Odor representations in the olfactory bulb evolve after the first breath and persist as an odor afterimage

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 35, 2013, Pages

  Patterson, Michael Andrew ^a   Lagier, Samuel ^a   Carleton, Alan ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

Multielectrode recording; Network dynamics; Optogenetics

Indexed keywords

AFTERIMAGE; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; MITRAL CELL; MOUSE; NONHUMAN; ODOR; ODOR AFTERIMAGE; OLFACTORY BULB; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; SNIFFING; SPIKE; ACTION POTENTIAL; ANIMAL; BREATHING; C57BL MOUSE; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; MICE; MICE, INBRED C57BL; ODORS; OLFACTORY BULB; RESPIRATION;

EID: 84883430541     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1303873110     Document Type: Article

References (65)

1. Krekelberg B, Boynton GM, van Wezel RJ (2006) Adaptation: From single cells to BOLD signals. Trends Neurosci 29(5):250-256.
2. Wilson RI, Mainen ZF (2006) Early events in olfactory processing. Annu Rev Neurosci 29:163-201.
3. Mather G, Pavan A, Campana G, Casco C (2008) The motion aftereffect reloaded. Trends Cogn Sci 12(12):481-487.
4. Zwicker E (1964) "Negative afterimage" in hearing. J Acoust Soc Am 36:2413.
5. Hoke ES, Hoke M, Ross B (1996) Neurophysiological correlate of the auditory afterimage ("Zwicker tone"). Audiol Neurootol 1(3):161-174.
6. Vogels IM, Kappers AM, Koenderink JJ (1996) Haptic aftereffect of curved surfaces. Perception 25(1):109-119.
7. Petreanu L, et al. (2012) Activity in motor-sensory projections reveals distributed coding in somatosensation. Nature 489(7415):299-303.
8. James GA, Li X, DuBois GE, Zhou L, Hu XP (2009) Prolonged insula activation during perception of aftertaste. Neuroreport 20(3):245-250.
9. Schiffman SS, Reilly DA, Clark TB III, (1979) Qualitative differences among sweeteners. Physiol Behav 23(1):1-9.
10. Mazor O, Laurent G (2005) Transient dynamics versus fixed points in odor representations by locust antennal lobe projection neurons. Neuron 48(4):661-673.
11. Brown SL, Joseph J, Stopfer M (2005) Encoding a temporally structured stimulus with a temporally structured neural representation. Nat Neurosci 8(11):1568-1576.
12. Matsumoto H, Kashiwadani H, Nagao H, Aiba A, Mori K (2009) Odor-induced persistent discharge of mitral cells in the mouse olfactory bulb. J Neurophysiol 101(4): 1890-1900.
13. Verhagen JV, Wesson DW, Netoff TI, White JA, Wachowiak M (2007) Sniffing controls an adaptive filter of sensory input to the olfactory bulb. Nat Neurosci 10(5):631-639.
14. Rospars J-P, Lansky P, Chaput M, Duchamp-Viret P (2008) Competitive and noncompetitive odorant interactions in the early neural coding of odorant mixtures. J Neurosci 28(10): 2659-2666.
15. Spors H, Grinvald A (2002) Spatio-temporal dynamics of odor representations in the mammalian olfactory bulb. Neuron 34(2):301-315.
16. Cury KM, Uchida N (2010) Robust odor coding via inhalation-coupled transient activity in the mammalian olfactory bulb. Neuron 68(3):570-585.
17. Shusterman R, Smear MC, Koulakov AA, Rinberg D (2011) Precise olfactory responses tile the sniff cycle. Nat Neurosci 14(8):1039-1044.
18. Gschwend O, Beroud J, Carleton A (2012) Encoding odorant identity by spiking packets of rate-invariant neurons in awake mice. PLoS ONE 7(1):e30155.
19. Rinberg D, Koulakov A, Gelperin A (2006) Speed-accuracy tradeoff in olfaction. Neuron 51(3):351-358.
20. Abraham NM, et al. (2004) Maintaining accuracy at the expense of speed: Stimulus similarity defines odor discrimination time in mice. Neuron 44(5):865-876.
21. Uchida N, Mainen ZF (2003) Speed and accuracy of olfactory discrimination in the rat. Nat Neurosci 6(11):1224-1229.
22. Miura K, Mainen ZF, Uchida N (2012) Odor representations in olfactory cortex: Distributed rate coding and decorrelated population activity. Neuron 74(6): 1087-1098.
23. Poo C, Isaacson JS (2009) Odor representations in olfactory cortex: "Sparse" coding, global inhibition, and oscillations. Neuron 62(6):850-861.
24. Kadohisa M, Wilson DA (2006) Olfactory cortical adaptation facilitates detection of odors against background. J Neurophysiol 95(3):1888-1896.
25. Best AR, Wilson DA (2004) Coordinate synaptic mechanisms contributing to olfactory cortical adaptation. J Neurosci 24(3):652-660.
26. Slotnick BM, Ptak JE (1977) Olfactory intensity-difference thresholds in rats and humans. Physiol Behav 19(6):795-802.
27. Stopfer M, Jayaraman V, Laurent G (2003) Intensity versus identity coding in an olfactory system. Neuron 39(6):991-1004.
28. Vincis R, Gschwend O, Bhaukaurally K, Beroud J, Carleton A (2012) Dense representation of natural odorants in the mouse olfactory bulb. Nat Neurosci 15(4): 537-539.
29. Meredith M (1986) Patterned response to odor in mammalian olfactory bulb: The influence of intensity. J Neurophysiol 56(3):572-597.
30. Rezec A, Krekelberg B, Dobkins KR (2004) Attention enhances adaptability: Evidence from motion adaptation experiments. Vision Res 44(26):3035-3044.
31. Chaudhuri A (1990) Modulation of the motion aftereffect by selective attention. Nature 344(6261):60-62.
32. Kato HK, Chu MW, Isaacson JS, Komiyama T (2012) Dynamic sensory representations in the olfactory bulb: Modulation by wakefulness and experience. Neuron 76(5): 962-975.
33. 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(4):586-598.
34. Rojas-Líbano D, Kay LM (2012) Interplay between sniffing and odorant sorptive properties in the rat. J Neurosci 32:15577-15589.
35. Cenier T, McGann JP, Tsuno Y, Verhagen JV, Wachowiak M (2013) Testing the sorption hypothesis in olfaction: A limited role for sniff strength in shaping primary odor representations during behavior. J Neurosci 33(1):79-92.
36. Gautam SH, Verhagen J V (2012) Retronasal odor representations in the dorsal olfactory bulb of rats. J Neurosci 32:7949-7959.
37. Philpot BD, Foster TC, Brunjes PC (1997) Mitral/tufted cell activity is attenuated and becomes uncoupled from respiration following naris closure. J Neurobiol 33(4): 374-386.
38. Kikuta S, Kashiwadani H, Mori K (2008) Compensatory rapid switching of binasal inputs in the olfactory cortex. J Neurosci 28(46):11989-11997.
39. Neville KR, Haberly LB (2003) Beta and gamma oscillations in the olfactory system of the urethane-anesthetized rat. J Neurophysiol 90(6):3921-3930.
40. Kay LM, et al. (2009) Olfactory oscillations: The what, how and what for. Trends Neurosci 32(4):207-214.
41. Boyd AM, Sturgill JF, Poo C, Isaacson JS (2012) Cortical feedback control of olfactory bulb circuits. Neuron 76(6):1161-1174.
42. Arenkiel BR, et al. (2007) In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2. Neuron 54(2):205-218.
43. Laurent G, Wehr M, Davidowitz H (1996) Temporal representations of odors in an olfactory network. J Neurosci 16(12):3837-3847.
44. Friedrich RW, Laurent G (2001) Dynamic optimization of odor representations by slow temporal patterning of mitral cell activity. Science 291(5505):889-894.
45. Chaput MA, Panhuber H (1982) Effects of long duration odor exposure on the unit activity of olfactory bulb cells in awake rabbits. Brain Res 250(1):41-52.
46. Kreher SA, Kwon JY, Carlson JR (2005) The molecular basis of odor coding in the Drosophila larva. Neuron 46(3):445-456.
47. Montague SA, Mathew D, Carlson JR (2011) Similar odorants elicit different behavioral and physiological responses, some supersustained. J Neurosci 31(21): 7891-7899.
48. Schoppa NE, Urban NN (2003) Dendritic processing within olfactory bulb circuits. Trends Neurosci 26(9):501-506.
49. Isaacson JS (2010) Odor representations in mammalian cortical circuits. Curr Opin Neurobiol 20(3):328-331.
50. Strowbridge BW (2009) Role of cortical feedback in regulating inhibitory microcircuits. Ann N Y Acad Sci 1170:270-274.
51. Gao Y, Strowbridge BW (2009) Long-term plasticity of excitatory inputs to granule cells in the rat olfactory bulb. Nat Neurosci 12(6):731-733.
52. Markopoulos F, Rokni D, Gire DH, Murthy VN (2012) Functional properties of cortical feedback projections to the olfactory bulb. Neuron 76(6):1175-1188.
53. Fukunaga I, Berning M, Kollo M, Schmaltz A, Schaefer ATT (2012) Two distinct channels of olfactory bulb output. Neuron 75(2):320-329.
54. Igarashi KM, et al. (2012) Parallel mitral and tufted cell pathways route distinct odor information to different targets in the olfactory cortex. J Neurosci 32(23):7970-7985.
55. Dalton P (2000) Psychophysical and behavioral characteristics of olfactory adaptation. Chem Senses 25(4):487-492.
56. Gottfried JA (2010) Central mechanisms of odour object perception. Nat Rev Neurosci 11(9):628-641.
57. Kauer JS (1974) Response patterns of amphibian olfactory bulb neurones to odour stimulation. J Physiol 243(3):695-715.
58. Turner SL, et al. (2011) Ultra-prolonged activation of CO2-sensing neurons disorients mosquitoes. Nature 474(7349):87-91.
59. 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 USA 98(3):1230-1234.
60. Kohn A (2007) Visual adaptation: Physiology, mechanisms, and functional benefits. J Neurophysiol 97(5):3155-3164.
61. Huk AC, Ress D, Heeger DJ (2001) Neuronal basis of the motion aftereffect reconsidered. Neuron 32(1):161-72.
62. Galán RF, Weidert M, Menzel R, Herz AV, Galizia CG (2006) Sensory memory for odors is encoded in spontaneous correlated activity between olfactory glomeruli. Neural Comput 18(1):10-25.
63. Zariwala HA, et al. (2012) A Cre-dependent GCaMP3 reporter mouse for neuronal imaging in vivo. J Neurosci 32(9):3131-3141.
64. Li J, Ishii T, Feinstein P, Mombaerts P (2004) Odorant receptor gene choice is reset by nuclear transfer from mouse olfactory sensory neurons. Nature 428(6981):393-399.
65. Bathellier B, Van De Ville D, Blu T, Unser M, Carleton A (2007) Wavelet-based multiresolution statistics for optical imaging signals: Application to automated detection of odour activated glomeruli in the mouse olfactory bulb. Neuroimage 34(3): 1020-1035.