY DISCRIMINATION; OLFACTORY SYSTEM; OLFACTORY TRACT; OPTOGENETICS; OSCILLATION; PRIORITY JOURNAL; SENSITIVITY ANALYSIS; SENSORY STIMULATION;

ANIMALS; DISCRIMINATION (PSYCHOLOGY); ELECTROENCEPHALOGRAPHY; ELECTROENCEPHALOGRAPHY PHASE SYNCHRONIZATION; FOURIER ANALYSIS; GABA ANTAGONISTS; LEARNING; MICE; NEURONS; ODORS; OLFACTORY BULB; OPTOGENETICS; RECEPTORS, GABA-A; RECEPTORS, N-METHYL-D-ASPARTATE; SMELL; WAKEFULNESS;

EID: 84888046947     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.07.025     Document Type: Article

References (48)

1. Abraham N.M., Egger V., Shimshek D.R., Renden R., Fukunaga I., Sprengel R., Seeburg P.H., Klugmann M., Margrie T.W., Schaefer A.T., Kuner T. Synaptic inhibition in the olfactory bulb accelerates odor discrimination in mice. Neuron 2010, 65:399-411.
2. Akam T., Kullmann D.M. Oscillations and filtering networks support flexible routing of information. Neuron 2010, 67:308-320.
3. Aroniadou-Anderjaska V., Ennis M., Shipley M.T. Dendrodendritic recurrent excitation in mitral cells of the rat olfactory bulb. J.Neurophysiol. 1999, 82:489-494.
4. Bathellier B., Lagier S., Faure P., Lledo P.-M. Circuit properties generating γ oscillations in a network model of the olfactory bulb. J.Neurophysiol. 2006, 95:2678-2691.
5. Boyd A.M., Sturgill J.F., Poo C., Isaacson J.S. Cortical feedback control of olfactory bulb circuits. Neuron 2012, 76:1161-1174.
6. Brunel N., Wang X.-J. What determines the frequency of fast network oscillations with irregular neural discharges? I. Synaptic dynamics and excitation-inhibition balance. J.Neurophysiol. 2003, 90:415-430.
7. Buzsáki G., Wang X.-J. Mechanisms of γ oscillations. Annu. Rev. Neurosci. 2012, 35:203-225.
8. Cardin J.A., Carlén M., Meletis K., Knoblich U., Zhang F., Deisseroth K., Tsai L.-H., Moore C.I. Driving fast-spiking cells induces γ rhythm and controls sensory responses. Nature 2009, 459:663-667.
9. 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.
10. Eyre M.D., Antal M., Nusser Z. Distinct deep short-axon cell subtypes of the main olfactory bulb provide novel intrabulbar and extrabulbar GABAergic connections. J.Neurosci. 2008, 28:8217-8229.
11. Eyre M.D., Renzi M., Farrant M., Nusser Z. Setting the time course of inhibitory synaptic currents by mixing multiple GABA(A) receptor α subunit isoforms. J.Neurosci. 2012, 32:5853-5867.
12. Fries P., Reynolds J.H., Rorie A.E., Desimone R. Modulation of oscillatory neuronal synchronization by selective visual attention. Science 2001, 291:1560-1563.
13. Fukunaga I., Berning M., Kollo M., Schmaltz A., Schaefer A.T. Two distinct channels of olfactory bulb output. Neuron 2012, 75:320-329.
14. Greer C.A., Halász N. Plasticity of dendrodendritic microcircuits following mitral cell loss in the olfactory bulb of the murine mutant Purkinje cell degeneration. J.Comp. Neurol. 1987, 256:284-298.
15. Greer C.A., Shepherd G.M. Mitral cell degeneration and sensory function in the neurological mutant mouse Purkinje cell degeneration (PCD). Brain Res. 1982, 235:156-161.
16. Gschwend O., Beroud J., Carleton A. Encoding odorant identity by spiking packets of rate-invariant neurons in awake mice. PLoS ONE 2012, 7:e30155.
17. Isaacson J.S. Glutamate spillover mediates excitatory transmission in the rat olfactory bulb. Neuron 1999, 23:377-384.
18. Isaacson J.S., Strowbridge B.W. Olfactory reciprocal synapses: dendritic signaling in the CNS. Neuron 1998, 20:749-761.
19. Kay L.M. Two species of γ oscillations in the olfactory bulb: dependence on behavioral state and synaptic interactions. J.Integr. Neurosci. 2003, 2:31-44.
20. Kay L.M., Beshel J., Brea J., Martin C., Rojas-Líbano D., Kopell N. Olfactory oscillations: the what, how and what for. Trends Neurosci. 2009, 32:207-214.
21. Kopell N., Ermentrout G.B., Whittington M.A., Traub R.D. Γrhythms and β rhythms have different synchronization properties. Proc. Natl. Acad. Sci. USA 2000, 97:1867-1872.
22. Lagier S., Carleton A., Lledo P.-M. Interplay between local GABAergic interneurons and relay neurons generates γ oscillations in the rat olfactory bulb. J.Neurosci. 2004, 24:4382-4392.
23. Lagier S., Panzanelli P., Russo R.E., Nissant A., Bathellier B., Sassoè-Pognetto M., Fritschy J.-M., Lledo P.-M. GABAergic inhibition at dendrodendritic synapses tunes γ oscillations in the olfactory bulb. Proc. Natl. Acad. Sci. USA 2007, 104:7259-7264.
24. Li A., Zhang L., Liu M., Gong L., Liu Q., Xu F. Effects of different anesthetics on oscillations in the rat olfactory bulb. J.Am. Assoc. Lab. Anim. Sci. 2012, 51:458-463.
25. Lindén H., Tetzlaff T., Potjans T.C., Pettersen K.H., Grün S., Diesmann M., Einevoll G.T. Modeling the spatial reach of the LFP. Neuron 2011, 72:859-872.
26. Löw K., Crestani F., Keist R., Benke D., Brünig I., Benson J.A., Fritschy J.M., Rülicke T., Bluethmann H., Möhler H., Rudolph U. Molecular and neuronal substrate for the selective attenuation of anxiety. Science 2000, 290:131-134.
27. Lowe G. Inhibition of backpropagating action potentials in mitral cell secondary dendrites. J.Neurophysiol. 2002, 88:64-85.
28. Luna V.M., Schoppa N.E. GABAergic circuits control input-spike coupling in the piriform cortex. J.Neurosci. 2008, 28:8851-8859.
29. Margrie T.W., Schaefer A.T. Theta oscillation coupled spike latencies yield computational vigour in a mammalian sensory system. J.Physiol. 2003, 546:363-374.
30. Margrie T.W., Sakmann B., Urban N.N. 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 2001, 98:319-324.
31. 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.
32. Martin C., Gervais R., Messaoudi B., Ravel N. Learning-induced oscillatory activities correlated to odour recognition: a network activity. Eur. J. Neurosci. 2006, 23:1801-1810.
33. Neville K.R., Haberly L.B. Beta and gamma oscillations in the olfactory system of the urethane-anesthetized rat. J.Neurophysiol. 2003, 90:3921-3930.
34. Pallotto M., Nissant A., Fritschy J.-M., Rudolph U., Sassoè-Pognetto M., Panzanelli P., Lledo P.-M. Early formation of GABAergic synapses governs the development of adult-born neurons in the olfactory bulb. J.Neurosci. 2012, 32:9103-9115.
35. Panzanelli P., Perazzini A.-Z., Fritschy J.-M., Sassoè-Pognetto M. Heterogeneity of γ-aminobutyric acid type A receptors in mitral and tufted cells of the rat main olfactory bulb. J.Comp. Neurol. 2005, 484:121-131.
36. Poo C., Isaacson J.S. Odor representations in olfactory cortex: "sparse" coding, global inhibition, and oscillations. Neuron 2009, 62:850-861.
37. Reinhart R.M.G., Mathalon D.H., Roach B.J., Ford J.M. Relationships between pre-stimulus γ power and subsequent P300 and reaction time breakdown in schizophrenia. Int. J. Psychophysiol. 2011, 79:16-24.
38. Rinberg D., Koulakov A., Gelperin A. Sparse odor coding in awake behaving mice. J.Neurosci. 2006, 26:8857-8865.
39. Rudolph U., Crestani F., Benke D., Brünig I., Benson J.A., Fritschy J.M., Martin J.R., Bluethmann H., Möhler H. Benzodiazepine actions mediated by specific gamma-aminobutyric acid(A) receptor subtypes. Nature 1999, 401:796-800.
40. Salin P.A., Lledo P.M., Vincent J.D., Charpak S. Dendritic glutamate autoreceptors modulate signal processing in rat mitral cells. J.Neurophysiol. 2001, 85:1275-1282.
41. Schoppa N.E., Westbrook G.L. Glomerulus-specific synchronization of mitral cells in the olfactory bulb. Neuron 2001, 31:639-651.
42. Stopfer M., Bhagavan S., Smith B.H., Laurent G. Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 1997, 390:70-74.
43. Tan J., Savigner A., Ma M., Luo M. Odor information processing by the olfactory bulb analyzed in gene-targeted mice. Neuron 2010, 65:912-926.
44. Tikka S.K., Nizamie S.H., Das B., Katshu M.Z., Goyal N. Increased spontaneous γ power and synchrony in schizophrenia patients having higher minor physical anomalies. Psychiatry Res. 2012, 207:164-172.
45. Vincis R., Gschwend O., Bhaukaurally K., Beroud J., Carleton A. Dense representation of natural odorants in the mouse olfactory bulb. Nat. Neurosci. 2012, 15:537-539.
46. Wang X.-J. Neurophysiological and computational principles of cortical rhythms in cognition. Physiol. Rev. 2010, 90:1195-1268.
47. Whittington M.A., Cunningham M.O., LeBeau F.E.N., Racca C., Traub R.D. Multiple origins of the cortical γ rhythm. Dev. Neurobiol. 2011, 71:92-106.
48. Xiong W., Chen W.R. Dynamic gating of spike propagation in the mitral cell lateral dendrites. Neuron 2002, 34:115-126.