Abstract
Unilateral naris occlusion has been the method of choice for effecting stimulus deprivation in studies of olfactory plasticity. Early experiments emphasized the deleterious effects of this technique on the developing olfactory system while more recent studies have pointed to several apparently “compensatory” responses. However, the evidence for deprivation-induced compensatory processes in olfaction remains fragmentary. High-throughput methods such as microarray analysis can help fill the deficits in our understanding of naris occlusion as a mode of stimulus deprivation. Here we report for young adult mice the effects of early postnatal naris occlusion on the olfactory mucosal transcriptome using microarray analysis with RT–PCR confirmation. The transcripts of key genes involved in olfactory reception, transduction, and transmission were up-regulated in deprived-side olfactory mucosa, with opposite effects in non-deprived-side mucosa, compared to controls. Results support the hypothesis that odor environment triggers a previously unknown homeostatic control mechanism in olfactory receptor neurons designed to maximize information transfer.
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References
Angely C, Coppola DM (2010) How does long-term odor deprivation affect the olfactory capacity of adult mice? Behav Brain Funct 6(26):i–ij
Arechiga H, Alcocer-Cuaron C (1969) Adrenergic effects on the electro-olfactogram. Exp Med Surg 27:384–394
Bader A, Bautze V, Haid D, Breer H, Strotmann J (2010) Gene switching and odor induced activity shape expression of the OR37 family of olfactory receptor genes. Eur J Neurosci 32:1813–1824
Belluscio L, Gold GH, Nemes A, Axel R (1998) Mice deficient in Golf are anosmic. Neuron 20:69–81
Bennett MK, Kulaga HM, Reed RR (2010) Odor-evoked gene regulation and visualization in olfactory receptor neurons. Mol Cell Neurosci 43:353–362
Benson TE, Ryugo DK, Hinds JW (1984) Effects of sensory deprivation on the developing mouse olfactory system: a light and electron microscope morphometric analysis. J Neurosci 4:638–653
Brunjes PC (1994) Unilateral naris closure and olfactory system development. Brain Res Rev 19:146–160
Brunjes PC, Borror MJ (1983) Unilateral odor deprivation: differential effects due to time of onset. Brain Res Bull 11:501–503
Brunjes PC, Smith-Crafts LK, McCarty R (1985) Unilateral odor deprivation: effects on the development of olfactory bulb catecholamines and behavior. Dev Brain Res 22:1–6
Coppola DM (2008) The effect of stimulus deprivation on the olfactory system: a case of use it or find it! Chemosense 10(2):1–6
Coppola DM, Coltrane JA, Arsov I (1994) Retronasal or internasal olfaction can mediate odor-guided behaviors in newborn mice. Physiol Behav 56:729–736
Coppola DM, Waguespack A, Reems M, Butman ML, Cherry J (2006) Naris occlusion alters transductory protein immunoreactivity in olfactory epithelium. Histol Histopath 21:487–501
Ennis M, Hamilton KA, Hayar A (2007) Neurochemistry of the main olfactory system. In: Lajtha A (ed) Handbook of neurochemistry and molecular neurobiology, vol 20, 3rd edn. Springer, New York, pp 137–204
Farbman AI, Brunjes PC, Rentfro L, Michas J, Ritz S (1988) The effects of unilateral naris occlusion on cell dynamics in the developing rat olfactory epithelium. J Neurosci 8:3290–3295
Ferreira JA, Zwinderman AH (2006) On the Benjamini–Hochberg method. Ann Stat 34(4):1827–1849
Frazier-Cierpial LL, Brunjes PC (1989) Early postnatal cellular proliferation and survival in the olfactory bulb and rostral migratory stream of normal and unilaterally odor-deprived rats. J Comp Neurol 289:481–492
Guthrie KM, Pullara JM, Marshall JF, Leon M (1991) Olfactory deprivation increases dopamine D2 receptor density in the rat olfactory bulb. Synapse 8:61–70
Hall R. A. (2011) Autonomic modulation of olfactory signaling. Sci Signal 4, pe1.
Harris JA, Rubel EW (2006) Afferent regulation of neuron number in the cochlear nucleus: cellular and molecular analyses of a critical period. Hear Res 216–217:127–137
Huang DW, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nature Protoc 4(1):44–57
Hunt NL, Slotnick BM (1991) Functional capacity of the rat olfactory bulb after neonatal naris occlusion. Chem Senses 16(2):131–142
Katz LC, Shatz CJ (1996) Synaptic activity and the construction of cortical circuits. Science 274:1133–1138
Kawai F, Kurahashi T, Kaneko A (1999) Adrenaline enhances odorant contrast by modulating signal encoding in olfactory receptor cells. Nat Neurosci 2:133–138
Leon M (1998) Compensatory responses to early olfactory restriction. Ann NY Acad Sci 855:104–108
Li Y. R. and Matsunami H. (2011) Activation state of the M3 muscarinic acetylcholine receptor modulates mammalian odorant receptor signaling. Sci Signal 4, ra1
Maruniak JA, Lin PJ, Henagar JR (1989) Effects of unilateral naris closure on the olfactory epithelium of adult mice. Brain Res 490(2):212–218
Maruniak JA, Henagar JR, Sweeney TP (1990) Effects of long-term naris closure on the olfactory epithelium of adult mice. Brain Res 526(1):65–72
Meisami E (1976) Effects of olfactory deprivation on postnatal growth of the rat olfactory bulb utilizing a new method for production of neonatal unilateral anosmia. Brain Res 107:437–444
Miyamichi K, Serizawa S, Kimura HM, Sakano H (2005) Continuous and overlapping expression domains of odorant receptor genes in the olfactory epithelium determine the dorsal/ventral positioning of glomeruli in the olfactory bulb. J Neurosci 25(14):3586–3592
Rimbault M, Robin R, Vaysse A, Galbert F (2009) RNA profiles of rat olfactory epithelia: individual and age related variations. BMC Genomics 10:572
Saghatelyan A, Roux P, Migliore M, Rochefort C, Desmaisons D, Charneau P, Shepherd GM, Lledo P (2005) Activity-dependent adjustments of the inhibitory network in the olfactory bulb following early postnatal deprivation. Neuron 46:103–116
Sammeta N, Yu TT, Bose SC, McClintock TS (2007) Mouse olfactory sensory neurons express 10,000 genes. J Comp Neurol 502(6):1138–56
Schmitten TA, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nature Protoc 3(6):1101–1108
Semjidsuren GU, Im GJ, Lee SH, Park SJ, Hwang HY, Jung HH (2008) Differential gene expression profiles of the olfactory bulb after nasal obstruction in neonatal rats. Otolaryngol Head Neck Surg 138(5):648–54
Stemmler M, Koch C (1999) How voltage-dependent conductances can adapt to maximize the information encoded by neural firing rate. Nat Neurosci 2:521–527
Stephan AB, Shum EY, Hirsh S, Cygnar KD, Reisert J, Zhao H (2009) ANO2 is the cilial calcium-activated chloride channel that may mediate olfactory amplification. Proc Natl Acad Sci USA 106(28):11776–11781
Turrigiano GG (2008) The self-tuning neuron: synaptic scaling of excitatory synapses. Cell 135:422–435
Turrigiano GG, Nelson SB (2004) Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5:97–107
Tyler WJ, Petzold GC, Pal SK, Murthy VN (2007) Experience-dependent modification of primary sensory synapses in the mammalian olfactory bulb. J Neurosci 27:9427–9438
Waggener C, Coppola DM (2007) Naris occlusion alters the electro-olfactogram: evidence for compensatory plasticity in the olfactory system. Neurosci Lett 427:112–116
Waguespack A, Reems M, Butman ML, Cherry J, Coppola DM (2005) Olfactory receptor neurons have enhanced olfactory marker protein immunoreactivity in the nasal cavity ipsilateral to naris occlusion. Brain Res 1044(1):1–7
White L, Fitzpatrick D (2007) Visual and cortical map development. Neuron 56:327–338
Youngentob SL, Margolis FL (1999) OMP gene deletion causes an elevation in behavioral threshold sensitivity. Neuroreport 10:15–19
Yu CR, Power J, Barnea G, O’Donnell S, Brown HE, Osborne J, Axel R, Gogos JA (2004) Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map. Neuron 42:553–566
Zhang X, Firestein S (2002) The olfactory receptor gene superfamily in the mouse. Nat Neurosci 5(2):124–133
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Supported by NSF grant 0641433 (DMC). The authors would like to thank Jim Cherry for commenting on an earlier version of this manuscript.
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Coppola, D.M., Waggener, C.T. The Effects of Unilateral Naris Occlusion on Gene Expression Profiles in Mouse Olfactory Mucosa. J Mol Neurosci 47, 604–618 (2012). https://doi.org/10.1007/s12031-011-9690-4
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DOI: https://doi.org/10.1007/s12031-011-9690-4