Temporal dynamics and latency patterns of receptor neuron input to the olfactory bulb

Journal of Neuroscience

Volumn 26, Issue 4, 2006, Pages 1247-1259

  Spors, Hartwig ^a   Wachowiak, Matt ^b,c   Cohen, Lawrence B ^b   Friedrich, Rainer W ^a  

^a MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Boston University   (United States)

Author keywords

Imaging; in vivo; Maps; Mouse; Olfaction; Sensory coding

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BREATHING; CORRELATION ANALYSIS; GLOMERULUS; MODULATION; MOUSE; NONHUMAN; OLFACTORY BULB; OLFACTORY SYSTEM; PRIORITY JOURNAL; SENSORY NERVE CONDUCTION; SENSORY STIMULATION; SNIFFING;

ANIMALS; CALCIUM SIGNALING; INHALATION; MICE; MICE, INBRED C57BL; ODORS; OLFACTORY BULB; OLFACTORY PATHWAYS; OLFACTORY RECEPTOR NEURONS; REACTION TIME; TIME FACTORS; TRACHEOTOMY;

EID: 32544439828     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3100-05.2006     Document Type: Article

References (77)

1. Abraham NM, Spors H, Carleton A, Margrie TW, Kuner T, Schaefer AT (2004) Maintaining accuracy at the expense of speed; stimulus similarity defines odor discrimination time in mice. Neuron 44:865-876.
2. Adrian ED (1950) The electrical activity of the mammalian olfactory bulb. Electroencephalogr Clin Neurophysiol 2:377-388.
3. Ambros-Ingerson J, Granger R, Lynch G (1990) Simulation of paleocortex performs hierarchical clustering. Science 247:1344-1348.
4. B heteroreceptors. J Neurophysiol 84:1194-1203.
5. Belluscio L, Katz LC (2001) Symmetry, stereotypy, and topography of odorant representations in mouse olfactory bulbs. J Neurosci 21:2113-2122.
6. Bozza T, Feinstein P, Zheng C, Mombaerts P (2002) Odorant receptor expression defines functional units in the mouse olfactory system. J Neurosci 22:3033-3043.
7. Bozza T, McGann JP, Mombaerts P, Wachowiak M (2004) In vivo imaging of neuronal activity by targeted expression of a genetically encoded probe in the mouse. Neuron 42:9-21.
8. Buonviso N, Chaput MA, Berthommier F (1992) Temporal pattern analyses in pairs of neighboring mitral cells. J Neurophysiol 68:417-424.
9. 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.
10. Chaput M, Holley A (1980) Single unit responses of olfactory bulb neurones to odour presentation in awake rabbits. J Physiol (Paris) 76:551-558.
11. Chaput MA, Buonviso N, Berthommier F (1992) Temporal patterns in spontaneous and odor-evoked mitral cell discharges recorded in anesthetized freely breathing animals. Eur J Neurosci 4:813-822.
12. Cinelli AR, Hamilton KA, Kauer JS (1995) Salamander olfactory-bulb neuronal-activity observed by video-rate, voltage-sensitive dye imaging. 3. Spatial and temporal properties of responses evoked by odorant stimulation. J Neurophysiol 73:2053-2071.
13. Digital Signal Processing Committee (1979) Algorithm 8.1. In: Programs for digital signal processing. New York: IEEE.
14. Dorries KM, Kauer JS (2000) Relationships between odor-elicited oscillations in the salamander olfactory epithelium and olfactory bulb. J Neurophysiol 83:754-765.
15. Duchamp-Viret P, Chaput MA, Duchamp A (1999) Odor response properties of rat olfactory receptor neurons. Science 284:2171-2174.
16. Ennis M, Zhou FM, Ciombor KJ, Aroniadou-Anderjaska V, Hayar A, Borrelli E, Zimmer LA, Margolis F, Shipley MT (2001) Dopamine D2 receptor-mediated presynaptic inhibition of olfactory nerve terminals. J Neurophysiol 86:2986-2997.
17. Ezeh PI, Davis LM, Scott JW (1995) Regional distribution of rat electroolfactogram. J Neurophysiol 73:2207-2220.
18. Firestein S, Picco C, Menini A (1993) The relation between stimulus and response in olfactory receptor-cells of the tiger salamander. J Physiol (Lond) 468:1-10.
19. Fried HU, Fuss SH, Korsching SI (2002) Selective imaging of presynaptic activity in the mouse olfactory bulb shows concentration and structure dependence of odor responses in identified glomeruli. Proc Natl Acad Sci USA 99:3222-3227.
20. Friedrich RW, Korsching SI (1997) Combinatorial and chemotopic odorant coding in the zebrafish olfactory bulb visualized by optical imaging. Neuron 18:737-752.
21. Friedrich RW, Laurent G (2001) Dynamic optimization of odor representations by slow temporal patterning of mitral cell activity. Science 291:889-894.
22. Gawne TJ, Kjaer TW, Richmond BJ (1996) Latency: another potential code for feature binding in striate cortex. J Neurophysiol 76:1356-1360.
23. Goldberg SJ, Moulton DG (1987) Olfactory bulb responses telemetered during an odor discrimination task in rats. Exp Neurol 96:430-442.
24. Gray CM (1994) Synchronous oscillations in neuronal systems: mechanisms and functions. J Comput Neurosci 1:11-38.
25. Guthrie KM, Anderson AJ, Leon M, Gall C (1993) Odor-induced increases in c-fos messenger-RNA expression reveal an anatomical unit for odor processing in olfactory-bulb. Proc Natl Acad Sci USA 90:3329-3333.
26. Hallem EA, Ho MG, Carlson JR (2004) The molecular basis of odor coding in the Drosophila antenna. Cell 117:965-979.
27. Hildebrand JG, Shepherd GM (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20:595-631.
28. Hopfield JJ (1995) Pattern-recognition computation using action-potential timing for stimulus representation. Nature 376:33-36.
29. Jinks A, Laing DG, Hutchinson I, Oram N (1998) Temporal processing of odor mixtures reveals that identification of components takes precedence over temporal information in olfactory memory. Ann NY Acad Sci 855:834-836.
30. Johnson BA, Woo CC, Leon M (1998) Spatial coding of odorant features in the glomerular layer of the rat olfactory bulb. J Comp Neurol 393:457-471.
31. Johnson BN, Mainland JD, Sobel N (2003) Rapid olfactory processing implicates subcortical control of an olfactomotor system. J Neurophysiol 90:1084-1094.
32. Karpov AP (1980) Analysis of neuron activity in the rabbit's olfactory bulb during food-acquisition behavior. In: Neural mechanisms of goal-directed behavior (Thompson RF, Hicks LH, Shvyrkov VB, eds), pp 273-282. New York: Academic.
33. Kauer JS (1974) Response patterns of amphibian olfactory bulb neurones to odour stimulation. J Physiol (Lond) 243:695-715.
34. Kauer JS, Moulton DG (1974) Responses of olfactory bulb neurones to odour stimulation of small nasal areas in the salamander. J Physiol (Lond) 243:717-737.
35. Kauer JS, Senseman DM, Cohen LB (1987) Odor-elicited activity monitored simultaneously from 124 regions of the salamander olfactory bulb using a voltage-sensitive dye. Brain Res 418:255-261.
36. Kay LM, Laurent G (1999) Odor- and context-dependent modulation of mitral cell activity in behaving rats. Nat Neurosci 2:1003-1009.
37. Kent PF, Mozell MM, Murphy SJ, Hornung DE (1996) The interaction of imposed and inherent olfactory mucosal activity patterns and their composite representation in a mammalian species using voltage-sensitive dyes. J Neurosci 16:345-353.
38. Lagier S, Carleton A, Lledo PM (2004) Interplay between local GABAergic interneurons and relay neurons generates gamma oscillations in the rat olfactory bulb. J Neurosci 24:4382-4392.
39. Lam YW, Cohen LB, Wachowiak M, Zochowski MR (2000) Odors elicit three different oscillations in the turtle olfactory bulb. J Neurosci 20:749-762.
40. Laurent G (2002) Olfactory network dynamics and the coding of multidimensional signals. Nat Rev Neurosci 3:884-895.
41. Lehmkuhle MJ, Normann RA, Maynard EM (2003) High-resolution analysis of the spatio-temporal activity patterns in rat olfactory bulb evoked by enantiomer odors. Chem Senses 28:499-508.
42. Leveteau J, MacLeod P (1966) Olfactory discrimination in the rabbit olfatory glomerulus. Science 175:170-178.
43. Lin W, Arellano J, Slotnick B, Restrepo D (2004) Odors detected by mice deficient in cyclic nucleotide-gated channel subunit A2 stimulate the main olfactory system. J Neurosci 24:3703-3710.
44. Luo M, Katz LC (2001) Response correlation maps of neurons in the mammalian olfactory bulb. Neuron 32:1165-1179.
45. Macrides F, Chorover SL (1972) Olfactory bulb units: activity correlated with inhalation cycles and odor quality. Science 175:84-87.
46. Margrie TW, Schaefer AT (2003) Theta oscillation coupled spike latencies yield computational vigour in a mammalian sensory system. J Physiol (Lond) 546:363-374.
47. Martin C, Gervais R, Hugues E, Messaoudi B, 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.
48. McGann JP, Pirez N, Gainey MA, Muratore C, Elias AS, Wachowiak M (2005) Odorant representation are modulated by intraglomerular but not interglomerular presynaptic inhibition of olfactory sensory neurons. Neuron 48:1039-1053.
49. Meister M, Bonhoeffer T (2001) Tuning and topography in an odor map on the rat olfactory bulb. J Neurosci 21:1351-1360.
50. Meredith M (1986) Patterned response to odor in mammalian olfactory bulb: the influence of intensity. J Neurophysiol 56:572-597.
51. Mombaerts P, Wang F, Dulac C, Chao SK, Nemes A, Mendelsohn M, Edmondson J, Axel R (1996) Visualizing an olfactory sensory map. Cell 87:675-686.
52. Optican LM, Richmond BJ (1987) Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. III. Information theoretic analysis. J Neurophysiol 57:162-178.
53. Pager J (1985) Respiration and olfactory-bulb unit-activity in the unrestrained rat - statements and reappaisals. Behav Brain Res 16:81-94.
54. Reisert J, Matthews HR (2001) Response properties of isolated mouse olfactory receptor cells. J Physiol (Lond) 530:113-122.
55. Ressler KJ, Sullivan SL, Buck LB (1994) Information coding in the olfactory system - evidence for a stereotyped and highly organized epitope map in the olfactory-bulb. Cell 79:1245-1255.
56. Richmond BJ, Gawne TJ, Jin GX (1997) Neuronal codes: reading them and learning how their structure influences network organization. Biosystems 40:149-157.
57. Rubin BD, Katz LC (1999) Optical imaging of odorant representations in the mammalian olfactory bulb. Neuron 23:499-511.
58. Sachse S, Galizia CG (2002) Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. J Neurophysiol 87:1106-1117.
59. Sachse S, Rappert A, Galizia CG (1999) The spatial representation of chemical structures in the antennal lobe of honeybees: steps towards the olfactory code. Eur J Neurosci 11:3970-3982.
60. Slotnick BM, Nigrosh BJ (1974) Olfactory stimulus control evaluated in a small animal olfactometer. Percept Mot Skills 39:583-597.
61. Spehr M, Wetzel CH, Hatt H, Ache BW (2002) 3-Phosphoinositides modulate cyclic nucleotide signaling in olfactory receptor neurons. Neuron 33:731-739.
62. Spors H, Grinvald A (2002) Spatio-temporal dynamics of odor representations in the mammalian olfactory bulb. Neuron 34:301-315.
63. Stewart WB, Kauer JS, Shepherd GM (1979) Functional-organization of rat olfactory-bulb analyzed by the 2-deoxyglucose method. J Comp Neurol 185:715-734.
64. Strotmann J, Conzelmann S, Beck A, Feinstein P, Breer H, Mombaerts P (2000) Local permutations in the glomerular array of the mouse olfactory bulb. J Neurosci 20:6927-6938.
65. Uchida N, Mainen ZF (2003) Speed and accuracy of olfactory discrimination in the rat. Nat Neurosci 6:1224-1229.
66. Urban NN, Sakmann B (2002) Reciprocal intraglomerular excitation and intra- and interglomerular lateral inhibition between mouse olfactory bulb mitral cells. J Physiol (Lond) 542:355-367.
67. Vassar R, Chao S, Sitcher, Nunez JM, Vosshall LB, Axel R (1994) Topographic organization of sensory projections to the olfactory-bulb. Cell 79:981-991.
68. Wachowiak M, Cohen LB (1999) Presynaptic inhibition of primary olfactory afferents mediated by different mechanisms in lobster and turtle. J Neurosci 19:8808-8817.
69. Wachowiak M, Cohen LB (2001) Representation of odorants by receptor neuron input to the mouse olfactory bulb. Neuron 32:723-735.
70. Wachowiak M, Cohen LB (2003) Correspondence between odorant-evoked patterns of receptor neuron input and intrinsic optical signals in the mouse olfactory bulb. J Neurophysiol 89:1623-1639.
71. Wachowiak M, Denk W, Friedrich RW (2004) Functional organization of sensory input to the olfactory bulb glomerulus analyzed by two-photon calcium imaging. Proc Natl Acad Sci USA 101:9097-9102.
72. Wachowiak M, McGann JP, Heyward PM, Shao Z, Puche AC, Shipley MT (2005) Inhibition of olfactory receptor neuron input to olfactory bulb glomeruli mediated by suppression of presynaptic calcium influx. J Neurophysiol 94:2700-2712.
73. Wellis DP, Scott JW, Harrison TA (1989) Discrimination among odorants by single neurons of the rat olfactory-bulb. J Neurophysiol 61:1161-1177.
74. Wise PM, Cain WS (2000) Latency and accuracy of discriminations of odor quality between binary mixtures and their components. Chem Senses 25:247-265.
75. Xu F, Kida I, Hyder F, Shulman RG (2000) Assessment and discrimination of odor stimuli in rat olfactory bulb by dynamic functional MRI. Proc Natl Acad Sci USA 97:10601-10606.
76. Xu F, Liu N, Kida I, Rothman DL, Hyder F, Shepherd GM (2003) Odor maps of aldehydes and esters revealed by functional MRI in the glomerular layer of the mouse olfactory bulb. Proc Natl Acad Sci USA 100:11029-11034.
77. Youngentob SL, Mozell MM, Sheehe PR, Hornung DE (1987) A quantitative analysis of sniffing strategies in rats performing odor detection tasks. Physiol Behav 41:59-69.