Functional recovery of odor representations in regenerated sensory inputs to the olfactory bulb

Frontiers in Neural Circuits

Volumn 7, Issue JAN, 2014, Pages

  Cheung, Man C ^a   Jang, Woochan ^b   Schwob, James E ^b   Wachowiak, Matt ^a,c  

^a Boston University   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c The Brain Institute at the University of Utah   (United States)

Author keywords

Axon targeting; Olfactory bulb; Regeneration; Sensory neurons; Synaptophluorin

Indexed keywords

OLFACTORY MARKER PROTEIN; SYNAPTOPHLUORIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; MALE; MOUSE; NERVE REGENERATION; NONHUMAN; ODOR; OLFACTOMETRY; OLFACTORY BULB; OLFACTORY EPITHELIUM; OLFACTORY NERVOUS SYSTEM; REINNERVATION; SENSORY NERVE CELL; SENSORY STIMULATION; SIGNAL TRANSDUCTION; TOPOGRAPHY; 129 MOUSE; ANIMAL; AXON TARGETING; C57BL MOUSE; CONVALESCENCE; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NERVE FIBER; NERVOUS SYSTEM DEVELOPMENT; OLFACTORY RECEPTOR; PHYSIOLOGY; REGENERATION; SENSORY NEURONS; SENSORY RECEPTOR; SYNAPTOPHLUORIN;

AXON TARGETING; OLFACTORY BULB; REGENERATION; SENSORY NEURONS; SYNAPTOPHLUORIN;

ANIMALS; AXONS; MALE; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; NEUROGENESIS; OLFACTORY BULB; OLFACTORY MUCOSA; RECEPTORS, ODORANT; RECOVERY OF FUNCTION; SENSORY RECEPTOR CELLS;

EID: 84892585541     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2013.00207     Document Type: Article

References (51)

1. Blanco-Hernández, E., Valle-Leija, P., Zomosa-Signoret, V., Drucker-Colín, R., and Vidaltamayo, R. (2012). Odor memory stability after reinnervation of the olfactory bulb. PLoS One 7:e46338. doi: 10.1371/journal.pone.0046338
2. Bozza, T., McGann, J. P., Mombaerts, P., and Wachowiak, M. (2004). In vivo imaging of neuronal activity by targeted expression of a genetically encoded probe in the mouse. Neuron 42, 9-21. doi: 10.1016/s0896-6273(04)00144-8
3. Bozza, T., Vassalli, A., Fuss, S., Zhang, J. J., Weiland, B., Pacifico, R., et al. (2009). Mapping of class I and class II odorant receptors to glomerular domains by two distinct types of olfactory sensory neurons in the mouse. Neuron 61, 220-233. doi: 10.1016/j.neuron.2008.11.010
4. Bracey, E. F., Pichler, B., Schaefer, A. T., Wallace, D. J., and Margrie, T. W. (2013). Perceptual judgements and chronic imaging of altered odour maps indicate comprehensive stimulus template matching in olfaction. Nat. Commun. 4:2100. doi: 10.1038/ncomms3100
5. Chen, X., Fang, H., and Schwob, J.E. (2004). Multipotency of purified, transplanted globose basal cells in olfactory epithelium. J. Comp. Neurol. 469, 457-474. doi: 10.1002/cne.11031
6. Christensen, M. D., Holbrook, E. H., Costanzo, R. M., and Schwob, J. E. (2001). Rhinotopy is disrupted during the re-innervation of the olfactory bulb that follows transection of the olfactory nerve. Chem. Senses 26, 359-369. doi: 10. 1093/chemse/26.4.359
7. Costanzo, R. M. (2000). Rewiring the olfactory bulb: changes in odor maps following recovery from nerve transection. Chem. Senses 25, 199-205. doi: 10. 1093/chemse/25.2.199
8. Costanzo, R. M., and Kobayashi, M. (2010). Age-related changes in P2 odorant receptor mapping in the olfactory bulb. Chem. Senses 35, 417-426. doi: 10. 1093/chemse/bjq029
9. Cummings, D. M., Emge, D. K., Small, S. L., and Margolis, F. L. (2000). Pattern of olfactory bulb innervation returns after recovery from reversible peripheral deafferentation. J. Comp. Neurol. 421, 362-373. doi: 10.1002/(sici)1096-9861(20000605)421:3<362::aid-cne5>3.0.co;2-8
10. Cummings, D. M., Henning, H. E., and Brunjes, P. C. (1997). Olfactory bulb recovery after early sensory deprivation. J. Neurosci. 17, 7433-7440.
11. Doty, R. L. (1979). A review of olfactory dysfunctions in man. Am. J. Otolaryngol. 1, 57-79. doi: 10.1016/s0196-0709(79)80010-1
12. Feinstein, P., Bozza, T., Rodriguez, I., Vassalli, A., and Mombaerts, P. (2004). Axon guidanceofmouse olfactorysensory neuronsbyodorant receptors and the beta2 adrenergic receptor. Cell 117, 833-846. doi: 10.1016/j.cell.2004.05.013
13. Gogos, J. A., Osborne, J., Nemes, A., Mendelsohn, M., and Axel, R. (2000). Genetic ablation and restoration of the olfactory topographic map. Cell 103, 609-620. doi: 10.1016/s0092-8674(00)00164-1
14. Imamura, K., Mataga, N., and Mori, K. (1992). Coding of odor molecules by mitral/tufted cells in rabbit olfactory bulb. I. Aliphatic compounds. J. Neuro-physiol. 68, 1986-2002.
15. Iwema, C. L., Fang, H., Kurtz, D. B., Youngentob, S. L., and Schwob, J. E. (2004). Odorant receptor expression patterns are restored in lesion-recovered rat olfactory epithelium. J. Neurosci. 24, 356-369. doi: 10.1523/jneurosci.1219-03.2004
16. Jang, W., Youngentob, S. L., and Schwob, J. E. (2003). Globose basal cells are required for reconstitution of olfactory epithelium after methyl bromide lesion. J. Comp. Neurol. 460, 123-140. doi: 10.1002/cne.10642
17. Johnson, B. A., Ho, S. L., Xu, Z., Yihan, J. S., Yip, S., Hingco, E. E., et al. (2002). Functional mapping of the rat olfactory bulb using diverse odorants reveals modular responses to functional groups and hydrocarbon structural features. J. Comp. Neurol. 449, 180-194. doi: 10.1002/cne.10284
18. Jones, S. V., Choi, D. C., Davis, M., and Ressler, K. J. (2008). Learning-dependent structural plasticity in the adult olfactory pathway. J. Neurosci. 28, 13106-13111. doi: 10.1523/jneurosci.4465-08.2008
19. Kass, M. D., Moberly, A. H., Rosenthal, M. C., Guang, S. A., and McGann, J. P. (2013). Odor-specific, olfactorymarker protein-mediated sparseningof primary olfactory input to the brain after odor exposure. J. Neurosci. 33, 6594-6602. doi: 10.1523/jneurosci.1442-12.2013
20. Kerr, M. A., and Belluscio, L. (2006). Olfactory experience accelerates glomerular refinement in the mammalian olfactory bulb. Nat. Neurosci. 9, 484-486. doi: 10. 1038/nn1673
21. Lam, Y.-W., Cohen, L. B., Wachowiak, M., and Zochowski, M. R. (2000). Odors elicit three different oscillations in the turtle olfactory bulb. J. Neurosci. 20, 749-762.
22. Matsumoto, H., Kobayakawa, K., Kobayakawa, R., Tashiro, T., Mori, K., and Sakano, H. (2010). Spatial arrangement of glomerular molecular-feature clusters in the odorant-receptor class domains of the mouse olfactory bulb. J. Neurophysiol. 103, 3490-3500. doi: 10.1152/jn.00035.2010
23. McGann, J. P., Pírez, N., Gainey, M. A., Muratore, C., Elias, A. S., and Wachowiak, M. (2005). Odorant representations are modulated by intra-but not inter-glomerular presynaptic inhibition of olfactory sensory neurons. Neuron 48, 1039-1053. doi: 10.1016/j.neuron.2005.10.031
24. McMillan Carr, V., Ring, G., Youngentob, S. L., Schwob, J. E., and Farbman, A. I. (2004). Altered epithelial density and expansion of bulbar projections of a discrete HSP70 immunoreactive subpopulation of rat olfactory receptor neurons in reconstituting olfactory epithelium following exposure to methyl bromide. J. Comp. Neurol. 469, 475-493. doi: 10.1002/cne.11020
25. Meisami, E., Mikhail, L., Baim, D., and Bhatnagar, K. P. (1998). Human olfactory bulb: aging of glomeruli and mitral cells and a search for the accessory olfactory bulb. Ann. N Y Acad. Sci. 855, 708-715. doi: 10.1111/j.1749-6632.1998.tb10649.x
26. Meister, M., and Bonhoeffer, T. (2001). Tuning and topography in an odor map on the rat olfactory bulb. J. Neurosci. 21, 1351-1360.
27. Mombaerts, P., Wang, F., Dulac, C., Chao, S. K., Nemes, A., Mendelsohn, M., et al. (1996). Visualizing an olfactory sensory map. Cell 87, 675-686. doi: 10. 1016/s0092-8674(00)81387-2
28. Nagao, H., Yamaguchi, M., Takahash, Y., and Mori, K. (2002). Grouping and representation of odorant receptors in domains of the olfactory bulb sensory map. Microsc. Res. Tech. 58, 168-175. doi: 10.1002/jemt.10146
29. Nakatani, H., Serizawa, S., Nakajima, M., Imai, T., and Sakano, H. (2003). Developmental elimination of ectopic projection sites for the transgenic OR gene that has lost zone specificity in the olfactory epithelium. Eur. J. Neurosci. 18, 2425-2432. doi: 10.1046/j.1460-9568.2003.02998.x
30. Oka, Y., Takai, Y., and Touhara, K. (2009). Nasal airflow rate affects the sensitivity and pattern of glomerular odorant responses in the mouse olfactory bulb. J. Neurosci. 29, 12070-12078. doi: 10.1523/jneurosci.1415-09.2009
31. Pacifico, R., Dewan, A., Cawley, D., Guo, C., and Bozza, T. (2012). An olfactory subsystem that mediates high-sensitivity detection of volatile amines. Cell Rep. 2, 76-88. doi: 10.1016/j.celrep.2012.06.006
32. Pírez, N., and Wachowiak, M. (2008). In vivo modulation of sensory input to the olfactory bulb by tonic and activity-dependent presynaptic inhibition of receptor neurons. J. Neurosci. 28, 6360-6371. doi: 10.1523/jneurosci.0793-08. 2008
33. Schaefer, M. L., Finger, T. E., and Restrepo, D. (2001). Variability of position of the P2 glomerulus within a map of the mouse olfactory bulb. J. Comp. Neurol. 436, 351-362. doi: 10.1002/cne.1072
34. Schoenfeld, T. A., Clancy, A. N., Forbes, W. B., and Macrides, F. (1994). The spatial organization of the peripheral olfactory system of the hamster. part I: receptor neuron projections to the main olfactory bulb. Brain Res. Bull. 34, 183-210. doi: 10.1016/0361-9230(94)90059-0
35. Schwarting, G. A., and Henion, T. R. (2011). Regulation and function of axon guidance and adhesion molecules during olfactory map formation. J. Cell.Biochem. 112, 2663-2671. doi: 10.1002/jcb.23203
36. Schwob, J. E. (2002). Neural regeneration and the peripheral olfactory system. Anat. Rec. 269, 33-49. doi: 10.1002/ar.10047
37. Schwob, J. E., and Gottlieb, D. I. (1986). The primary olfactory projection has two chemically distinct zones. J. Neurosci. 6, 3393-3404.
38. Schwob, J. E., Youngentob, S. L., and Mezza, R. C. (1995). Reconstitution of the rat olfactory epithelium after methyl bromide-induced lesion. J. Comp. Neurol. 359, 15-37. doi: 10.1002/cne.903590103
39. Schwob, J. E., Youngentob, S. L., Ring, G., Iwema, C. L., and Mezza, R. C. (1999). Reinnervation of the rat olfactory bulb after methyl bromide-induced lesion: timing and extent of reinnervation. J. Comp. Neurol. 412, 439-457. doi: 10. 1002/(sici)1096-9861(19990927)412:3<439::aid-cne5>3.0.co;2-h
40. St John, J., and Key, B. (2003). Axon mis-targeting in the olfactory bulb during regeneration of olfactory neuroepithelium. Chem. Senses 28, 773-779. doi: 10. 1093/chemse/bjg068
41. Strotmann, J., Conzelmann, S., Beck, A., Feinstein, P., Breer, H., and Mombaerts, P. (2000). Local permutations in the glomerular array of the mouse olfactory bulb. J. Neurosci. 20, 6927-6938.
42. Takahashi, Y. K., Kurosaki, M., Hirono, S., and Mori, K. (2004). Topographic representation of odorant molecular features in the rat olfactory bulb. J. Neurophysiol. 92, 2413-2427. doi: 10.1152/jn.00236.2004
43. Treloar, H. B., Feinstein, P., Mombaerts, P., and Greer, C. A. (2002). Specificity of glomerular targeting by olfactory sensory axons. J. Neurosci. 22,2469-2477.
44. Uchida, N., Takahashi, Y. K., Tanifuji, M., and Mori, K. (2000). Odor maps in the mammalian olfactory bulb: domain organization and odorant structural features. Nat. Neurosci. 3, 1035-1043. doi: 10.1038/79857
45. Vedin, V., Slotnick, B., and Berghard, A. (2004). Zonal ablation of the olfactory sensory neuroepithelium of the mouse: effects on odorant detection. Eur. J. Neurosci. 20, 1858-1864. doi: 10.1111/j.1460-9568.2004.03634.x
46. Wachowiak, M., and Cohen, L. B. (2001). Representation of odorants by receptor neuron input to the mouse olfactory bulb. Neuron 32, 723-735. doi: 10. 1016/s0896-6273(01)00506-2
47. Wachowiak, M., Denk, W., and Friedrich, R. W. (2004). Functional organization of sensory input to the olfactory bulb glomerulus analyzed by two-photon calcium imaging. Proc. Natl. Acad. Sci. U S A 101, 9097-9102. doi: 10.1073/pnas.0400438101
48. Wachowiak, M., Economo, M. N., Díaz-Quesada, M., Brunert, D., Wesson, D. W., White, J. A., et al. (2013). Optical dissection of odor information processing in vivo using gcamps expressed in specified cell types of the olfactory bulb. J. Neurosci. 33, 5285-5300. doi: 10.1523/jneurosci.4824-12.2013
49. Xu, H. T., Pan, F., Yang, G., and Gan, W. B. (2007). Choice of cranial window type for in vivo imaging affects dendritic spine turnover in the cortex. Nat. Neurosci. 10, 549-551. doi: 10.1038/nn1883
50. Yee, K. K., and Costanzo, R. M. (1998). Changes in odor quality discrimination following recovery from olfactory nerve transection. Chem. Senses 23, 513-519. doi: 10.1093/chemse/23.5.513
51. Zou, D.-J., Feinstein, P., Rivers, A. L., Mathews, G. A., Kim, A., Greer, C. A., et al. (2004). Postnatal refinement of peripheral olfactory projections. Science 304, 1976-1979. doi: 10.1126/science.1093468