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Neural Plasticity
Volume 2012 (2012), Article ID 351752, 14 pages
http://dx.doi.org/10.1155/2012/351752
Review Article

Studies of Olfactory System Neural Plasticity: The Contribution of the Unilateral Naris Occlusion Technique

David M. Coppola

Department of Biology, Randolph Macon College, Ashland, VA 23005, USA

Received 16 December 2011; Revised 1 March 2012; Accepted 19 March 2012

Academic Editor: Ron Kupers

Copyright © 2012 David M. Coppola. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. Held, Y. Ostrovsky, B. Degelder et al., “The newly sighted fail to match seen with felt,” Nature Neuroscience, vol. 14, no. 5, pp. 551–553, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. C. Darwin, The Variation of Animals and Plants Under Domestication, vol. 1, John Murray, London, UK, 1868.
  3. L. Sarikcioglu, “Johann Bernhard Aloys von Gudden: an outstanding scientist,” Journal of Neurology, Neurosurgery & Psychiatry, vol. 78, no. 2, p. 195, 2007. View at Publisher · View at Google Scholar
  4. Gudden, “Experimentaluntersuchungen über das peripherische und centrale Nervensystem,” Archiv für Psychiatrie und Nervenkrankheiten, vol. 2, no. 3, pp. 693–723, 1870. View at Publisher · View at Google Scholar · View at Scopus
  5. T. N. Wiesel, “Postnatal development of the visual cortex and the influence of environment,” Nature, vol. 299, no. 5884, pp. 583–591, 1982. View at Google Scholar · View at Scopus
  6. P. C. Brunjes, “Unilateral naris closure and olfactory system development,” Brain Research Reviews, vol. 19, no. 1, pp. 146–160, 1994. View at Publisher · View at Google Scholar · View at Scopus
  7. G. V. Ronnett and C. Moon, “G proteins and olfactory signal transduction,” Annual Review of Physiology, vol. 64, pp. 189–222, 2002. View at Publisher · View at Google Scholar · View at Scopus
  8. T. Hengl, H. Kaneko, K. Dauner, K. Vocke, S. Frings, and F. Möhrlen, “Molecular components of signal amplification in olfactory sensory cilia,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 13, pp. 6052–6057, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. D. J. Zou, A. Chesler, and S. Firestein, “How the olfactory bulb got its glomeruli: a just so story?” Nature Reviews Neuroscience, vol. 10, no. 8, pp. 611–618, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. T. E. Benson, D. K. Ryugo, and J. W. Hinds, “Effects of sensory deprivation on the developing mouse olfactory system: a light and electron microscopic, morphometric analysis,” Journal of Neuroscience, vol. 4, no. 3, pp. 638–653, 1984. View at Google Scholar · View at Scopus
  11. D. M. Cummings, B. R. Knab, and P. C. Brunjes, “Effects of unilateral olfactory deprivation in the developing opossum, Monodelphis domestica,” Journal of Neurobiology, vol. 33, no. 4, pp. 429–438, 1997. View at Google Scholar
  12. E. Meisami, “Effects of olfactory deprivation on postnatal growth of the rat olfactory bulb utilizing a new method for production of neonatal unilateral anosmia,” Brain Research, vol. 107, no. 2, pp. 437–444, 1976. View at Publisher · View at Google Scholar · View at Scopus
  13. E. Meisami and L. Safari, “A quantitative study of the effects of early unilateral olfactory deprivation on the number and distribution of mitral and tufted cells and of glomeruli in the rat olfactory bulb,” Brain Research, vol. 221, no. 1, pp. 81–107, 1981. View at Publisher · View at Google Scholar · View at Scopus
  14. L. L. Frazier and P. C. Brunjes, “Unilateral odor deprivation: early postnatal changes in olfactory bulb cell density and number,” Journal of Comparative Neurology, vol. 269, no. 3, pp. 355–370, 1988. View at Google Scholar · View at Scopus
  15. D. M. Cummings and L. Belluscio, “Continuous neural plasticity in the olfactory intrabulbar circuitry,” Journal of Neuroscience, vol. 30, no. 27, pp. 9172–9180, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. A. M. Oliva, K. R. Jones, and D. Restrepo, “Sensory-dependent asymmetry for a urine-responsive olfactory bulb glomerulus,” Journal of Comparative Neurology, vol. 510, no. 5, pp. 475–483, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. A. M. Oliva, E. Salcedo, J. L. Hellier et al., “Toward a mouse neuroethology in the laboratory environment,” PLoS ONE, vol. 5, no. 6, Article ID e11359, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. L. Frazier-Cierpial and P. C. Brunjes, “Early postnatal cellular proliferation and survival in the olfactory bulb and rostral migratory stream of normal and unilaterally odor-deprived rats,” Journal of Comparative Neurology, vol. 289, no. 3, pp. 481–492, 1989. View at Google Scholar · View at Scopus
  19. A. Saghatelyan, P. Roux, M. Migliore et al., “Activity-dependent adjustments of the inhibitory network in the olfactory bulb following early postnatal deprivation,” Neuron, vol. 46, no. 1, pp. 103–116, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. D. L. Korol and P. C. Brunjes, “Rapid changes in 2-deoxyglucose uptake and amino acid incorporation following unilateral odor deprivation: a laminar analysis,” Developmental Brain Research, vol. 52, no. 1-2, pp. 75–84, 1990. View at Google Scholar · View at Scopus
  21. P. E. Pedersen, G. M. Shephard, and C. A. Greer, “Cytochrome oxidase staining in the olfactory epithelium and bulb of normal and odor-deprived neonatal rats,” Annals of the New York Academy of Sciences, vol. 510, pp. 544–546, 1987. View at Google Scholar · View at Scopus
  22. E. Meisami and R. Mousavi, “Lasting effects of early olfactory deprivation on the growth, DNA, RNA and protein content, and Na-K-ATPase and AChE activity of the rat olfactory bulb,” Developmental Brain Research, vol. 2, no. 2, pp. 217–229, 1981. View at Publisher · View at Google Scholar · View at Scopus
  23. H. Baker, “Unilateral, neonatal olfactory deprivation alters tyrosine hydroxylase expression but not aromatic amino acid decarboxylase or GABA immunoreactivity,” Neuroscience, vol. 36, no. 3, pp. 761–771, 1990. View at Publisher · View at Google Scholar · View at Scopus
  24. H. Baker, K. Morel, D. M. Stone, and J. A. Maruniak, “Adult naris closure profoundly reduces tyrosine hydroxylase expression in mouse olfactory bulb,” Brain Research, vol. 614, no. 1-2, pp. 109–116, 1993. View at Google Scholar · View at Scopus
  25. T. Kosaka, K. Kosaka, and K. Hama, “Differential effect of functional olfactory deprivation on the GABAergic and catecholaminergic traits in the rat main olfactory bulb,” Brain Research, vol. 413, no. 1, pp. 197–203, 1987. View at Google Scholar · View at Scopus
  26. H. Baker, T. Kawano, F. L. Margolis, and T. H. Joh, “Transneuronal regulation of tyrosine hydroxylase expression in olfactory bulb of mouse and rat,” Journal of Neuroscience, vol. 3, no. 1, pp. 69–78, 1983. View at Google Scholar · View at Scopus
  27. N. S. Nadi, R. Head, M. Grillo, J. Hempstead, N. Grannot-Reisfeldc, and F. L. Margolis, “Chemical deafferentation of the olfactory bulb: plasticity of the levels of tyrosine hydroxylase, dopamine and norepinephrine,” Brain Research, vol. 213, no. 2, pp. 365–377, 1981. View at Google Scholar
  28. C. C. Woo and M. Leon, “Distribution and development of beta-adrenergic receptors in the rat olfactory bulb,” Journal of Comparative Neurology, vol. 352, no. 1, pp. 1–10, 1995. View at Publisher · View at Google Scholar · View at Scopus
  29. P. C. Brunjes, L. K. Smith-Crafts, and R. McCarty, “Unilateral odor deprivation: effects on the development of olfactory bulb catecholamines and behavior,” Brain Research, vol. 354, no. 1, pp. 1–6, 1985. View at Google Scholar · View at Scopus
  30. K. A. Hamilton and D. M. Coppola, “Distribution of GluR1 is altered in the olfactory bulb following neonatal naris occlusion,” Journal of Neurobiology, vol. 54, no. 2, pp. 326–336, 2003. View at Publisher · View at Google Scholar · View at Scopus
  31. F. Gomez-Pinilla, K. M. Guthrie, M. Leon, and M. Nieto-Sampedro, “NGF receptor increase in the olfactory bulb of the rat after early odor deprivation,” Developmental Brain Research, vol. 48, no. 2, pp. 161–165, 1989. View at Google Scholar · View at Scopus
  32. J. H. McLean, A. Darby-King, and W. S. Bonnell, “Neonatal olfactory sensory deprivation decreases BDNF in the olfactory bulb of the rat,” Developmental Brain Research, vol. 128, no. 1, pp. 17–24, 2001. View at Publisher · View at Google Scholar · View at Scopus
  33. K. C. Biju, T. G. Mast, and D. A. Fadool, “Olfactory sensory deprivation increases the number of proBDNF-immunoreactive mitral cells in the olfactory bulb of mice,” Neuroscience Letters, vol. 447, no. 1, pp. 42–47, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. D. A. Fadool, K. Tucker, J. J. Phillips, and J. A. Simmen, “Brain insulin receptor causes activity-dependent current suppression in the olfactory bulb through multiple phosphorylation of Kv1.3,” Journal of Neurophysiology, vol. 83, no. 4, pp. 2332–2348, 2000. View at Google Scholar · View at Scopus
  35. K. Tucker and D. A. Fadool, “Neurotrophin modulation of voltage-gated potassium channels in rat through TrkB receptors is time and sensory experience dependent,” Journal of Physiology, vol. 542, no. 2, pp. 413–429, 2002. View at Publisher · View at Google Scholar · View at Scopus
  36. J. M. Mirich, K. R. Illig, and P. C. Brunjes, “Experience-dependent activation of Extracellular Signal-Related Kinase (ERK) in the olfactory bulb,” Journal of Comparative Neurology, vol. 479, no. 2, pp. 234–241, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. D. A. Wilson, K. M. Guthrie, and M. Leon, “Modification of olfactory bulb synaptic inhibition by early unilateral olfactory deprivation,” Neuroscience Letters, vol. 116, no. 3, pp. 250–256, 1990. View at Publisher · View at Google Scholar · View at Scopus
  38. D. A. Wilson and J. G. Wood, “Functional consequences of unilateral olfactory deprivation: time-course and age sensitivity,” Neuroscience, vol. 49, no. 1, pp. 183–192, 1992. View at Publisher · View at Google Scholar · View at Scopus
  39. D. A. Wilson, “NMDA receptors mediate expression of one form of functional plasticity induced by olfactory deprivation,” Brain Research, vol. 677, no. 2, pp. 238–242, 1995. View at Publisher · View at Google Scholar · View at Scopus
  40. D. A. Wilson and R. M. Sullivan, “The D2 antagonist spiperone mimics the effects of olfactory deprivation on mitral/tufted cell odor response patterns,” Journal of Neuroscience, vol. 15, no. 8, pp. 5574–5581, 1995. View at Google Scholar · View at Scopus
  41. B. D. Philpot, T. C. Foster, and P. C. Brunjes, “Mitral/tufted cell activity is attenuated and becomes uncoupled from respiration following naris closure,” Journal of Neurobiology, vol. 33, no. 4, pp. 374–386, 1997. View at Google Scholar
  42. B. J. Maher, M. J. McGinley, and G. L. Westbrook, “Experience-dependent maturation of the glomerular microcircuit,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 39, pp. 16865–16870, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. K. M. Guthrie, D. A. Wilson, and M. Leon, “Early unilateral deprivation modifies olfactory bulb function,” Journal of Neuroscience, vol. 10, no. 10, pp. 3402–3412, 1990. View at Google Scholar · View at Scopus
  44. P. C. Brunjes, A. O. Caggiano, D. L. Korol, and J. S. Stewart, “Unilateral olfactory deprivation: effects on succinate dehydrogenase histochemistry and [3H]leucine incorporation in the olfactory mucosa,” Developmental Brain Research, vol. 62, no. 2, pp. 239–244, 1991. View at Publisher · View at Google Scholar · View at Scopus
  45. A. I. Farbman, P. C. Brunjes, L. Rentfro, J. Michas, and S. Ritz, “The effect of unilateral naris occlusion on cell dynamics in the developing rat olfactory epithelium,” Journal of Neuroscience, vol. 8, no. 9, pp. 3290–3295, 1988. View at Google Scholar · View at Scopus
  46. B. Stahl, H. Distel, and R. Hudson, “Effects of reversible nare occlusion on the development of the olfactory epithelium in the rabbit nasal septum,” Cell and Tissue Research, vol. 259, no. 2, pp. 275–281, 1990. View at Publisher · View at Google Scholar · View at Scopus
  47. D. M. Cummings and P. C. Brunjes, “Changes in cell proliferation in the developing olfactory epithelium following neonatal unilateral naris occlusion,” Experimental Neurology, vol. 128, no. 1, pp. 124–128, 1994. View at Publisher · View at Google Scholar · View at Scopus
  48. J. M. Mirich and P. C. Brunjes, “Activity modulates neuronal proliferation in the developing olfactory epithelium,” Developmental Brain Research, vol. 127, no. 1, pp. 77–80, 2001. View at Publisher · View at Google Scholar · View at Scopus
  49. M. A. Cavallin, K. Powell, K. C. Biju, and D. A. Fadool, “State-dependent sculpting of olfactory sensory neurons is attributed to sensory enrichment, odor deprivation, and aging,” Neuroscience Letters, vol. 483, no. 2, pp. 90–95, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. J. A. Cámara, M. Garrosa, and M. J. Gayoso, “Histological changes in rat nasal epithelia after unilateral neonatal naris occlusion,” Microscopy Research and Technique, vol. 69, no. 7, pp. 585–594, 2006. View at Publisher · View at Google Scholar · View at Scopus
  51. E. Weiler, J. Seeger, J. Cherry, and D. Coppola, The Effect of Perinatal Naris Occlusion on Nasal Turbinate Development: Does Emmetropization Occur in the Nose?European Chemoreception Research Organization, Manchester UK, 2011.
  52. T. Kaneko-Goto, S. I. Yoshihara, H. Miyazaki, and Y. Yoshihara, “BIG-2 Mediates Olfactory Axon Convergence to Target Glomeruli,” Neuron, vol. 57, no. 6, pp. 834–846, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. H. Oztokatli, M. Hörnberg, A. Berghard, and S. Bohm, “Retinoic acid receptor and CNGA2 channel signaling are part of a regulatory feedback loop controlling axonal convergence and survival of olfactory sensory neurons,” The FASEB Journal, vol. 26, no. 2, pp. 617–627, 2012. View at Publisher · View at Google Scholar
  54. E. O. Williams, H. M. Sickles, A. L. Dooley, S. Palumbos, A. J. Bisogni, and D. M. Lin, “Delta Protocadherin 10 is regulated by activity in the mouse main olfactory system,” Frontiers in Neural Circuits. In press. View at Publisher · View at Google Scholar
  55. D. A. Wilson, A. R. Best, and P. C. Brunjes, “Trans-neuronal modification of anterior piriform cortical circuitry in the rat,” Brain Research, vol. 853, no. 2, pp. 317–322, 2000. View at Publisher · View at Google Scholar · View at Scopus
  56. H. H. Kim, A. C. Puche, and F. L. Margolis, “Odorant deprivation reversibly modulates transsynaptic changes in the NR2B-mediated CREB pathway in mouse piriform cortex,” Journal of Neuroscience, vol. 26, no. 37, pp. 9548–9559, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. K. M. Franks and J. S. Isaacson, “Synapse-specific downregulation of NMDA receptors by early experience: a critical period for plasticity of sensory input to olfactory cortex,” Neuron, vol. 47, no. 1, pp. 101–114, 2005. View at Publisher · View at Google Scholar · View at Scopus
  58. A. R. Best and D. A. Wilson, “A postnatal sensitive period for plasticity of cortical afferents but not cortical association fibers in rat piriform cortex,” Brain Research, vol. 961, no. 1, pp. 81–87, 2003. View at Publisher · View at Google Scholar · View at Scopus
  59. J. L. Brown and P. C. Brunjes, “Development of the anterior olfactory nucleus in normal and unilaterally odor deprived rats,” Journal of Comparative Neurology, vol. 301, no. 1, pp. 15–22, 1990. View at Google Scholar · View at Scopus
  60. D. M. Yousem, R. J. Geckle, W. B. Bilker, H. Kroger, and R. L. Doty, “Posttraumatic smell loss: relationship of psychophysical tests and volumes of the olfactory bulbs and tracts and the temporal lobes,” Academic Radiology, vol. 6, no. 5, pp. 264–272, 1999. View at Google Scholar · View at Scopus
  61. D. Buschhüter, M. Smitka, S. Puschmann et al., “Correlation between olfactory bulb volume and olfactory function,” NeuroImage, vol. 42, no. 2, pp. 498–502, 2008. View at Publisher · View at Google Scholar · View at Scopus
  62. T. Hummel, M. Smitka, S. Puschmann, J. C. Gerber, B. Schaal, and D. Buschhüter, “Correlations between olfactory bulb volume and olfactory function in children and adolescents,” Experimental Brain Research, vol. 214, pp. 285–291, 2011. View at Google Scholar
  63. P. Rombaux, H. Potier, B. Bertrand, T. Duprez, and T. Hummel, “Olfactory bulb volume in patients with sinonasal disease,” American Journal of Rhinology, vol. 22, no. 6, pp. 598–601, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. V. Gudziol, D. Buschhüter, N. Abolmaali, J. Gerber, P. Rombaux, and T. Hummel, “Increasing olfactory bulb volume due to treatment of chronic rhinosinusitis-a longitudinal study,” Brain, vol. 132, no. 11, pp. 3096–3101, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. K. Wu, J. D. Howard, K. M. Phillips, D. Conley, and J. A. Gottfried, Odor Deprivation in the Human Brain, Society for Neuroscience Abstract, San Diego, Calif, USA, 2010.
  66. L. C. Katz and C. J. Shatz, “Synaptic activity and the construction of cortical circuits,” Science, vol. 274, no. 5290, pp. 1133–1138, 1996. View at Publisher · View at Google Scholar · View at Scopus
  67. L. C. Katz and M. Rubin, Keep your Brain Alive, Workman Publishing, New York, NY, USA, 1999.
  68. N. W. Daw, Visual Development, Springer, New York, NY, USA, 2006.
  69. C. R. Yu, J. Power, G. Barnea et al., “Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map,” Neuron, vol. 42, no. 4, pp. 553–566, 2004. View at Publisher · View at Google Scholar · View at Scopus
  70. P. C. Brunjes and M. J. Borror, “Unilateral odor deprivation: differential effects due to time of treatment,” Brain Research Bulletin, vol. 11, no. 5, pp. 501–503, 1983. View at Publisher · View at Google Scholar · View at Scopus
  71. J. R. Henegar and J. A. Maruniak, “Quantification of the effects of long-term unilateral naris closure on the olfactory bulbs of adult mice,” Brain Research, vol. 568, no. 1-2, pp. 230–234, 1991. View at Google Scholar · View at Scopus
  72. N. Mandairon, J. Sacquet, F. Jourdan, and A. Didier, “Long-term fate and distribution of newborn cells in the adult mouse olfactory bulb: influences of olfactory deprivation,” Neuroscience, vol. 141, no. 1, pp. 443–451, 2006. View at Publisher · View at Google Scholar · View at Scopus
  73. X. M. Zhang, K. Xiong, Y. Cai et al., “Functional deprivation promotes amyloid plaque pathogenesis in Tg2576 mouse olfactory bulb and piriform cortex,” European Journal of Neuroscience, vol. 31, no. 4, pp. 710–721, 2010. View at Publisher · View at Google Scholar · View at Scopus
  74. J. E Dahlen, D. A. Jimenez, R. C. Gerkin, and N. N. Urban, “Morphological analysis of activity-reduced adult-born neurons in the mouse olfactory bulb,” Frontiers in Neural Circuits. In press. View at Publisher · View at Google Scholar
  75. C. H. W. Leung and D. A. Wilson, “Trans-neuronal regulation of cortical apoptosis in the adult rat olfactory system,” Brain Research, vol. 984, no. 1-2, pp. 182–188, 2003. View at Publisher · View at Google Scholar · View at Scopus
  76. D. M. Cummings, H. E. Henning, and P. C. Brunjes, “Olfactory bulb recovery after early sensory deprivation,” Journal of Neuroscience, vol. 17, no. 19, pp. 7433–7440, 1997. View at Google Scholar · View at Scopus
  77. K. Fox and R. O. L. Wong, “A comparison of experience-dependent plasticity in the visual and somatosensory systems,” Neuron, vol. 48, no. 3, pp. 465–477, 2005. View at Publisher · View at Google Scholar · View at Scopus
  78. K. K. Gokoffski, S. Kawauchi, H. H. Wu et al., “Feedback regulation of neurogenesis in the mammalian olfactory epithelium: new insights from genetics and systems biology,” in The Neurobiology of Olfaction, A. Menini, Ed., chapter 10, CRC Press, Boca Raton, Fla, USA, 2010. View at Google Scholar
  79. F. Lazarini and P. M. Lledo, “Is adult neurogenesis essential for olfaction?” Trends in Neurosciences, vol. 34, no. 1, pp. 20–30, 2011. View at Publisher · View at Google Scholar · View at Scopus
  80. P. M. Lledo and A. Saghatelyan, “Integrating new neurons into the adult olfactory bulb: joining the network, life-death decisions, and the effects of sensory experience,” Trends in Neurosciences, vol. 28, no. 5, pp. 248–254, 2005. View at Publisher · View at Google Scholar · View at Scopus
  81. N. Sanai, T. Nguyen, R. A. Ihrie et al., “Corridors of migrating neurons in the human brain and their decline during infancy,” Nature, vol. 478, no. 7369, pp. 382–386, 2011. View at Google Scholar
  82. D. Krestel, D. Passe, J. C. Smith, and L. Jonsson, “Behavioral determination of olfactory thresholds to amyl acetate in dogs,” Neuroscience and Biobehavioral Reviews, vol. 8, no. 2, pp. 169–174, 1984. View at Publisher · View at Google Scholar · View at Scopus
  83. J. W. Hinds, P. L. Hinds, and N. A. McNelly, “An autoradiographic study of the mouse olfactory epithelium: evidence for long-lived receptors,” Anatomical Record, vol. 210, no. 2, pp. 375–383, 1984. View at Google Scholar · View at Scopus
  84. W. C. Watt, H. Sakano, Z. Y. Lee, J. E. Reusch, K. Trinh, and D. R. Storm, “Odorant stimulation enhances survival of olfactory sensory neurons via MAPK and CREB,” Neuron, vol. 41, no. 6, pp. 955–967, 2004. View at Publisher · View at Google Scholar · View at Scopus
  85. M. N. Batterton, D. Robarts, S. K. Woodley, and M. J. Baum, “Comparison of odor and mating-induced glomerular activation in the main olfactory bulb of estrous female ferrets,” Neuroscience Letters, vol. 400, no. 3, pp. 224–229, 2006. View at Publisher · View at Google Scholar · View at Scopus
  86. B. M. Slotnick and A. J. Pazos, “Rats with one olfactory bulb removed and the contralateral naris closed can detect odors,” Physiology & Behavior, vol. 48, no. 1, pp. 37–40, 1990. View at Publisher · View at Google Scholar · View at Scopus
  87. N. L. Hunt and B. M. Slotnick, “Functional capacity of the rat olfactory bulb after neonatal naris occlusion,” Chemical Senses, vol. 16, no. 2, pp. 131–142, 1991. View at Google Scholar · View at Scopus
  88. D. M. Coppola, J. A. Coltrane, and I. Arsov, “Retronasal or internasal olfaction can mediate odor-guided beaviors in newborn mice,” Physiology & Behavior, vol. 56, no. 4, pp. 729–736, 1994. View at Publisher · View at Google Scholar · View at Scopus
  89. C. J. Angely and D. M. Coppola, “How does long-term odor deprivation affect the olfactory capacity of adult mice?” Behavioral and Brain Functions, vol. 6, article 26, pp. i–ij, 2010. View at Publisher · View at Google Scholar · View at Scopus
  90. X. Grosmaitre, L. C. Santarelli, J. Tan, M. Luo, and M. Ma, “Dual functions of mammalian olfactory sensory neurons as odor detectors and mechanical sensors,” Nature Neuroscience, vol. 10, no. 3, pp. 348–354, 2007. View at Publisher · View at Google Scholar · View at Scopus
  91. M. L. Schaefer, B. Böttger, W. L. Silver, and T. E. Finger, “Trigeminal collaterals in the nasal epithelium and olfactory bulb: a potential route for direct modulation of olfactory information by trigeminal stimuli,” Journal of Comparative Neurology, vol. 444, no. 3, pp. 221–226, 2002. View at Publisher · View at Google Scholar · View at Scopus
  92. D. M. Coppola and C. Waggener, “The effects of unilateral naris occlusion on gene expression profiles in mouse olfactory mucosa,” Journal of Molecular Neuroscience. View at Publisher · View at Google Scholar
  93. J. A. Maruniak, P. J. Lin, and J. R. Henegar, “Effects of unilateral naris closure on the olfactory epithelia of adult mice,” Brain Research, vol. 490, no. 2, pp. 212–218, 1989. View at Google Scholar · View at Scopus
  94. J. A. Maruniak, J. R. Henegar, and T. P. Sweeney, “Effects of long-term unilateral naris closure on the olfactory epithelia of adult mice,” Brain Research, vol. 526, no. 1, pp. 65–72, 1990. View at Publisher · View at Google Scholar · View at Scopus
  95. M. Tos and C. Mogensen, “Changes of the nasal mucosa in altered airflow illustrated by blind quantitative histology,” Journal of Laryngology and Otology, vol. 92, no. 8, pp. 667–681, 1978. View at Google Scholar · View at Scopus
  96. M. Leon, “Compensatory responses to early olfactory restriction,” Annals of the New York Academy of Sciences, vol. 855, pp. 104–108, 1998. View at Google Scholar · View at Scopus
  97. K. M. Guthrie, J. M. Pullara, J. F. Marshall, and M. Leon, “Olfactory deprivation increases dopamine D2 receptor density in the rat olfactory bulb,” Synapse, vol. 8, no. 1, pp. 61–70, 1991. View at Google Scholar · View at Scopus
  98. W. J. Tyler, G. C. Petzold, S. K. Pal, and V. N. Murthy, “Experience-dependent modification of primary sensory synapses in the mammalian olfactory bulb,” Journal of Neuroscience, vol. 27, no. 35, pp. 9427–9438, 2007. View at Publisher · View at Google Scholar · View at Scopus
  99. G. G. Turrigiano and S. B. Nelson, “Homeostatic plasticity in the developing nervous system,” Nature Reviews Neuroscience, vol. 5, no. 2, pp. 97–107, 2004. View at Google Scholar · View at Scopus
  100. A. Waguespack, M. Reems, M. L. Butman, J. Cherry, and D. M. Coppola, “Olfactory receptor neurons have enhanced olfactory marker protein immunoreactivity in the nasal cavity ipsilateral to naris occlusion,” Brain Research, vol. 1044, no. 1, pp. 1–7, 2005. View at Google Scholar
  101. S. L. Youngentob and F. L. Margolis, “OMP gene deletion causes an elevation in behavioral threshold sensitivity,” NeuroReport, vol. 10, no. 1, pp. 15–19, 1999. View at Google Scholar · View at Scopus
  102. D. M. Coppola, A. M. Waguespack, M. R. Reems, M. L. Butman, and J. A. Cherry, “Naris occlusion alters transductory protein immunoreactivity in olfactory epithelium,” Histology and Histopathology, vol. 21, no. 4–6, pp. 487–501, 2006. View at Google Scholar · View at Scopus
  103. C. T. Waggener and D. M. Coppola, “Naris occlusion alters the electro-olfactogram: evidence for compensatory plasticity in the olfactory system,” Neuroscience Letters, vol. 427, no. 2, pp. 112–116, 2007. View at Publisher · View at Google Scholar · View at Scopus
  104. A. Mouret, G. Lepousez, J. Gras, M. M. Gabellec, and P. M. Lledo, “Turnover of newborn olfactory bulb neurons optimizes olfaction,” Journal of Neuroscience, vol. 29, no. 39, pp. 12302–12314, 2009. View at Publisher · View at Google Scholar · View at Scopus
  105. C. J. Wysocki, K. M. Dorries, and G. K. Beachamp, “Ability to perceive androstenone can be acquired by ostensibly anosmic people,” Proceedings of the National Academy of Sciences of the United States of America, vol. 86, no. 20, pp. 7976–7978, 1989. View at Google Scholar · View at Scopus
  106. H. W. Wang, C. J. Wysocki, and G. H. Gold, “Induction of olfactory receptor sensitivity in mice,” Science, vol. 260, no. 5110, pp. 998–1000, 1993. View at Google Scholar · View at Scopus
  107. K. K. Yee and C. J. Wysocki, “Odorant exposure increases olfactory sensitivity: olfactory epithelium is implicated,” Physiology & Behavior, vol. 72, no. 5, pp. 705–711, 2001. View at Google Scholar
  108. S. L. Youngentob and P. F. Kent, “Enhancement of odorant-induced mucosal activity patterns in rats trained on an odorant identification task,” Brain Research, vol. 670, no. 1, pp. 82–88, 1995. View at Publisher · View at Google Scholar · View at Scopus
  109. R. Hudson and H. Distel, “Induced peripheral sensitivity in the developing vertebrate olfactory system,” Annals of the New York Academy of Sciences, vol. 855, pp. 109–115, 1998. View at Google Scholar · View at Scopus
  110. D. A. Wilson and R. J. Stevenson, “Olfactory perceptual learning: the critical role of memory in odor discrimination,” Neuroscience and Biobehavioral Reviews, vol. 27, no. 4, pp. 307–328, 2003. View at Publisher · View at Google Scholar · View at Scopus
  111. M. M. Moreno, C. Linster, O. Escanilla, J. Sacquet, A. Didier, and N. Mandairon, “Olfactory perceptual learning requires adult neurogenesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 42, pp. 17980–17985, 2009. View at Publisher · View at Google Scholar · View at Scopus
  112. M. Stemmler and C. Koch, “How voltage-dependent conductances can adapt to maximize the information encoded by neuronal firing rate,” Nature Neuroscience, vol. 2, no. 6, pp. 521–527, 1999. View at Publisher · View at Google Scholar · View at Scopus
  113. D. Coppola and D. Purves, “The extraordinarily rapid disappearance of entoptic images,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 15, pp. 8001–8004, 1996. View at Publisher · View at Google Scholar · View at Scopus
  114. S. B. Laughlin, “The role of sensory adaptation in the retina,” Journal of Experimental Biology, vol. 146, pp. 39–62, 1989. View at Google Scholar · View at Scopus
  115. P. Dalton and C. J. Wysocki, “The nature and duration of adaptation following long-term odor exposure,” Perception and Psychophysics, vol. 58, no. 5, pp. 781–792, 1996. View at Google Scholar · View at Scopus
  116. D. M. Coppola and L. E. White, “Visual experience promotes the isotropic representation of orientation preference,” Visual Neuroscience, vol. 21, no. 1, pp. 39–51, 2004. View at Publisher · View at Google Scholar · View at Scopus
  117. L. E. White and D. Fitzpatrick, “Vision and cortical map development,” Neuron, vol. 56, no. 2, pp. 327–338, 2007. View at Google Scholar · View at Scopus