Anesthetic regimes modulate the temporal dynamics of local field potential in the mouse olfactory bulb

Journal of Neurophysiology

Volumn 111, Issue 5, 2014, Pages 908-917

  Chery, Romain ^a   Gurden, Hirac ^a   Martin, Claire ^a  

^a Centre National de la Recherche Scientifique   (France)

Author keywords

Ketamine; Medetomidine; Olfactory bulb; Oscillations; Xylazine

Indexed keywords

ANESTHETIC AGENT; KETAMINE; MEDETOMIDINE;

ANESTHESIA; ANIMAL EXPERIMENT; ARTICLE; BREATHING; CONTROLLED STUDY; DRUG BINDING; DYNAMICS; ELECTRIC POTENTIAL; ELECTRODE; GAMMA OSCILLATION; IMPLANTATION; INJECTION; INTRACELLULAR RECORDING; MALE; MOUSE; NONHUMAN; ODOR; OLFACTORY BULB; OLFACTORY SYSTEM; OSCILLATION; PRIORITY JOURNAL; RESPIRATORY BURST; WAKEFULNESS;

KETAMINE; MEDETOMIDINE; OLFACTORY BULB; OSCILLATIONS; XYLAZINE;

ADRENERGIC ALPHA-2 RECEPTOR AGONISTS; ANESTHETICS, DISSOCIATIVE; ANIMALS; BRAIN WAVES; ELECTROENCEPHALOGRAPHY; EXCITATORY AMINO ACID ANTAGONISTS; HYPNOTICS AND SEDATIVES; KETAMINE; MALE; MEDETOMIDINE; MICE; MICE, INBRED C57BL; ODORS; OLFACTORY BULB; SMELL; XYLAZINE;

EID: 84900791107     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00261.2013     Document Type: Article

References (62)

1. Aylwin ML, Aguilar GA, Flores FJ, Maldonado PE. Odorant modulation of neuronal activity and local field potential in sensory-deprived olfactory bulb. Neuroscience 162: 1265-1278, 2009.
2. Berridge CW, Waterhouse BD. The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res Brain Res Rev 42: 33-84, 2003.
3. Beshel J, Kopell N, Kay L. Olfactory bulb gamma oscillations are enhanced with task demands. J Neurosci 27: 8358-8365, 2007.
4. Buonviso N, Amat C, Litaudon P, Roux S, Royet JP, Farget V, Sicard G. Rhythm sequence through the olfactory bulb layers during the time window of a respiratory cycle. Eur J Neurosci 17: 1811-1819, 2003.
5. Carey RM, Wachowiak M. Effect of sniffing on the temporal structure of mitral/tufted cell output from the olfactory bulb. J Neurosci 31: 10615-10626, 2011.
6. Cenier T, Amat C, Litaudon P, Garcia S, Lafaye de Micheaux P, Liquet B, Roux S, Buonviso N. Odor vapor pressure and quality modulate local field potential oscillatory patterns in the olfactory bulb of the anesthetized rat. Eur J Neurosci 27: 1432-1440, 2008.
7. 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 29: 921-930, 2009.
8. Chapuis J, Garcia S, Messaoudi B, Thevenet M, Ferreira G, Gervais R, Ravel N. The way an odor is experienced during aversive conditioning determines the extent of the network recruited during retrieval: a multisite electrophysiological study in rats. J Neurosci 29: 10287-10298, 2009.
9. Chapuis J, Wilson DA. Bidirectional plasticity of cortical pattern recognition and behavioral sensory acuity. Nat Neurosci 15: 155-161, 2012.
10. Courtiol E, Amat C, Thévenet M, Messaoudi B, Garcia S, Buonviso N. Reshaping of bulbar odor response by nasal flow rate in the rat. PLoS One 6: e16445, 2011.
11. Davison IG, Katz LC. Sparse and selective odor coding by mitral/tufted neurons in the main olfactory bulb. J Neurosci 27: 2091-2101, 2007.
12. Economo MN, White JA. Membrane properties and the balance between excitation and inhibition control gamma-frequency oscillations arising from feedback inhibition. PLoS Comput Biol 8: e1002354, 2012.
13. Eeckman FH, Freeman WJ. Correlations between unit firing and EEG in the rat olfactory system. Brain Res 528: 238-244, 1990.
14. El-Etri MM, Ennis M, Griff ER, Shipley MT. Evidence for cholinergic regulation of basal norepinephrine release in the rat olfactory bulb. Neuroscience 93: 611-617, 1999.
15. Engel AK, Fries P, Singer W. Dynamic predictions: oscillations and synchrony in top-down processing. Nat Rev Neurosci 2: 704-716, 2001.
16. Ennis M, Hamilton KA, Hayar A. Neurochemistry of the main olfactory system. In: Handbook of Neurochemistry and Molecular Neurobiology, edited Lajtha A. New York: Springer, 2007.
17. Fletcher ML, Wilson DA. Olfactory bulb mitral-tufted cell plasticity: odorant- specific tuning reflects previous odorant exposure. J Neurosci 23: 6946-6955, 2003.
18. Fontanini A, Katz DB. Behavioral states, network states, and sensory response variability. J Neurophysiol 100: 1160-1168, 2008.
19. Fontanini A, Spano P, Bower J. Ketamine-xylazine-induced slow (>1.5 Hz) oscillations in the rat piriform (olfactory) cortex are functionally correlated with respiration. J Neurosci 23: 7993-8001, 2003.
20. Fourcaud-Trocmé N, Courtiol E, Buonviso N, Voegtlin T. Stability of fast oscillations in the mammalian olfactory bulb: experiments and modeling. J Physiol (Paris) 105: 59-70, 2011.
21. Fuentes RA, Aguilar MI, Aylwin ML, Maldonado PE. Neuronal activity of mitral-tufted cells in awake rats during passive and active odorant stimulation. J Neurophysiol 100: 422-430, 2008.
22. Fukunaga I, Berning M, Kollo M, Schmaltz A, Schaefer AT. Two distinct channels of olfactory bulb output. Neuron 75: 320-329, 2012.
23. Garcia S, Fourcaud-Trocmé N. OpenElectrophy: an electrophysiological data- and analysis-sharing framework. Front Neuroinform 3: 14, 2009.
24. Gray C, Skinner J. Centrifugal regulation of neuronal activity in the olfactory bulb of the waking rabbit as revealed by reversible cryogenic blockade. Exp Brain Res 69: 378-386, 1988.
25. Grosmaitre X, Santarelli LC, Tan J, Luo M, Ma M. Dual functions of mammalian olfactory sensory neurons as odor detectors and mechanical sensors. Nat Neurosci 10: 348-354, 2007.
26. Gurden H, Uchida N, Mainen Z. Sensory-evoked intrinsic optical signals in the olfactory bulb are coupled to glutamate release and uptake. Neuron 52: 335-345, 2006.
27. Hong LE, Summerfelt A, Buchanan RW, O'Donnell P, Thaker GK, Weiler MA, Lahti AC. Gamma and delta neural oscillations and association with clinical symptoms under subanesthetic ketamine. Neuropsychopharmacology 35: 632-640, 2010.
28. Joseph J, Dunn FA, Stopfer M. Spontaneous olfactory receptor neuron activity determines follower cell response properties. J Neurosci 32: 2900-2910, 2012.
29. Kay L, Beshel J, Brea J, Martin C, Rojas-Líbano D, Kopell N. Olfactory oscillations: the what, how and what for. Trends Neurosci 32: 207-214, 2009.
30. Kay LM. Two species of gamma oscillations in the olfactory bulb: dependence on behavioral state and synaptic interactions. J Integr Neurosci 2: 31-44, 2003.
31. Lazarewicz MT, Ehrlichman RS, Maxwell CR, Gandal MJ, Finkel LH, Siegel SJ. Ketamine modulates theta and gamma oscillations. J Cogn Neurosci 22: 1452-1464, 2010.
32. Lecoq J, Tiret P, Najac M, Shepherd GM, Greer CA, Charpak S. Odor-evoked oxygen consumption by action potential and synaptic transmission in the olfactory bulb. J Neurosci 29: 1424-1433, 2009.
33. Lepousez G, Mouret A, Loudes C, Epelbaum J, Viollet C. Somatostatin contributes to in vivo gamma oscillation modulation and odor discrimination in the olfactory bulb. J Neurosci 30: 870-875, 2010.
34. Li A, Gong L, Xu F. Brain-state-independent neural representation of peripheral stimulation in rat olfactory bulb. Proc Natl Acad Sci U S A 108: 5087-5092, 2011.
35. 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 51: 458-463, 2012.
36. Linster C, Nai Q, Ennis M. Nonlinear effects of noradrenergic modulation of olfactory bulb function in adult rodents. J Neurophysiol 105: 1432-1443, 2011.
37. Ma J, Leung LS. The supramammillo-septal-hippocampal pathway mediates sensorimotor gating impairment and hyperlocomotion induced by MK-801 and ketamine in rats. Psychopharmacology (Berl) 191: 961-974, 2007.
38. Manunta Y, Edeline JM. Noradrenergic induction of selective plasticity in the frequency tuning of auditory cortex neurons. J Neurophysiol 92: 1445-1463, 2004.
39. Martin C, Beshel J, Kay LM. An olfacto-hippocampal network is dynamically involved in odor-discrimination learning. J Neurophysiol 98: 2196-2205, 2007.
40. Martin C, Gervais R, Hugues E, Messaoudi B, Ravel N. Learning modulation of odor-induced oscillatory responses in the rat olfactory bulb: a correlate of odor recognition? J Neurosci 24: 389-397, 2004.
41. Martin C, Gervais R, Messaoudi B, Ravel N. Learning-induced oscillatory activities correlated to odour recognition: a network activity. Eur J Neurosci 23: 1801-1810, 2006.
42. Mouly AM, Elaagouby A, Ravel N. A study of the effects of noradrenaline in the rat olfactory bulb using evoked field potential response. Brain Res 681: 47-57, 1995.
43. Nai Q, Dong HW, Linster C, Ennis M. Activation of alpha1 and alpha2 noradrenergic receptors exert opposing effects on excitability of main olfactory bulb granule cells. Neuroscience 169: 882-892, 2010.
44. Neville KR, Haberly LB. Beta and gamma oscillations in the olfactory system of the urethane-anesthetized rat. J Neurophysiol 90: 3921-3930, 2003.
45. Nusser Z, Kay L, Laurent G, Homanics G, Mody I. Disruption of GABA(A) receptors on GABAergic interneurons leads to increased oscillatory power in the olfactory bulb network. J Neurophysiol 86: 2823-2833, 2001.
46. Pinault D. N-methyl-D-aspartate receptor antagonists ketamine and MK-801 induce wake-related aberrant gamma oscillations in the rat neocortex. Biol Psychiatry 63: 730-735, 2008.
47. Rall W, Shepherd G. Theoretical reconstruction of field potentials and dendrodendritic synaptic interactions in olfactory bulb. J Neurophysiol 31: 884-915, 1968.
48. Ravel N, Chabaud P, Martin C, Gaveau V, Hugues E, Tallon-Baudry C, Bertrand O, Gervais R. Olfactory learning modifies the expression of odour-induced oscillatory responses in the gamma (60-90 Hz) and beta (15-40 Hz) bands in the rat olfactory bulb. Eur J Neurosci 17: 350-358, 2003.
49. Rinberg D, Koulakov A, Gelperin A. Sparse odor coding in awake behaving mice. J Neurosci 26: 8857-8865, 2006.
50. Rojas-Líbano D, Kay L. Olfactory system gamma oscillations: the physiological dissection of a cognitive neural system. Cogn Neurodyn 2: 179-194, 2008.
51. Rosero MA, Aylwin ML. Sniffing shapes the dynamics of olfactory bulb gamma oscillations in awake behaving rats. Eur J Neurosci 34: 787-799, 2011.
52. Roughan JV, Ojeda OB, Flecknell PA. The influence of pre-anaesthetic administration of buprenorphine on the anaesthetic effects of ketamine/ medetomidine and pentobarbitone in rats and the consequences of repeated anaesthesia. Lab Anim 33: 234-242, 1999.
53. Roux S, Cenier T, Garcia S, Litaudon P, Buonviso N. A wavelet-based method for local phase extraction from a multi-frequency oscillatory signal. J Neurosci Methods 160: 135-143, 2007.
54. Rubin BD, Katz LC. Optical imaging of odorant representations in the mammalian olfactory bulb. Neuron 23: 499-511, 1999.
55. Schoppa N, Kinzie J, Sahara Y, Segerson T, Westbrook G. Dendrodendritic inhibition in the olfactory bulb is driven by NMDA receptors. J Neurosci 18: 6790-6802, 1998.
56. Soucy E, Albeanu D, Fantana A, Murthy V, Meister M. Precision and diversity in an odor map on the olfactory bulb. Nat Neurosci 12: 210-220, 2009.
57. Stakic J, Suchanek JM, Ziegler GP, Griff ER. The source of spontaneous activity in the main olfactory bulb of the rat. PLoS One 6: e23990, 2011.
58. Tallon-Baudry C, Bertrand O. Oscillatory gamma activity in humans and its role in object representation. Trends Cogn Sci 3: 151-162, 1999.
59. Trombley PQ, Shepherd GM. Noradrenergic inhibition of synaptic transmission between mitral and granule cells in mammalian olfactory bulb cultures. J Neurosci 12: 3985-3991, 1992.
60. Virtanen R. Pharmacological profiles of medetomidine and its antagonist, atipamezole. Acta Vet Scand Suppl 85: 29-37, 1989.
61. Wilson DA, Sullivan RM, Gall CM, Guthrie KM. NMDA-receptor modulation of lateral inhibition and c-fos expression in olfactory bulb. Brain Res 719: 62-71, 1996.
62. Wixon SK, Smiler KL. Anesthesia and analgesia in rodents. In: Anesthesia and Analgesia in Laboratory Animals, edited by Kohn DJ, White WJ, Benson GJ. London: Academic, 1997, p. 165.