Abstract
The removal of afferent input to the olfactory bulb by both cautery and chemical olfactory organ ablation in adult zebrafish results in a significant decrease in volume of the ipsilateral olfactory bulb. To examine the effects of deafferentation at a cellular level, primary output neurons of the olfactory bulb, the mitral cells, were investigated using retrograde tract tracing with fluorescent dextran using ex vivo brain cultures. Morphological characteristics including the number of major dendritic branches, total length of dendritic branches, area of the dendritic arbor, overall dendritic complexity, and optical density of the arbor were used to determine the effects of deafferentation on mitral cell dendrites. Following 8 weeks of permanent deafferentation there were significant reductions in the total length of dendritic branches, the area of the dendritic arbor, and the density of fine processes in the dendritic tuft. With 8 weeks of chronic, partial deafferentation there were significant reductions in all parameters examined, including a modified Sholl analysis that showed significant decreases in overall dendritic complexity. These results show the plasticity of mitral cell dendritic structures in the adult brain and provide information about the response of these output neurons following the loss of sensory input in this key model system.
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References
Baier H, Korsching S (1994) Olfactory glomeruli in the zebrafish form an invariant pattern and are identifiable across animals. J Neurosci 14:219–230
Baker H, Kawano T, Albert V, Joh TH, Reis DJ, Margolis FL (1984) Olfactory bulb dopamine neurons survive deafferentation-induced loss of tyrosine hydroxylase. Neuroscience 11:605–615
Baker H, Morel K, Stone DM, Maruniak JA (1993) Adult naris closure profoundly reduces tyrosine hydroxylase expression in mouse olfactory bulb. Brain Res 614:109–116
Bloomfield SA, Hitchcock PF (1991) Dendritic arbors of large-field ganglion cells show scaled growth during expansion of the goldfish retina: a study of morphometric and electronic properties. J Neurosci 11:910–917
Braubach OR, Fine A, Croll RP (2012) Distribution and functional organization of glomeruli in the olfactory bulbs of zebrafish (Danio rerio). J Comp Neurol 520:2317–2339
Brunjes PC (1985) Unilateral odor deprivation: time course of changes in laminar volume. Brain Res Bull 14:233–237
Brunjes PC (1994) Unilateral naris closure and olfactory system development. Brain Res Rev 19:146–160
Byrd CA (2000) Deafferentation-induced changes in the olfactory bulb of adult zebrafish. Brain Res 866:92–100
Byrd CA, Brunjes PC (2001) Neurogenesis in the olfactory bulb of adult zebrafish. Neuroscience 105:793–801
Casabona G, Catania MV, Sorto M, Ferraris N, Perroteau I, Fasolo A, Nicoletti F, Bovolin P (1998) Deafferentation up-regulates the expression of the mGluR1a metabotropic glutamate receptor protein in the olfactory bulb. Eur J Neurosci 10:771–776
Charych EI, Akum BF, Goldberg JS, Jornsten RJ, Rongo C, Zheng JQ, Firestein BL (2006) Activity-independent regulation of dendrite patterning by postsynaptic density protein PSD-95. J Neurosci 26:10164–10176
Chow DK, Groszer M, Pribadi M, Machniki M, Carmichael ST, Liu X, Trachtenberg JT (2009) Laminar and compartmental regulation of dendritic growth in mature cortex. Nat Neurosci 12:116–118
Coppola DM (2012) Studies of olfactory system neural plasticity: the contribution of the unilateral naris occlusion technique. Neural Plast 2012:351752
Corotto FS, Henegar JR, Maruniak JA (1994) Odor deprivation leads to reduced neurogenesis and reduced neuronal survival in the olfactory bulb of the adult mouse. Neuroscience 61:739–744
Couper Leo JM, Brunjes PC (2003) Neonatal focal denervation of the rat olfactory bulb alters cell structure and survival: a Golgi, Nissl, and confocal study. Dev Brain Res 140:277–286
Couper Leo JM, Devine AH, Brunjes PC (2000) Focal denervation alters cellular phenotypes and survival in the developing rat olfactory bulb. J Comp Neurol 417:325–336
Edwards JG, Michel WC (2002) Odor-stimulated glutamatergic neurotransmission in the zebrafish olfactory bulb. J Comp Neurol 454:294–309
Ehrlich M, Grillo M, Joh TH, Margolis FL, Baker H (1990) Transneuronal regulation of neuronal specific gene expression in the mouse olfactory bulb. Mol Brain Res 7:115–122
Ferraris N, Perroteau I, De Marchis S, Fasolo A, Bovolin P (1997) Glutamatergic deafferentation of olfactory bulb modulates the expression of mGluR1a mRNA. Neuroreport 8:1949–1953
Fuller CL, Villanueva R, Byrd CA (2005) Changes in glutamate receptor subunit 4 expression in the deafferented olfactory bulb of zebrafish. Brain Res 1044(2):251–261
Fuller CL, Yettaw HK, Byrd CA (2006) Mitral cells in the olfactory bulb of adult zebrafish Danio rerio: morphology and distribution. J Comp Neurol 499:218–230
Gemberling M, Bailey TJ, Hyde DR, Poss KD (2013) The zebrafish as a model for complex tissue regeneration. Trends Genet 29:611–620
Harding JW, Getchell TV, Margolis FL (1978) Denervation of the primary olfactory pathway in mice. V. Long-term effect of intranasal ZnSO4 irrigation on behavior, biochemistry and morphology. Brain Res 14:271–285
Hansen A, Zielinski BS (2005) Diversity in the olfactory epithelium of bony fishes: development, lamellar arrangement, sensory neuron cell types and transduction components. J Neurocytol 34(3–5):183–208
Henegar JR, Maruniak JA (1991) Quantification of the effects of long-term unilateral naris closure on the olfactory bulbs of adult mice. Brain Res 568:230–234
Holtmaat AJ, Trachtenberg JT, Wilbrecht L (2005) Transient and persistent dendritic spines in the neocortex in vivo. Neuron 45:279–291
Iqbal T, Byrd-Jacobs C (2010) Rapid degeneration and regeneration of the zebrafish olfactory epithelium after triton X-100 application. Chem Senses 35:351–361
Kosaka K, Aika Y, Toida K, Koska T (2001) Structure of intraglomerular dendritic tufts of mitral cells and their contacts with olfactory nerve terminals and calbindin-immunoreactive type 2 periglomerular neurons. J Comp Neurol 440:219–235
Lee S, Stevens CF (2007) General design principle for scalable neural circuits in a vertebrate retina. Proc Natl Acad Sci U S A 104:12931–12935
Lee KW, Kim Y, Kim AM, Helmin K, Naim AC, Greengard P (2006) Cocaine-induced dendritic spine formation in D1 and D2 dopamine receptor-containing medium spiny neurons in nucleus accumbens. PNAS 103:3399–3404
Lledo PM, Gheusi G, Vincent JD (2005) Information processing in the mammalian olfactory system. Physiol Rev 85:281–317
Lopez-Mascaraque L, Garcia C, Blanchart A, De Carlos JA (2004) Olfactory epithelium influences the orientation of mitral cell dendrites during development. Dev Dyn 232:325–335
Margolis FL, Roberts N, Ferriero D, Feldman J (1974) Denervation in the primary olfactory pathway of mice: biochemical and morphological effects. Brain Res 81:469–483
Matsutani S, Yamamoto N (2000) Differentiation of mitral cell dendrites in the developing main olfactory bulbs of normal and naris-occluded rats. J Comp Neurol 418:402–410
Matthews MR, Powell TPS (1962) Some observations on transneuronal cell degeneration in the olfactory bulb of the rabbit. J Anat 96:89–102
Meisami E, Safari L (1991) 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 Res 221:81–107
Mizrahi A, Katz LC (2003) Dendritic stability in the adult olfactory bulb. Nat Neurosci 6(11):1201–1207
Nadi NS, Head R, Grillo M, Hempstead J, Grannot-Reisfeld N, Margolis FL (1981) Chemical deafferentation of the olfactory bulb: plasticity of the levels of tyrosine hydroxylase, dopamine and norepinephrine. Brain Res 213:365–377
Oberto M, Soncin I, Bovolin P, Voyron S, De Bortoli M, Dati C, Fasolo A (2001) I. Perroteau, ErbB-4 and neuregulin expression in the adult mouse olfactory bulb after peripheral deafferentation. Eur J Neurosci 14:513–521
Parrish JZ, Emoto K, Kim MD, Jan YN (2007) Mechanisms that regulate establishment, maintenance, and remodeling of dendritic fields. Annu Rev Neurosci 30:399–423
Paskin TR, Byrd-Jacobs CA (2012) Reversible deafferentation of the adult zebrafish olfactory bulb affects glomerular distribution and olfactory–mediated behavior. Behav Brain Res 235:293–301
Paskin TR, Iqbal TR, Byrd-Jacobs CA (2011) Olfactory bulb recovery following reversible deafferentation with repeated detergent application in the adult zebrafish. Neuroscience 196:276–284
Poling KR, Brunjes PC (2000) Sensory deafferentation and olfactory bulb morphology in the zebrafish and related species. Brain Res 856(1–2):135–141
Schaefer J, Ryan A (2006) Developmental plasticity in the thermal tolerance of zebrafish Dani rerio. Fish Biol 69:722–734
Schindelin J, Arganda-Carreras I, Frise E (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682
Sholl DA (1953) Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat 87:387–406
Sirbulescu RF, Zupanc GKH (2009) Dynamics of caspase-3-mediated apoptosis during spinal cord regeneration in the teleost fish, apteronotus leptorhynchus. Brain Res 1304:14–25
Stone DM, Grillo M, Margolis FL, Joh TH, Baker H (1991) Differential effect of functional olfactory bulb deafferentation on tyrosine hydroxylase and glutamic acid decarboxylase messenger RNA levels in rodent juxtaglomerular neurons. J Comp Neurol 311:223–233
Tomizawa K, Kunieda J, Nakayasu H (2001) Ex vivo culture of isolated zebrafish whole brain. J Neurosci Methods 107:31–38
Tran H, Chen H, Walz A, Posthumus JC, Gong Q (2008) Influence of olfactory epithelium on mitral/tufted cell dendritic outgrowth. PLoS One 3:e3816
Trimpe DM, Byrd-Jacobs CA (2016) Patterns of olfactory bulb neurogenesis in the adult zebrafish are altered following reversible deafferentation. Neuroscience 331:134–147
Vankirk AM, Byrd CA (2003) Apoptosis following peripheral sensory deafferentation in the olfactory bulb of adult zebrafish. J Comp Neurol 455:488–498
Villanueva R, Byrd-Jacobs CA (2009) Peripheral sensory deafferentation affects olfactory bulb neurogenesis in zebrafish. Brain Res 1269:31–39
White EJ, Kounelis SK, Byrd-Jacobs CA (2015) Plasticity of glomeruli and olfactory-mediated behavior in zebrafish following detergent lesioning of the olfactory epithelium. Neuroscience 284:622–631
Wilson D, Wood JG (1992) Functional consequences of unilateral olfactory deprivation: time-course and age sensitivity. Neuroscience 49(1):183–192
Wong ROL, Gosh A (2002) Activity-dependent regulation of dendritic growth and patterning. Nature Rev 3:803–812
Zippel HP, von Rekowski C (1993) In goldfish the qualitative discriminative ability for odors rapidly returns after bilateral nerve axotomy and lateral olfactory tract transection. Brain Res 618:338–340
Acknowledgements
We are grateful to the Western Michigan University Biological Imaging Center for the use of the confocal microscope and Natalie K. Hamilton for her technical assistance.
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Supported by National Institutes of Health-NIDCD grants #04262 and #011137 (CBJ).
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Pozzuto, J.M., Fuller, C.L. & Byrd-Jacobs, C.A. Deafferentation-induced alterations in mitral cell dendritic morphology in the adult zebrafish olfactory bulb. J Bioenerg Biomembr 51, 29–40 (2019). https://doi.org/10.1007/s10863-018-9772-x
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DOI: https://doi.org/10.1007/s10863-018-9772-x