The olfactory bulb theta rhythm follows all frequencies of diaphragmatic respiration in the freely behaving rat

Frontiers in Behavioral Neuroscience

Volumn 8, Issue JUNE, 2014, Pages

  Rojas Líbano, Daniel ^a,b,c   Frederick, Donald E ^a,b   Egaña, José I ^c   Kay, Leslie M ^a,b  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c UNIVERSITY OF CHILE   (Chile)

Author keywords

Local field potential; Olfactory bulb; Rat; Respiration; Theta rhythm

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BREATHING PATTERN; BREATHING RATE; CONNECTOME; CONTROLLED STUDY; DIAPHRAGMATIC RESPIRATION; ELECTROMYOGRAM; LOCAL FIELD POTENTIAL; MALE; NERVOUS SYSTEM PARAMETERS; NEUROMODULATION; NEUROMONITORING; NONHUMAN; OLFACTORY BULB; OLFACTORY DISCRIMINATION; OLFACTORY SYSTEM; OSCILLATION; RAT; RELIABILITY; RESPIRATORY FUNCTION; RESPIRATORY TRACT PARAMETERS; SENSORIMOTOR FUNCTION; SENSORY CORTEX; SNIFF FREQUENCY; THETA RHYTHM;

EID: 84902281996     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2014.00214     Document Type: Article

References (51)

1. Adrian, E. D. (1950). The electrical activity of the mammalian olfactory bulb. EEG Clin. Neurophysiol. 2, 377-388.
2. Aylwin, M. L., Aguilar, G. A., Flores, F. J., and Maldonado, P. E. (2009). Odorant modulation of neuronal activity and local field potential in sensory-deprived olfactory bulb. Neuroscience. 162, 1265-1278. doi: 10.1016/j.neuroscience.2009.05.051
3. Buonviso, N., Amat, C., Litaudon, P., Roux, S., Royet, J. P., Farget, V., et al. (2003). Rhythm sequence through the olfactory bulb layers during the time window of a respiratory cycle. Eur. J. Neurosci. 17, 1811-1819. doi: 10.1046/j.1460-9568.2003.02619.x
4. Carey, R. M., Verhagen, J. V., Wesson, D. W., Pírez, N., and Wachowiak, M. (2009). Temporal structure of receptor neuron input to the olfactory bulb imaged in behaving rats. J. Neurophysiol. 101, 1073-1088. doi: 10.1152/jn.90902.2008
5. Carey, R. M., and Wachowiak, M. (2011). Effect of sniffing on the temporal structure of mitral/tufted cell output from the olfactory bulb. J. Neurosci. 31, 10615-10626. doi: 10.1523/JNEUROSCI.1805-11.2011
6. Cenier, T., David, F., Litaudon, P., Garcia, S., Amat, C., and Buonviso, N. (2009). Respiration-gated formation of gamma and beta neural assemblies in the mammalian olfactory bulb. Eur. J. Neurosci. 29, 921-930. doi: 10.1111/j.1460-9568.2009.06651.x
7. Courtiol, E., Amat, C., Thévenet, M., Messaoudi, B., Garcia, S., and Buonviso, N. (2011a). Reshaping of bulbar odor response by nasal flow rate in the rat. PLoS ONE 6:e16445. doi: 10.1371/journal.pone.0016445
8. Courtiol, E., Hegoburu, C., Litaudon, P., Garcia, S., Fourcaud-Trocmé, N., and Buonviso, N. (2011b). Individual and synergistic effects of sniffing frequency and flow rate on olfactory bulb activity. J. Neurophysiol. 106, 2813-2824. doi: 10.1152/jn.00672.2011
9. Cunliffe-Beamer, T. L. (1993). Applying principles of aseptic surgery to rodents. AWIC Newsl. 4, 3-6.
10. Diamond, M. E., von Heimendahl, M., Knutsen, P. M., Kleinfeld, D., and Ahissar, E. (2008). 'Where' and 'what' in the whisker sensorimotor system. Nat. Rev. Neurosci. 9, 601-612. doi: 10.1038/nrn2411
11. Domino, E. F., and Ueki, S. (1960). An analysis of the electrical burst phenomenon in some rhinencephalic structures of the dog and monkey. Electroencephalogr. Clin. Neurophysiol. 12, 635-648. doi: 10.1016/0013-4694(60)90107-3
12. Esclassan, F., Courtiol, E., Thévenet, M., Garcia, S., Buonviso, N., and Litaudon, P. (2012). Faster, deeper, better: the impact of sniffing modulation on bulbar olfactory processing. PLoS ONE 7:e40927. doi: 10.1371/journal.pone.0040927
13. Feldman, J. L., Del Negro, C. A., and Gray, P. A. (2013). Understanding the rhythm of breathing: so near, yet so far. Annu. Rev. Physiol. 75, 423-452. doi: 10.1146/annurev-physiol-040510-130049
14. Fontanini, A., Spano, P., and Bower, J. M. (2003). Ketamine-xylazine-induced slow (<1.5 Hz) oscillations in the rat piriform (olfactory) cortex are functionally correlated with respiration. J. Neurosci. 23, 7993-8001. doi: 10.1152/jn.01320.2004
15. Freeman, W. J. (1972). Depth recording of averaged evoked potential of olfactory bulb. J. Neurophysiol. 35, 780-796.
16. Freeman, W. J. (1975). Mass Action in the Nervous System. Academic Press.
17. Freeman, W. J. (1976). "Quantitative patterns of integrated neural activity, " in Simpler Networks and Behavior, ed. J. C. Fentress (Sunderland, MA: Sinauer Assoc.), 280-296.
18. Fukunaga, I., Berning, M., Kollo, M., Schmaltz, A., and Schaefer, A. T. (2012). Two distinct channels of olfactory bulb output. Neuron 75, 320-329. doi: 10.1016/j.neuron.2012.05.017
19. Gault, F. P., and Leaton, R. N. (1963). Electrical activity of the olfactory system. EEG Clin. Neurophysiol. 15:299-304.
20. Gray, C. M., and Skinner, J. E. (1988). 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.
21. Grosmaitre, X., Santarelli, L. C., Tan, J., Luo, M., and Ma, M. (2007). Dual functions of mammalian olfactory sensory neurons as odor detectors and mechanical sensors. Nat. Neurosci. 10, 348-354. doi: 10.1038/nn1856
22. Katz, R., Fink, B., and Ngai, S. (1962). Relationship between electrical activity of the diaphragm and ventilation. Proc. Soc. Exp. Biol. Med. 110, 792-794.
23. Kay, L. M. (2003). Two species of gamma oscillations in the olfactory bulb: dependence on behavioral state and synaptic interactions. J. Integr. Neurosci. 2, 31-44. doi: 10.1142/S0219635203000196
24. Kay, L. M. (2005). Theta oscillations and sensorimotor performance. Proc. Natl. Acad. Sci. USA. 102, 3863-3868. doi: 10.1073/pnas.0407920102
25. Kay, L. M., Lancaster, L. R., and Freeman, W. J. (1996). Reafference and attractors in the olfactory system during odor recognition. Int. J. Neural Syst. 7, 489-495.
26. Liversedge, S. P., and Findlay, J. M. (2000). Saccadic eye movements and cognition. Trends Cogn. Sci. 4, 6-14. doi: 10.1016/S1364-6613(99)01418-7
27. Lowry, C. A., and Kay, L. M. (2007). Chemical factors determine olfactory system beta oscillations in waking rats.J. Neurophysiol. 98, 394-404. doi: 10.1152/jn.00124.2007
28. Macrides, F., and Chorover, S. L. (1972). Olfactory bulb units: activity correlated with inhalation cycles and odor quality. Science 175, 84-87.
29. Macrides, F., Eichenbaum, H. B., and Forbes, W. B. (1982). Temporal relationship between sniffing and the limbic theta rhythm during odor discrimination reversal learning. J. Neurosci. 2, 1705-1717.
30. Manabe, H., and Mori, K. (2013). Sniff rhythm-paced fast and slow gamma-oscillations in the olfactory bulb: relation to tufted and mitral cells and behavioral states. J. Neurophysiol. 110, 1593-1599. doi: 10.1152/jn.00379.2013
31. Martin, C., Beshel, J., and Kay, L. M. (2007). An olfacto-hippocampal network is dynamically involved in odor-discrimination learning. J. Neurophysiol. 98, 2196-2205. doi: 10.1152/jn.00524.2007
32. Martin, C., Gervais, R., Hugues, E., Messaoudi, B., and Ravel, N. (2004). Learning modulation of odor-induced oscillatory responses in the rat olfactory bulb: a correlate of odor recognition? J. Neurosci. 24, 389-397. doi: 10.1523/JNEUROSCI.3433-03.2004
33. Mitchinson, B., Martin, C. J., Grant, R. A., and Prescott, T. J. (2007). Feedback control in active sensing: rat exploratory whisking is modulated by environmental contact. Proc. Biol. Sci. 274, 1035-1041. doi: 10.1098/rspb.2006.0347
34. Onoda, N., and Mori, K. (1980). Depth distribution of temporal firing patterns in olfactory bulb related to air-intake cycles. J. Neurophysiol. 44, 29-39.
35. Percival, D. B., and Walden, A. T. (1993). Spectral Analysis for Physical Applications: Multitaper and Conventional Univariate Techniques. Cambridge: Cambridge University Press.
36. Phillips, M. E., Sachdev, R. N., Willhite, D. C., and Shepherd, G. M. (2012). Respiration drives network activity and modulates synaptic and circuit processing of lateral inhibition in the olfactory bulb. J. Neurosci. 32, 85-98. doi: 10.1523/JNEUROSCI.4278-11.2012
37. Ravel, N., Caille, D., and Pager, J. (1987). A centrifugal respiratory modulation of olfactory bulb unit activity: a study on acute rat preparation. Exp. Brain Res. 65, 623-628.
38. Ravel, N., Chabaud, P., Martin, C., Gaveau, V., Hugues, E., Tallon-Baudry, C., et al. (2003). 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.
39. Rojas-Líbano, D., and Kay, L. M. (2008). Olfactory system gamma oscillations: the physiological dissection of a cognitive neural system. Cogn. Neurodyn. 2, 179-194. doi: 10.1007/s11571-008-9053-1
40. Rojas-Líbano, D., and Kay, L. M. (2012). Interplay between sniffing and odorant sorptive properties in the rat. J. Neurosci. 32, 15577-15589. doi: 10.1523/JNEUROSCI.1464-12.2012
41. Rosero, M. A., and Aylwin, M. L. (2011). Sniffing shapes the dynamics of olfactory bulb gamma oscillations in awake behaving rats. Eur. J. Neurosci. 34, 787-799. doi: 10.1111/j.1460-9568.2011.07800.x
42. Shafford, H. L., Strittmatter, R. R., and Schadt, J. C. (2006). A novel electrode design for chronic recording of electromyographic activity. J. Neurosci. Methods 156, 228-230. doi: 10.1016/j.jneumeth.2006.03.009
43. Slepian, D. (1978). Prolate spheroidal wave functions, Fourier analysis, and uncertainty V: the discrete case. Bell Syst. Tech. J. 57, 1371-1429.
44. Thomson, D. J. (1982). Spectrum estimation and harmonic analysis. Proc. IEEE 70, 1055-1096.
45. Thomson, D. J. (2001). "Multitaper analysis of nonstationary and nonlinear time series data, " in Nonlinear and Nonstationary Signal Processing, eds W. Fitzgerald, R. Smith, A. Walden, and P. Young (Cambridge: Cambridge University Press).
46. Tort, A. B., Komorowski, R., Eichenbaum, H., and Kopell, N. (2010). Measuring phase-amplitude coupling between neuronal oscillations of different frequencies. J. Neurophysiol. 104, 1195-1210. doi: 10.1152/jn.00106.2010
47. Tort, A. B., Komorowski, R. W., Manns, J. R., Kopell, N. J., and Eichenbaum, H. (2009). Theta-gamma coupling increases during the learning of item-context associations. Proc. Natl. Acad. Sci. U.S.A. 106, 20942-20947. doi: 10.1073/pnas.0911331106
48. Ueki, S., and Domino, E. F. (1961). Some evidence for a mechanical receptor in olfactory function. J. Neurophysiol. 24, 12-25.
49. Verhagen, J. V., Wesson, D. W., Netoff, T. I., White, J. A., and Wachowiak, M. (2007). Sniffing controls an adaptive filter of sensory input to the olfactory bulb. Nat. Neurosci. 10, 631-639. doi: 10.1038/nn1892
50. Wachowiak, M. (2011). All in a sniff: olfaction as a model for active sensing. Neuron 71, 962-973. doi: 10.1016/j.neuron.2011.08.030
51. Walsh, R. R. (1956). Single cell spike activity in the olfactory bulb. Am. J. Physiol. 186, 255-257.