The Relationship between Respiration-Related Membrane Potential Slow Oscillations and Discharge Patterns in Mitral/Tufted Cells: What Are the Rules?

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Briffaud, Virginie ^a   Fourcaud Trocmé, Nicolas ^a   Messaoudi, Belkacem ^a   Buonviso, Nathalie ^a   Amat, Corine ^a  

^a INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BREATHING; CELL STIMULATION; CELL SYNCHRONIZATION; CONTROLLED STUDY; EVOKED RESPONSE; MALE; MATHEMATICAL ANALYSIS; MEMBRANE POTENTIAL; MEMBRANE POTENTIAL SLOW OSCILLATION; MITRAL CELL; NONHUMAN; ODOR; OSCILLATION; RAT; SPIKE WAVE;

ANIMALS; INTRACELLULAR SPACE; KINETICS; MALE; MEMBRANE POTENTIALS; ODORS; OLFACTORY BULB; PERIODICITY; RATS; RATS, WISTAR; RESPIRATION;

RATTUS;

EID: 84865661733     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043964     Document Type: Article

References (48)

1. Lisman J, (2005) The theta/gamma discrete phase code occuring during the hippocampal phase precession may be a more general brain coding scheme. Hippocampus 15: 913-922.
2. Wang X, (2010) Neurophysiological and computational principles of cortical rhythms in cognition. Physiol Rev 90: 1195-1268.
3. Lisman J, Buzsáki G, (2008) A neural coding scheme formed by the combined function of gamma and theta oscillations. Schizophr Bull 34: 974-980.
4. Steriade M, (2006) Grouping of brain rhythms in corticothalamic systems. Neuroscience 137: 1087-1106.
5. Adrian ED, (1942) Olfactory reactions in the brain of the hedgehog. J Physiol 100: 459-473.
6. Freeman WJ, (1978) Spatial properties of an EEG event in the olfactory bulb and cortex. Electroencephalogr Clin Neurophysiol 44: 586-605.
7. Fontanini A, Spano P, Bower JM, (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.
8. Buonviso N, Amat C, Litaudon P, Roux S, Royet JP, et al. (2003) Rhythm sequence through the olfactory bulb layers during the time window of a respiratory cycle. Eur J Neurosci 17: 1811-1819.
9. Macrides F, Chorover SL, (1972) Olfactory bulb units: activity correlated with inhalation cycles and odor quality. Science 175: 84-87.
10. Onoda N, Mori K, (1980) Depth distribution of temporal firing patterns in olfactory bulb related to air-intake cycles. J Neurophysiol 44: 29-39.
11. Ravel N, Caille D, Pager J, (1987) A centrifugal respiratory modulation of olfactory bulb unit activity: a study on acute rat preparation. Exp Brain Res 65: 623-628.
12. Ravel N, Pager J, (1990) Respiratory patterning of the rat olfactory bulb unit activity: nasal versus tracheal breathing. Neurosci Lett 115: 213-218.
13. Chaput MA, Buonviso N, Berthommier F, (1992) Temporal patterns in spontaneous and odour-evoked mitral cell discharges recorded in anaesthetized freely breathing animals. Eur J Neurosci 4: 813-822.
14. Aylwin MDLL, Díaz E, Maldonado PE, (2005) Simultaneous single unit recording in the mitral cell layer of the rat olfactory bulb under nasal and tracheal breathing. Biol Res 38: 13-26.
15. Charpak S, Mertz J, Beaurepaire E, Moreaux L, Delaney K, (2001) Odor-evoked calcium signals in dendrites of rat mitral cells. Proc Natl Acad Sci U S A 98: 1230-1234.
16. Cang J, Isaacson JS, (2003) In vivo whole-cell recording of odor-evoked synaptic transmission in the rat olfactory bulb. J Neurosci 23: 4108-4116.
17. Lehmkuhle MJ, Normann RA, Maynard EM, (2006) Trial-by-trial discrimination of three enantiomer pairs by neural ensembles in mammalian olfactory bulb. J Neurophysiol 95: 1369-1379.
18. Bathellier B, Buhl DL, Accolla R, Carleton A, (2008) Dynamic ensemble odor coding in the mammalian olfactory bulb: sensory information at different timescales. Neuron 57: 586-598.
19. Cury KM, Uchida N, (2010) Robust odor coding via inhalation-coupled transient activity in the mammalian olfactory bulb. Neuron 68: 570-585.
20. Kepecs A, Uchida N, Mainen ZF, (2006) The sniff as a unit of olfactory processing. Chem Senses 31: 167-179.
21. Shusterman R, Smear MC, Koulakov AA, Rinberg D, (2011) Precise olfactory responses tile the sniff cycle. Nat Neurosci 14: 1039-1044.
22. Schaefer AT, Angelo K, Spors H, Margrie TW, (2006) Neuronal oscillations enhance stimulus discrimination by ensuring action potential precision. PLoS Biol 4: e163.
23. Litaudon P, Garcia S, Buonviso N, (2008) Strong coupling between pyramidal cell activity and network oscillations in the olfactory cortex. Neuroscience 156: 781-787.
24. Cenier T, David F, Litaudon P, Garcia S, Amat C, et al. (2009) Respiration-gated formation of gamma and beta neural assemblies in the mammalian olfactory bulb. Eur J Neurosci 29: 921-930.
25. Margrie TW, Schaefer AT, (2003) Theta oscillation coupled spike latencies yield computational vigour in a mammalian sensory system. J Physiol 546: 363-374.
26. Phillips ME, Sachdev RN, Willhite DC, Shepherd GM, (2012) Respiration drives network activity and modulates synaptic and circuit processing of lateral inhibition in the olfactory bulb. J Neurosci 32: 85-98.
27. Luo M, Katz LC, (2001) Response correlation maps of neurons in the mammalian olfactory bulb. Neuron 32: 1165-1179.
28. Courtiol E, Amat C, Thévenet M, Messaoudi B, Garcia S, et al. (2011) Reshaping of bulbar odor response by nasal flow rate in the rat. PLoS One 6: e16445.
29. Grosmaitre X, Santarelli LC, Tan J, Luo M, Ma M, (2007) Dual functions of mammalian olfactory sensory neurons as odor detectors and mechanical sensors. Nat Neurosci 10: 348-354.
30. Sobel EC, Tank DW, (1993) Timing of odor stimulation does not alter patterning of olfactory bulb unit activity in freely breathing rats. J Neurophysiol 69: 1331-1337.
31. Carey RM, Wachowiak M, (2011) Effect of sniffing on the temporal structure of mitral/tufted cell output from the olfactory bulb. J Neurosci 31: 10615-10626.
32. Yuan Q, Knöpfel T, (2006) Olfactory nerve stimulation-evoked mGluR1 slow potentials, oscillations, and calcium signaling in mouse olfactory bulb mitral cells. J Neurophysiol 95: 3097-3104.
33. Balu R, Strowbridge BW, (2007) Opposing inward and outward conductances regulate rebound discharges in olfactory mitral cells. J Neurophysiol 97: 1959-1968.
34. Johnston J, Delaney KR, (2010) Synaptic activation of T-type Ca2+ channels via mGluR activation in the primary dendrite of mitral cells. J Neurophysiol 103: 2557-2569.
35. Balu R, Larimer P, Strowbridge BW, (2004) Phasic stimuli evoke precisely timed spikes in intermittently discharging mitral cells. J Neurophysiol 92: 743-753.
36. Carlson GC, Shipley MT, Keller A, (2000) Long-lasting depolarizations in mitral cells of the rat olfactory bulb. J Neurosci 20: 2011-2021.
37. Schoppa NE, Westbrook GL, (2001) Glomerulus-specific synchronization of mitral cells in the olfactory bulb. Neuron 31: 639-651.
38. Chaput MA, (2000) EOG responses in anesthetized freely breathing rats. Chem Senses 25: 695-701.
39. Padmanabhan K, Urban NN, (2010) Intrinsic biophysical diversity decorrelates neuronal firing while increasing information content. Nat Neurosci 13: 1276-1282.
40. Debarbieux F, Audinat E, Charpak S, (2003) Action potential propagation in dendrites of rat mitral cells in vivo. J Neurosci 23: 5553-5560.
41. Egger V, (2008) Synaptic sodium spikes trigger long-lasting depolarizations and slow calcium entry in rat olfactory bulb granule cells. Eur J Neurosci 27: 2066-2075.
42. Yokoi M, Mori K, Nakanishi S, (1995) Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proc Natl Acad Sci U S A 92: 3371-3375.
43. Ennis M, Hamilton K, Hayar A (2007) Neurochemistry of the main olfactory system. In: Lajtha A, editor-in-chief. Handbook of neurochemistry and molecular neurobiology. Heidelberg: Springer. 137-204.
44. Roux SG, Garcia S, Bertrand B, Cenier T, Vigouroux M, et al. (2006) Respiratory cycle as time basis: an improved method for averaging olfactory neural events. J Neurosci Methods 152: 173-178.
45. Garcia S, Fourcaud-Trocmé N, (2009) Openelectrophy: an electrophysiological data- and analysis-sharing framework. Front Neuroinform 3: 14.
46. Wellis DP, Scott JW, (1990) Intracellular responses of identified rat olfactory bulb interneurons to electrical and odor stimulation. J Neurophysiol 64: 932-947.
47. Migliore M, Shepherd GM, (2008) Dendritic action potentials connect distributed dendrodendritic microcircuits. J Comput Neurosci 24: 207-221.
48. Tuckwell HC (1988) Introduction to Theoretical Neurobiology, Cambridge: Cambridge University Press.