Two distinct olfactory bulb sublaminar networks involved in gamma and beta oscillation generation: A CSD study in the anesthetized rat

Frontiers in Neural Circuits

Volumn 8, Issue JULY, 2014, Pages

  Fourcaud Trocmé, Nicolas ^a,b   Courtiol, Emmanuelle ^a,b,c   Buonviso, Nathalie ^a,b  

^a LYON NEUROSCIENCE RESEARCH CENTER   (France)

^b UNIVERSITÉ LYON 1   (France)

^c NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Beta; Current source density; Gamma; Olfactory bulb; Oscillation; Rat

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BETA RHYTHM; DENDRITE; ELECTRIC POTENTIAL; GAMMA RHYTHM; GRANULE CELL; MALE; NONHUMAN; ODOR; OLFACTORY BULB; OLFACTORY NERVE; OLFACTORY SYSTEM; OSCILLATION; RAT; SENSORY STIMULATION; STIMULUS RESPONSE; SYNAPSE; ACTION POTENTIAL; ANIMAL; CYTOLOGY; DRUG EFFECTS; NERVE CELL; NERVE CELL NETWORK; PHYSIOLOGY; WISTAR RAT;

ANESTHETIC AGENT;

ACTION POTENTIALS; ANESTHETICS; ANIMALS; BETA RHYTHM; GAMMA RHYTHM; MALE; NERVE NET; NEURONS; ODORS; OLFACTORY BULB; OLFACTORY PATHWAYS; RATS; RATS, WISTAR;

EID: 84905182954     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2014.00088     Document Type: Article

References (51)

1. Bastos, A. M., Usrey, W. M., Adams, R. A., Mangun, G. R., Fries, P., and Friston, K. J. (2012). Canonical microcircuits for predictive coding. Neuron.76, 695-711. doi: 10.1016/j.neuron.2012.10.038
2. Bastos, A. M., Vezoli, J., Bosman, C. A., Schoffelen, J.-M., Oostenveld, R., Dowdall, J. R., et al. (2014). Visual areas exert feedforward and feedback influences through distinct frequency channels. bioRxiv Available online at:http://biorxiv.org/content/early/2014/05/06/004804 [Accessed May 21, 2014].
3. Beshel, J., Kopell, N., and Kay, L. M. (2007). Olfactory bulb gamma oscillations are enhanced with task demands. J. Neurosci.27, 8358-8365. doi: 10.1523/jneurosci.1199-07.2007
4. Bosman, C. A., Schoffelen, J.-M., Brunet, N., Oostenveld, R., Bastos, A. M., Womelsdorf, T., et al. (2012). Attentional stimulus selection through selective synchronization between monkey visual areas. Neuron.75, 875-888. doi: 10.1016/j.neuron.2012.06.037
5. Briffaud, V., Fourcaud-Trocmé, N., Messaoudi, B., Buonviso, N., and Amat, C. (2012). The relationship between respiration-related membrane potential slow oscillations and discharge patterns in mitral/tufted cells: what are the rules? PLoS One.7:e43964. doi: 10.1371/journal.pone.0043964
6. Buffalo, E. A., Fries, P., Landman, R., Buschman, T. J., and Desimone, R. (2011). Laminar differences in gamma and alpha coherence in the ventral stream. Proc. Natl. Acad. Sci. U S A.108, 11262-11267. doi: 10.1073/pnas.1011284108
7. Buonviso, N., Amat, C., and Litaudon, P. (2006). Respiratory modulation of olfactory neurons in the rodent brain. Chem. Senses.31, 145-154. doi: 10.1093/chemse/bjj010
8. 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
9. Cang, J., and Isaacson, J. S. (2003). In vivo whole-cell recording of odor-evoked synaptic transmission in the rat olfactory bulb. J. Neurosci.23, 4108-4116.
10. 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
11. Carleton, A., Petreanu, L. T., Lansford, R., Alvarez-Buylla, A., and Lledo, P.-M. (2003). Becoming a new neuron in the adult olfactory bulb. Nat. Neurosci.6, 507-518. doi: 10.1038/nn1048
12. Cenier, T., Amat, C., Litaudon, P., Garcia, S., Lafaye de Micheaux, P., Liquet, B., et al. (2008). 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. doi: 10.1111/j.1460-9568.2008.06123.x
13. 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
14. Courtiol, E., Amat, C., Thévenet, M., Messaoudi, B., Garcia, S., and Buonviso, N. (2011). Reshaping of bulbar odor response by nasal flow rate in the rat. PLoS One.6:e16445. doi: 10.1371/journal.pone.0016445
15. Ennis, M., Hamilton, K. A., and Hayar, A. (2007). "Neurochemistry of the main olfactory system, " in Handbook of Neurochemistry and Molecular Neurobiology. eds A. Lajtha, D. A. Johnson (US: Springer), 137-204. Available online at: http://link.springer.com.gate1.inist.fr/referenceworkentry/10.1007/978-0-387-30374-1_6 [Accessed May 15, 2014].
16. 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
17. Fourcaud-Trocmé, N., Courtiol, E., Buonviso, N., and Voegtlin, T. (2011). Stability of fast oscillations in the mammalian olfactory bulb: experiments and modeling. J. Physiol. Paris.105, 59-70. doi: 10.1016/j.jphysparis.2011.07.009
18. Freeman, W. J., and Schneider, W. (1982). Changes in spatial patterns of rabbit olfactory EEG with conditioning to odors. Psychophysiology.19, 44-56. doi: 10.1111/j.1469-8986.1982.tb02598.x
19. Gao, Y., and Strowbridge, B. W. (2009). Long-term plasticity of excitatory inputs to granule cells in the rat olfactory bulb. Nat. Neurosci.12, 731-733. doi: 10.1038/nn.2319
20. Garcia, S., and Fourcaud-Trocmé, N. (2009). OpenElectrophy: an electrophysiological data-and analysis-sharing framework. Front. Neuroinform.3:14. doi: 10.3389/neuro.11.014.2009
21. 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. doi: 10.1007/bf00247583
22. 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
23. Kay, L. M. (2014). Circuit oscillations in odor perception and memory. Prog. Brain Res.208, 223-251. doi: 10.1016/b978-0-444-63350-7.00009-7
24. Kay, L. M., and Beshel, J. (2010). A beta oscillation network in the rat olfactory system during a 2-alternative choice odor discrimination task. J. Neurophysiol.104, 829-839. doi: 10.1152/jn.00166.2010
25. Kepecs, A., Uchida, N., and Mainen, Z. F. (2006). The sniff as a unit of olfactory processing. Chem. Senses.31, 167-179. doi: 10.1093/chemse/bjj016
26. Kepecs, A., Uchida, N., and Mainen, Z. F. (2007). Rapid and precise control of sniffing during olfactory discrimination in rats. J. Neurophysiol.98, 205-213. doi: 10.1152/jn.00071.2007
27. Lagier, S., Carleton, A., and Lledo, P.-M. (2004). Interplay between local GABAergic interneurons and relay neurons generates gamma oscillations in the rat olfactory bulb. J. Neurosci.24, 4382-4392. doi: 10.1523/jneurosci.5570-03.2004
28. Lemasson, M., Saghatelyan, A., Olivo-Marin, J.-C., and Lledo, P.-M. (2005). Neonatal and adult neurogenesis provide two distinct populations of newborn neurons to the mouse olfactory bulb. J. Neurosci.25, 6816-6825. doi: 10.1523/jneurosci.1114-05.2005
29. Lepousez, G., and Lledo, P.-M. (2013). Odor discrimination requires proper olfactory fast oscillations in awake mice. Neuron.80, 1010-1024. doi: 10.1016/j.neuron.2013.07.025
30. Łeski, S., Lindén, H., Tetzlaff, T., Pettersen, K. H., and Einevoll, G. T. (2013). Frequency dependence of signal power and spatial reach of the local field potential. PLoS Comput. Biol.9:e1003137. doi: 10.1371/journal.pcbi.1003137
31. Maier, A., Adams, G. K., Aura, C., and Leopold, D. A. (2010). Distinct superficial and deep laminar domains of activity in the visual cortex during rest and stimulation. Front. Syst. Neurosci.4:31. doi: 10.3389/fnsys.2010.00031
32. 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
33. 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
34. Martin, C., Gervais, R., Messaoudi, B., and Ravel, N. (2006). Learning-induced oscillatory activities correlated to odour recognition: a network activity. Eur. J. Neurosci.23, 1801-1810. doi: 10.1111/j.1460-9568.2006.04711.x
35. Mitzdorf, U. (1985). Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol. Rev.65, 37-100.
36. Mouradian, L. E., and Scott, J. W. (1988). Cytochrome oxidase staining marks dendritic zones of the rat olfactory bulb external plexiform layer. J. Comp. Neurol.271, 507-518. doi: 10.1002/cne.902710404
37. Naritsuka, H., Sakai, K., Hashikawa, T., Mori, K., and Yamaguchi, M. (2009). Perisomatic-targeting granule cells in the mouse olfactory bulb. J. Comp. Neurol.515, 409-426. doi: 10.1002/cne.22063
38. Neville, K. R., and Haberly, L. B. (2003). Beta and gamma oscillations in the olfactory system of the urethane-anesthetized rat. J. Neurophysiol.90, 3921-3930. doi: 10.1152/jn.00475.2003
39. Nusser, Z., Kay, L. M., Laurent, G., Homanics, G. E., and Mody, I. (2001). Disruption of GABA(A) receptors on GABAergic interneurons leads to increased oscillatory power in the olfactory bulb network. J. Neurophysiol.86, 2823-2833.
40. Orona, E., Rainer, E. C., and Scott, J. W. (1984). Dendritic and axonal organization of mitral and tufted cells in the rat olfactory bulb. J. Comp. Neurol.226, 346-356. doi: 10.1002/cne.902260305
41. Orona, E., Scott, J. W., and Rainer, E. C. (1983). Different granule cell populations innervate superficial and deep regions of the external plexiform layer in rat olfactory bulb. J. Comp. Neurol.217, 227-237. doi: 10.1002/cne.902170209
42. Panzanelli, P., Perazzini, A.-Z., Fritschy, J.-M., and Sassoè-Pognetto, M. (2005). Heterogeneity of gamma-aminobutyric acid type A receptors in mitral and tufted cells of the rat main olfactory bulb. J. Comp. Neurol.484, 121-131. doi: 10.1002/cne.20440
43. Pettersen, K. H., Devor, A., Ulbert, I., Dale, A. M., and Einevoll, G. T. (2006). Current-source density estimation based on inversion of electrostatic forward solution: effects of finite extent of neuronal activity and conductivity discontinuities. J. Neurosci. Methods.154, 116-133. doi: 10.1016/j.jneumeth.2005.12.005
44. Rall, W., and Shepherd, G. M. (1968). Theoretical reconstruction of field potentials and dendrodendritic synaptic interactions in olfactory bulb. J. Neurophysiol.31, 884-915.
45. 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. doi: 10.1046/j.1460-9568.2003.02445.x
46. Roopun, A. K., Kramer, M. A., Carracedo, L. M., Kaiser, M., Davies, C. H., Traub, R. D., et al. (2008). Period concatenation underlies interactions between gamma and beta rhythms in neocortex. Front. Cell. Neurosci.2:1. doi: 10.3389/neuro.03.001.2008
47. Roux, S. G., Cenier, T., Garcia, S., Litaudon, P., and Buonviso, N. (2007). A wavelet-based method for local phase extraction from a multi-frequency oscillatory signal. J. Neurosci. Methods.160, 135-143. doi: 10.1016/j.jneumeth.2006.09.001
48. Sassoè-Pognetto, M., Panzanelli, P., Lagier, S., Fritschy, J.-M., and Lledo, P.-M. (2009). GABA receptor heterogeneity modulates dendrodendritic inhibition. Ann. N Y Acad. Sci.1170, 259-263. doi: 10.1111/j.1749-6632.2009.03882.x
49. Schaefer, A. T., and Margrie, T. W. (2007). Spatiotemporal representations in the olfactory system. Trends Neurosci.30, 92-100. doi: 10.1016/j.tins.2007.01.001
50. 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
51. Wellis, D. P., and Scott, J. W. (1990). Intracellular responses of identified rat olfactory bulb interneurons to electrical and odor stimulation. J. Neurophysiol.64, 932-947.