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1

Vogt, R. G., S. M. Lindsay, C. A. Byrd, and M. Sun. "Spatial patterns of olfactory neurons expressing specific odor receptor genes in 48-hour-old embryos of zebrafish Danio rerio." Journal of Experimental Biology 200, no. 3 (February 1, 1997): 433–43. http://dx.doi.org/10.1242/jeb.200.3.433.

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Olfactory neurons have a complex phenotype characterized by their expression of a specific odor receptor (OR) gene and their targeting of an equally specific locus in the olfactory bulb. In the adult fish, olfactory neurons expressing specific ORs are broadly distributed in the epithelium, intermingling with neurons expressing other OR phenotypes. This distributed adult pattern has led to the suggestion that olfactory neuron phenotype is determined by a stochastic process, independent of external positional cues. However, when the fish olfactory system is established during embryogenesis it is simple in its organization, with few olfactory neurons and an olfactory epithelium that has not yet folded into the adult morphology. It is possible that positional cues might act in the embryo to establish an initial population and pattern of olfactory neuron phenotypes and that subsequent morphogenesis and neuronal addition lead to the randomized distribution of neurons. To test this possibility, we examined the spatial patterns of olfactory neurons expressing specific OR genes in 48 h embryos, a time of relative simplicity in the developing olfactory epithelium. Three-dimensional plots of neuron distributions were made, and comparison of OR expression patterns were made between right and left epithelia, between individual animals and between different OR genes. The patterns of OR gene expression were not conserved in these comparison. Mathematical analysis of 21 epithelia for the degree of order in the distribution of olfactory neurons argued strongly that the neurons expressing given ORs are randomly distributed in the 48 h embryos. These results are consistent with those observed from adult tissue and support models suggesting that extrinsic positional cues do not have a major role in specifying olfactory neuron phenotypes.
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2

Ohta, Yasushi, Nobuko Marino, Minako Takanosawa, Shinichi Ishimoto, Chiori Matumoto, and Keiichi Ichimura. "High-Dose Glucocorticoids Inhibit Proliferation of Rat Olfactory Epithelium." Annals of Otology, Rhinology & Laryngology 111, no. 10 (October 2002): 909–11. http://dx.doi.org/10.1177/000348940211101008.

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Glucocorticoids (GCs) are commonly prescribed for treatment of olfactory dysfunction. However, the effects of GCs on olfactory epithelium are not well known. We investigated the effects of high-dose GCs on proliferating cells of olfactory epithelium. Five adult male rats (300 g) received a single daily subcutaneous dose of vehicle containing 0.3 mg dexamethasone (DEX) for 9 days (DEX+ group), and a control group received vehicle alone (DEX– group). We compared sections from the Two groups for numbers of Ki67-positive cells. The mean number of Ki67-positive cells per 500 olfactory epithelial cells was 9.6 for the DEX+ group and 58 for the DEX– group (significant difference). We conclude that high-dose GC suppressed proliferation of olfactory epithelium. We suggest that high-dose GC suppresses cytokines and growth factors, resulting in secondary suppression of proliferating ability.
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3

Menco, B. P., and A. I. Farbman. "Genesis of cilia and microvilli of rat nasal epithelia during pre-natal development. I. Olfactory epithelium, qualitative studies." Journal of Cell Science 78, no. 1 (October 1, 1985): 283–310. http://dx.doi.org/10.1242/jcs.78.1.283.

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Rat foetuses from intra-uterine days E13 through E22 (day before parturition) and adults were used for a qualitative electron-microscopic investigation of the development of ciliated/microvillous surfaces of the olfactory epithelium. In the E13 and most of the E14 embryos the epithelial surface is not yet characteristically olfactory. Apical cell profiles show primary cilia. These can arise at the epithelial surface or below. From E14 onwards the epithelial surface acquires olfactory characteristics. Dendritic endings of the olfactory receptor cells can be found amidst microvillous profiles of supporting cells. Either cell type may bear primary cilia. From E16 onwards the receptor cells sprout multiple olfactory cilia, but cells with primary cilia are found throughout pre-natal development. These primary cilia are, at least for a while, retained during the formation of the secondary cilia. Primary cilia always have distinct necklaces at their base. Otherwise, especially with respect to their tips, their morphology can vary. Originally they have expanded tips (up to E14); later on such wide tips are no longer encountered (E16 and E17). Primary cilia of receptor cells never have wide tips. Appreciable numbers of endings with tapering olfactory cilia are discerned around E18 and especially E19. Throughout pre-natal development posterior/superior parts of the septal olfactory epithelium are more precocious than anterior/inferior parts, in particular in the region of transition with the respiratory epithelium. This advance in development includes total densities of dendritic endings of olfactory receptor cells, densities of multiciliated endings alone and lengths of supporting cell microvilli. This difference is discussed with respect to the topography of the olfactory epithelial surface in adult animals. In addition to the systematic topographic variation, a number of more local, apparently not-systematically distributed, topographic variations present during development are described. Most of these also occur in adult animals and they include heterogeneity in length of supporting cell microvilli and the presence of patches of supporting cells with rounded apical protuberances, of patches displaying dendrites with polyaxonemes rather than individual cilia and of scattered atypical cells (neither typical olfactory receptor nor olfactory supporting cells). At their surfaces such atypical cells can resemble inner-ear hair cells. Relative to olfactory receptor and supporting cells there are only very few atypical cells.(ABSTRACT TRUNCATED AT 400 WORDS)
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4

Feron, F., J. Bianco, I. Ferguson, and A. Mackay-Sim. "Neurotrophin expression in the adult olfactory epithelium." Brain Research 1196 (February 2008): 13–21. http://dx.doi.org/10.1016/j.brainres.2007.12.003.

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5

Hegg, Colleen C., Edmund Au, A. Jane Roskams, and Mary T. Lucero. "PACAP Is Present in the Olfactory System and Evokes Calcium Transients in Olfactory Receptor Neurons." Journal of Neurophysiology 90, no. 4 (October 2003): 2711–19. http://dx.doi.org/10.1152/jn.00288.2003.

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Pituitary adenylate cyclase activating peptide (PACAP), a neuroregulatory peptide, is found in germinative regions of the CNS, including the olfactory bulb, throughout adulthood. We show that 1) PACAP immunoreactivity is also present in the neonatal mouse and adult mouse and rat olfactory epithelium, 2) PACAP expression pattern differs between neonatal and adult mice, and 3) PACAP is produced by olfactory ensheathing cells. PACAP may thus be a key factor in the uniquely supportive role of olfactory ensheathing cells in regeneration of neurons from olfactory epithelium and lesioned spinal cord. Using calcium imaging, we demonstrated physiological responses to PACAP in both neonatal and adult olfactory receptor neurons (ORNs). We propose that PACAP plays an important role in normal turnover of ORNs by providing neurotrophic support during development and regeneration and neuroprotective support of mature neurons.
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6

Weiss, Lukas, Paola Segoviano Arias, Thomas Offner, Sara Joy Hawkins, Thomas Hassenklöver, and Ivan Manzini. "Distinct interhemispheric connectivity at the level of the olfactory bulb emerges during Xenopus laevis metamorphosis." Cell and Tissue Research 386, no. 3 (September 28, 2021): 491–511. http://dx.doi.org/10.1007/s00441-021-03527-3.

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AbstractDuring metamorphosis, the olfactory system of anuran tadpoles undergoes substantial restructuring. The main olfactory epithelium in the principal nasal cavity of Xenopus laevis tadpoles is associated with aquatic olfaction and transformed into the adult air-nose, while a new adult water-nose emerges in the middle cavity. Impacts of this metamorphic remodeling on odor processing, behavior, and network structure are still unexplored. Here, we used neuronal tracings, calcium imaging, and behavioral experiments to examine the functional connectivity between the epithelium and the main olfactory bulb during metamorphosis. In tadpoles, olfactory receptor neurons in the principal cavity project axons to glomeruli in the ventral main olfactory bulb. These projections are gradually replaced by receptor neuron axons from the newly forming middle cavity epithelium. Despite this reorganization in the ventral bulb, two spatially segregated odor processing streams remain undisrupted and behavioral responses to waterborne odorants are unchanged. Contemporaneously, new receptor neurons in the remodeling principal cavity innervate the emerging dorsal part of the bulb, which displays distinct wiring features. Glomeruli around its midline are innervated from the left and right nasal epithelia. Additionally, postsynaptic projection neurons in the dorsal bulb predominantly connect to multiple glomeruli, while half of projection neurons in the ventral bulb are uni-glomerular. Our results show that the “water system” remains functional despite metamorphic reconstruction. The network differences between the dorsal and ventral olfactory bulb imply a higher degree of odor integration in the dorsal main olfactory bulb. This is possibly connected with the processing of different odorants, airborne vs. waterborne.
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7

Diaz, J. P., M. Prié-Granié, C. Blasco, T. Noëll, and R. Connes. "Ultrastructural study of the olfactory organ in adult and developing European sea bass, Dicentrarchus labrax." Canadian Journal of Zoology 80, no. 9 (September 1, 2002): 1610–22. http://dx.doi.org/10.1139/z02-162.

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The olfactory organ of the European sea bass (Dicentrarchus labrax) in adults and during development has been studied by light microscopy and by transmission and scanning electron microscopy. This organ includes two cavities, each extended by an accessory sac and opening to the outside through two nostrils. It contains a rosette consisting of about forty lamellae. The olfactory epithelium is characterized by the presence of two types of receptor cells, ciliated or with microvilli, and numerous ciliated nonsensory cells. Rod cells, essentially found in the altered epithelia of farmed bass, and rodlet cells are also observed. The olfactory organ forms very early in the developmental process. Two olfactory pits holding both types of sensory receptors appear 24 h before hatching. The ciliated nonsensory cells only appear at the end of the endotrophic period, shortly before the mouth opens. Although it is rather unspectacular during the larval stage, the development of the olfactory organ is characterized at the start of the juvenile stage by three important events: the formation of the nostrils, the hollowing of the accessory sacs, and the development of the rosette. This is created by raising the floor of the cavity and forming successive folds, which are the lamellae where the sensory epithelium is found.
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8

Murrell, W., G. Bushell, J. McGrath, P. Bates, and A. Mackay-Sim. "Neurogenesis in vitro of adult human olfactory epithelium." Schizophrenia Research 18, no. 2-3 (February 1996): 178–79. http://dx.doi.org/10.1016/0920-9964(96)85563-0.

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9

Suzuki, Yuko, and Masako Takeda. "Observation of basal cells in the olfactory epithelium after axotomy." Proceedings, annual meeting, Electron Microscopy Society of America 48, no. 3 (August 12, 1990): 334–35. http://dx.doi.org/10.1017/s0424820100159229.

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In the olfactory epithelium of mice, cytokeratin was present in the basal cells but not in the olfactory cells. Our previous study using antikeratin antibodies showed that the basal cells were columnar or pyramidal in shape in the early postnatal period, but became flat in adult mice. In this study, structural changes of the basal cells after axotomy were investigated by immunohistochemistry, transmission electron microscopy (TEM), and scanning electron microscopy (SEM).The unilateral olfactory nerves of adult mice were sectioned at the level of the lamina cribrosa. The mice were sacrificed 4, 8-10, and 14 days postoperatively. The olfactory mucosae were removed, frozen with freon 22, and cut on a cryostat at 10 μm. The sections were stained by the PAP method using a PAP kit. The antikeratin antibody (PKK 2) against pig kidney epithelial cell line, which reacts with 40, 46, 48, and 54 kd subunits (Immunotech), was used. To label the dividing cells, bromodeoxyuridine (BrdU) was administered to mice each postoperative day 1 hour before sacrificing. The presence of BrdU was detected imrnunohistochemically using anti-BrdU antibody (Becton-Dickinson).
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10

Franco, Marie-Dominique, Michael P. Pape, Jennifer J. Swiergiel, and Gail D. Burd. "Differential and overlapping expression patterns of X-dll3 and Pax-6 genes suggest distinct roles in olfactory system development of the African clawed frog Xenopus laevis." Journal of Experimental Biology 204, no. 12 (June 15, 2001): 2049–61. http://dx.doi.org/10.1242/jeb.204.12.2049.

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SUMMARY In Xenopus laevis, the formation of the adult olfactory epithelium involves embryonic, larval and metamorphic phases. The olfactory epithelium in the principal cavity (PC) develops during embryogenesis from the olfactory placode and is thought to respond to water-borne odorants throughout larval life. During metamorphosis, the PC undergoes major transformations and is exposed to air-borne odorants. Also during metamorphosis, the middle cavity (MC) develops de novo. The olfactory epithelium in the MC has the same characteristics as that in the larval PC and is thought to respond to water-borne odorants. Using in situ hybridization, we analyzed the expression pattern of the homeobox genes X-dll3 and Pax-6 within the developing olfactory system. Early in development, X-dll3 is expressed in both the neuronal and non-neuronal ectoderm of the sense plate and in all cell layers of the olfactory placode and larval PC. Expression becomes restricted to the neurons and basal cells of the PC by mid-metamorphosis. During metamorphosis, X-dll3 is also expressed throughout the developing MC epithelium and becomes restricted to neurons and basal cells at metamorphic climax. This expression pattern suggests that X-dll3 is first involved in the patterning and genesis of all cells forming the olfactory tissue and is then involved in neurogenesis or neuronal maturation in putative water- and air-sensing epithelia. In contrast, Pax-6 expression is restricted to the olfactory placode, larval PC and metamorphic MC, suggesting that Pax-6 is specifically involved in the formation of water-sensing epithelium. The expression patterns suggest that X-dll3 and Pax-6 are both involved in establishing the olfactory placode during embryonic development, but subtle differences in cellular and temporal expression patterns suggest that these genes have distinct functions.
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11

Sarnat, Harvey B., and Laura Flores-Sarnat. "Olfactory Development, Part 2: Neuroanatomic Maturation and Dysgeneses." Journal of Child Neurology 32, no. 6 (February 19, 2017): 579–93. http://dx.doi.org/10.1177/0883073816685192.

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Olfactory axons project from nasal epithelium to the primitive telencephalon before olfactory bulbs form. Olfactory bulb neurons do not differentiate in situ but arrive via the rostral migratory stream. Synaptic glomeruli and concentric laminar architecture are unlike other cortices. Fetal olfactory maturation of neuronal differentiation, synaptogenesis, and myelination remains incomplete at term and have a protracted course of postnatal development. The olfactory ventricular recess involutes postnatally but dilates in congenital hydrocephalus. Olfactory bulb, tract and epithelium are repositories of progenitor stem cells in fetal and adult life. Diverse malformations of the olfactory bulb can be diagnosed by clinical examination, imaging, and neuropathologically. Cellular markers of neuronal differentiation and synaptogenesis demonstrate immaturity of the olfactory system at birth, previously believed by histology alone to occur early in fetal life. Immaturity does not preclude function.
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12

Goldstein, Bradley J., Hengsheng Fang, Steven L. Youngentob, and James E. Schwob. "Transplantation of multipotent progenitors from the adult olfactory epithelium." NeuroReport 9, no. 7 (May 1998): 1611–17. http://dx.doi.org/10.1097/00001756-199805110-00065.

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13

Newman, M. P., F. Féron, and A. Mackay-Sim. "Growth factor regulation of neurogenesis in adult olfactory epithelium." Neuroscience 99, no. 2 (September 2000): 343–50. http://dx.doi.org/10.1016/s0306-4522(00)00194-9.

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14

Guo, Zhen, Adam Packard, Richard C. Krolewski, Margaret T. Harris, Glen L. Manglapus, and James E. Schwob. "Expression of Pax6 and Sox2 in adult olfactory epithelium." Journal of Comparative Neurology 518, no. 21 (July 26, 2010): 4395–418. http://dx.doi.org/10.1002/cne.22463.

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15

Minovi, Amir, Tobias Dombrowski, Martin Brüne, Stefan Dazert, and Georg Juckel. "Olfactory function and morphology of olfactory epithelium in an adult population with schizophrenia." Schizophrenia Research 161, no. 2-3 (February 2015): 513–14. http://dx.doi.org/10.1016/j.schres.2014.11.023.

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16

Aragona, Marialuisa, Caterina Porcino, Maria Cristina Guerrera, Giuseppe Montalbano, Rosaria Laurà, Maria Levanti, Francesco Abbate, et al. "Localization of BDNF and Calretinin in Olfactory Epithelium and Taste Buds of Zebrafish (Danio rerio)." International Journal of Molecular Sciences 23, no. 9 (April 23, 2022): 4696. http://dx.doi.org/10.3390/ijms23094696.

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Brain-derived neurotrophic factor (BDNF) is a member of the neurotrophin family and it is involved in several fundamental functions in the central and peripheral nervous systems, and in sensory organs. BDNF regulates the chemosensory systems of mammals and is consistently expressed in those organs. In zebrafish, the key role of BDNF in the biology of the hair cells of the inner ear and lateral line system has recently been demonstrated. However, only some information is available about its occurrence in the olfactory epithelium, taste buds, and cutaneous isolated chemosensory cells. Therefore, this study was undertaken to analyze the involvement of BDNF in the chemosensory organs of zebrafish during the larval and adult stages. To identify cells displaying BDNF, we compared the cellular pattern of BDNF-displaying cells with those immunoreactive for calretinin and S100 protein. Our results demonstrate the localization of BDNF in the sensory part of the olfactory epithelium, mainly in the ciliated olfactory sensory neurons in larvae and adult zebrafish. Intense immunoreaction for BDNF was also observed in the chemosensory cells of oral and cutaneous taste buds. Moreover, a subpopulation of olfactory sensory neurons and chemosensory cells of olfactory rosette and taste bud, respectively, showed marked immunopositivity for calcium-binding protein S100 and calretinin. These results demonstrate the possible role of BDNF in the development and maintenance of olfactory sensory neurons and sensory cells in the olfactory epithelium and taste organs of zebrafish during all stages of development.
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Dávila-Vera, Delsy, Rosa Virginia Mendoza-Briceño, Henry Andrade-Ruiz, Zulma Peña-Contreras, Yzoleth Torres-Vielma, Emilitza Labarca-Villasmil, Leisalba Zavala-Morillo, José Gregorio Peña, Beluardi Sánchez-Gil, and Yulianny Vergara-Dávila. "Modifications in the olfactory mucosa of young adult mice exposed to cigarette smoke." Anales de Biología, no. 44 (July 7, 2022): 71–80. http://dx.doi.org/10.6018/analesbio.44.07.

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Se analizaron las alteraciones ocasionados por el humo de cigarrillo en la mucosa olfatoria, haciendo énfasis en el epitelio olfatorio, en ratones NMRI adultos jóvenes distribuidos en un grupo control y cuatro grupos experimentales expuestos al humo de cigarrillo a distintas dosis y tiempos. El efecto de los tóxicos presentes en el humo de cigarrillo, durante el tiempo de exposición experimentalmente programado, produjo leves modificaciones de la citoarquitectura epitelial como son la distribución irregular de las células y el desplazamiento de un alto porcentaje de ellas hacia la superficie; así como un incremento de la producción de sustancia mucosa verificada por microscopía óptica y de barrido, lo cual afecta la actividad normal del epitelio olfatorio. The alterations caused by cigarette smoke in the olfactory mucosa were analyzed, with emphasis on the olfactory epithelium, in young adult NMRI mice distributed in a control group and four experimental groups exposed to cigarette smoke at different doses and times. The effect of the toxins present in cigarette smoke, during the experimentally programmed exposure time, produced slight modifications of the epithelial cytoarchitecture, such as the irregular distribution of the cells and the displacement of a high percentage of them towards the surface; as well as an increase in the production of mucous substance verified by optical and scanning microscopy, which affects the normal activity of the olfactory epithelium.
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18

Menco, B. P., and A. I. Farbman. "Genesis of cilia and microvilli of rat nasal epithelia during pre-natal development. II. Olfactory epithelium, a morphometric analysis." Journal of Cell Science 78, no. 1 (October 1, 1985): 311–36. http://dx.doi.org/10.1242/jcs.78.1.311.

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Rat foetuses from intra-uterine days E14 through E22 (day before parturition) and adults were used for a quantitative scanning electron-microscopic examination of ciliogenesis in olfactory receptor cells and microvillogenesis in olfactory supporting cells. Four developmental stages in olfactory ciliogenesis can be discerned. Two of these are characterized by the presence of primary cilia only, the other two concern outgrowth in number and length of secondary cilia. (1) Primary cilia on undifferentiated cells; this stage occurs up to E14. (2) Primary cilia on differentiating olfactory receptor and also olfactory supporting cells. This stage begins at E14 and lasts, for the olfactory receptor cells, at least up to E22. On the supporting cells primary cilia are rarely observed after E18. Virtually all primary cilia are about 1 micron long. Up to E21 dendritic endings with primary cilia occur more frequently than those with any other number of cilia; all endings have a transitional stage in which they bear primary cilia only. (3) Secondary olfactory cilia increase in number. From E16 onwards the cells become multiciliated. Beginning at this stage and continuing up to E22 an average of one cilium per day is added to the endings. At E22 the average number of cilia observed per ending is about 70% of that in adults; more than 90% of the endings are multiciliated. From E15 to E22 the exchange rate between receptor cells with only primary cilia and multiciliated cells is about 0.5 X 10(6) cells/cm2 per day. When considered in the light of electrophysiological data on developing rats, our data suggest that when the cells have just primary cilia, they may respond indiscriminately to all odorants, whereas multiciliated cells display odorant specificity. (4) Secondary olfactory cilia increase in length. From E14 to E19 and over the whole population of receptor cells the cilia grow at an average rate of about 0.5 micron/day. Proximal parts of olfactory cilia are longer than primary cilia; olfactory cilia begin to taper in increasing numbers around E18. At E19 the receptive membrane surface, i.e. regions of the cells facing the nasal lumen, of individual cells is about 8%, and the increase in epithelial surface due to sprouting of cilia is 5% of such values in adult animals. Concomitant with the onset of tapering of olfactory cilia, i.e. around E18, microvilli of supporting cells show a spurt in growth from about 0.4 micron to about 1.3 micron. Unlike olfactory cilia they show no growth, on average, after E19.(ABSTRACT TRUNCATED AT 400 WORDS)
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19

Sarnat, Harvey B., Laura Flores-Sarnat, and Xing-Chang Wei. "Olfactory Development, Part 1: Function, From Fetal Perception to Adult Wine-Tasting." Journal of Child Neurology 32, no. 6 (February 19, 2017): 566–78. http://dx.doi.org/10.1177/0883073817690867.

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Discrimination of odorous molecules in amniotic fluid occur after 30 weeks’ gestation; fetuses exhibit differential responses to maternal diet. Olfactory reflexes enable reliable neonatal testing. Olfactory bulbs can be demonstrated reliably by MRI after 30 weeks’ gestation, and their hypoplasia or aplasia also documented by late prenatal and postnatal MRI. Olfactory axons project from nasal epithelium to telencephalon before olfactory bulbs form. Fetal olfactory maturation remains incomplete at term for neuronal differentiation, synaptogenesis, myelination, and persistence of the transitory fetal ventricular recess. Immaturity does not signify nonfunction. Olfaction is the only sensory system without thalamic projection because of its own intrinsic thalamic equivalent. Diverse malformations of the olfactory bulb can be diagnosed by clinical examination, imaging, and neuropathology. Some epileptic auras might be primarily generated in the olfactory bulb. Cranial nerve 1 should be tested in all neonates and especially in patients with brain malformations, endocrinopathies, chromosomopathies, and genetic/metabolic diseases.
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20

Morrison, Filomene G., Brian G. Dias, and Kerry J. Ressler. "Extinction reverses olfactory fear-conditioned increases in neuron number and glomerular size." Proceedings of the National Academy of Sciences 112, no. 41 (September 29, 2015): 12846–51. http://dx.doi.org/10.1073/pnas.1505068112.

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Although much work has investigated the contribution of brain regions such as the amygdala, hippocampus, and prefrontal cortex to the processing of fear learning and memory, fewer studies have examined the role of sensory systems, in particular the olfactory system, in the detection and perception of cues involved in learning and memory. The primary sensory receptive field maps of the olfactory system are exquisitely organized and respond dynamically to cues in the environment, remaining plastic from development through adulthood. We have previously demonstrated that olfactory fear conditioning leads to increased odorant-specific receptor representation in the main olfactory epithelium and in glomeruli within the olfactory bulb. We now demonstrate that olfactory extinction training specific to the conditioned odor stimulus reverses the conditioning-associated freezing behavior and odor learning-induced structural changes in the olfactory epithelium and olfactory bulb in an odorant ligand-specific manner. These data suggest that learning-induced freezing behavior, structural alterations, and enhanced neural sensory representation can be reversed in adult mice following extinction training.
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21

Jia, Cuihong, and Colleen Cosgrove Hegg. "NPY mediates ATP-induced neuroproliferation in adult mouse olfactory epithelium." Neurobiology of Disease 38, no. 3 (June 2010): 405–13. http://dx.doi.org/10.1016/j.nbd.2010.02.013.

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22

Sülz, Lorena, Guadalupe Astorga, Bernadette Bellette, Rodrigo Iturriaga, Alan Mackay-Sim, and Juan Bacigalupo. "Nitric oxide regulates neurogenesis in adult olfactory epithelium in vitro." Nitric Oxide 20, no. 4 (June 2009): 238–52. http://dx.doi.org/10.1016/j.niox.2009.01.004.

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23

Wolozin, Benjamin, Trey Sunderland, Bin-bin Zheng, James Resau, Bernard Dufy, Jeffrey Barker, Richard Swerdlow, and Hayden Coon. "Continuous culture of neuronal cells from adult human olfactory epithelium." Journal of Molecular Neuroscience 3, no. 3 (September 1992): 137–46. http://dx.doi.org/10.1007/bf02919405.

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24

Schwob, JE, NB Farber, and DI Gottlieb. "Neurons of the olfactory epithelium in adult rats contain vimentin." Journal of Neuroscience 6, no. 1 (January 1, 1986): 208–17. http://dx.doi.org/10.1523/jneurosci.06-01-00208.1986.

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Radaelli, G., M. Patruno, L. Maccatrozzo, and B. Funkenstein. "Expression and cellular localization of insulin-like growth factor-II protein and mRNA in Sparus aurata during development." Journal of Endocrinology 178, no. 2 (August 1, 2003): 285–99. http://dx.doi.org/10.1677/joe.0.1780285.

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The spatial localization of IGF-II protein and mRNA was investigated during larval and postlarval developmental stages of the gilthead sea bream (Sparus aurata) by immunohistochemistry and in situ hybridization, using specific antisera and riboprobes. Steady-state levels of IGF-II mRNA in larvae were determined by Northern blot analysis and were found to be increased. Immunoreactivity towards IGF-II was found in larval skin, muscle, gills, gut, olfactory epithelium and kidney. After metamorphosis, the strongest immunoreactivity was found in red skeletal muscle. Positive reaction with IGF-II antibodies was also found in the olfactory epithelium and in the epithelia of pharynx, oesophagus, stomach and kidney. In the adult, the most intense signal was observed in the red and pink musculature and in heart musculature. Immunostaining was also found in saccus vasculosus, thymus, spleen and ovary. IGF-II mRNA was detected by in situ hybridization in the brain, olfactory epithelium, eye, pharynx, skeletal musculature and liver. The spatial distribution of IGF-II shown in this study is consistent with previous findings on the cellular localization of IGF type 1 receptor in the sea bream and supports a role for IGF-II during development and growth of sea bream. Furthermore, these results suggest that IGF-II acts in an autocrine/paracrine manner.
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Song, Su Jeong, Bongkyun Park, Kyuhyung Jo, and Chan-Sik Kim. "Damage to Olfactory Organs of Adult Zebrafish Induced by Diesel Particulate Matter." International Journal of Molecular Sciences 23, no. 1 (December 30, 2021): 407. http://dx.doi.org/10.3390/ijms23010407.

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Particulate matter (PM) is an environmental hazard that is associated with various human health risks. The olfactory system is directly exposed to PM; therefore, the influence of PM exposure on olfactory function must be investigated. In this study, we propose a zebrafish olfactory model to evaluate the effects of exposure to diesel particulate matter (DPM), which was labeled Korean diesel particulate matter (KDP20). KDP20 comprises heavy metals and polycyclic aromatic hydrocarbons (PAHs). KDP20 exposed olfactory organs exhibited reduced cilia and damaged epithelium. Olfactory dysfunction was confirmed using an odor-mediated behavior test. Furthermore, the olfactory damage was analyzed using Alcian blue and anti-calretinin staining. KDP20 exposed olfactory organs exhibited histological damages, such as increased goblet cells, decreased cell density, and calretinin level. Quantitative real-time polymerase chain reaction (qRT-PCR) revealed that PAHs exposure related genes (AHR2 and CYP1A) were upregulated. Reactive oxidation stress (ROS) (CAT) and inflammation (IL-1B) related genes were upregulated. Furthermore, olfactory sensory neuron (OSN) related genes (OMP and S100) were downregulated. In conclusion, KDP20 exposure induced dysfunction of the olfactory system. Additionally, the zebrafish olfactory system exhibited a regenerative capacity with recovery conditions. Thus, this model may be used in future investigating PM-related diseases.
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Dhong, Hun-Jong, Hyo Yeol Kim, and Byung Suk Ha. "Histologic changes to olfactory epithelium in hypothyroid rats." Otolaryngology–Head and Neck Surgery 129, no. 1 (July 2003): 24–32. http://dx.doi.org/10.1016/s0194-59980300530-8.

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OBJECTIVE: The purpose of this study was to immunohistochemically evaluate the effects of thyroid hormones on the olfactory epithelium (OE) in adult rats. STUDY DESIGN AND SETTING: Hypothyroidism was induced in rats by propylthiouracil (PTU) administration. Animals were grouped into 5 consisting of a control group, and 4 groups that had been treated with PTU for 3, 6, 9, or 12 weeks, respectively. The thickness and cell densities of the OE were examined according to the duration of PTU treatment. Changes to OE cell properties were investigated with immunohistochemical stains. RESULTS: No statistically significant differences were found in the thickness and cell densities of the OE among the 5 groups. The number of olfactory receptor neurons positive for neuron-specific enolase or protein gene product 9.5, however, decreased with increasing duration of PTU treatment. CONCLUSION: Thyroid hormones play an important role in the maturation of olfactory receptor neurons.
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Corps, Kara N., Zahidul Islam, James J. Pestka, and Jack R. Harkema. "Neurotoxic, Inflammatory, and Mucosecretory Responses in the Nasal Airways of Mice Repeatedly Exposed to the Macrocyclic Trichothecene Mycotoxin Roridin A." Toxicologic Pathology 38, no. 3 (April 2010): 429–51. http://dx.doi.org/10.1177/0192623310364026.

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Macrocyclic trichothecene mycotoxins encountered in water-damaged buildings have been suggested to contribute to illnesses of the upper respiratory tract. Here, the authors characterized the adverse effects of repeated exposures to roridin A (RA), a representative macrocyclic trichothecene, on the nasal airways of mice and assessed the persistence of these effects. Young, adult, female C57BL/6 mice were exposed to single daily, intranasal, instillations of RA (0.4, 2, 10, or 50 μg/kg body weight [bw]) in saline (50 μl) or saline alone (controls) over 3 weeks or 250 μg/kg RA over 2 weeks. Histopathologic, immunohistochemical, and morphometric analyses of nasal airways conducted 24 hr after the last instillation revealed that the lowest-effect level was 10 μg/kg bw. RA exposure induced a dose-dependent, neutrophilic rhinitis with mucus hypersecretion, atrophy and exfoliation of nasal transitional and respiratory epithelium, olfactory epithelial atrophy and loss of olfactory sensory neurons (OSNs). In a second study, the persistence of lesions in mice instilled with 250 μg/kg bw RA was assessed. Nasal inflammation and excess luminal mucus were resolved after 3 weeks, but OSN loss was still evident in olfactory epithelium (OE). These results suggest that nasal inflammation, mucus hypersecretion, and olfactory neurotoxicity could be important adverse health effects associated with short-term, repeated, airborne exposures to macrocyclic trichothecenes.
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Themmara, V., P. Mehlen, F. Jourdan, and E. Moyse. "Molecular correlates of neuronal apoptosis in olfactory epithelium of adult mouse." Biology of the Cell 91, no. 7 (September 1999): 561. http://dx.doi.org/10.1016/s0248-4900(99)90289-7.

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Mackay-Sim, A., and M. D. Beard. "Hypothyroidism disrupts neural development in the olfactory epithelium of adult mice." Developmental Brain Research 36, no. 2 (December 1987): 190–98. http://dx.doi.org/10.1016/0165-3806(87)90023-x.

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Savya, Sajishnu P., Tenzin Kunkhyen, and Claire E. J. Cheetham. "Low survival rate of young adult-born olfactory sensory neurons in the undamaged mouse olfactory epithelium." Journal of Bioenergetics and Biomembranes 51, no. 1 (October 9, 2018): 41–51. http://dx.doi.org/10.1007/s10863-018-9774-8.

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Romashchenko, A. V., Р. Е. Kireeva, M. В. Sharapova, Т. A. Zapara, and A. S. Ratushnyak. "Learning-induced sensory plasticity of mouse olfactory epithelium." Vavilov Journal of Genetics and Breeding 22, no. 8 (January 3, 2019): 1070–77. http://dx.doi.org/10.18699/vj18.452.

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Traditionally, studies of the neurobiology of learning and memory focus on the circuitry that interfaces between sensory inputs and behavioral outputs, such as the amygdala and cerebellum. However, evidence is accumulating that some forms of learning can in fact drive stimulus­specifc changes very early in sensory systems, including not only primary sensory cortices but also precortical structures and even the peripheral sensory organs themselves. In this study, we investigated the effect of olfactory associative training on the functional activity of olfactory epithelium neurons in response to an indifferent stimulus (orange oil). It was found that such a peripheral structure of the olfactory system of adult mice as the olfactory epithelium (OE) demonstrates experience­dependent plasticity. In our experiment, associative learning led to changes in the patterns of OE cell activation in response to orange oil in comparison with the control group and animals that were given odor without reinforcement. To interpret the results obtained, we compared the distribution of MRI contrast across the zones of OE in response to a conditioned odor in trained animals and in control animals that were given orange oil at three concentrations: original (used for conditioning), 4­fold higher and 4­fold lower. Since the OE activation patterns obtained coincided in the group of trained animals and controls, which were stimulated with orange oil at the 4­fold higher concentration, it can be concluded that associative conditioning increased the sensitivity of the OE to the conditioned stimulus. The observed increase in OE response to orange oil may be the result of neurogenesis, i. e. the maturation of new olfactory neurons responsive to this stimulus, or the consequence of an increase in individual sensitivity of each OE neuron. Based on data of MRI contrast accumulation in mouse OE, the sensory plasticity way in learning­induced increase in sensitivity of OE to conditioned stimulus is more possible. Thus, the sensory plasticity of the OE plays a signifcant role in the formation of the neuronal response to the provision of an initially indifferent odor and is part of the adaptive responses to the environmental changing.
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Barber, Casey N., and David M. Coppola. "Compensatory plasticity in the olfactory epithelium: age, timing, and reversibility." Journal of Neurophysiology 114, no. 3 (September 2015): 2023–32. http://dx.doi.org/10.1152/jn.00076.2015.

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Like other biological systems, olfaction responds “homeostatically” to enduring change in the stimulus environment. This adaptive mechanism, referred to as compensatory plasticity, has been studied almost exclusively in developing animals. Thus it is unknown if this phenomenon is limited to ontogenesis and irreversible, characteristics common to some other forms of plasticity. Here we explore the effects of odor deprivation on the adult mouse olfactory epithelium (OE) using nasal plugs to eliminate nasal airflow unilaterally. Plugs were in place for 2–6 wk after which electroolfactograms (EOGs) were recorded from the occluded and open sides of the nasal cavity. Mean EOG amplitudes were significantly greater on the occluded than on the open side. The duration of plugging did not affect the results, suggesting that maximal compensation occurs within 2 wk or less. The magnitude of the EOG difference between the open and occluded side in plugged mice was comparable to adults that had undergone surgical naris occlusion as neonates. When plugs were removed after 4 wk followed by 2 wk of recovery, mean EOG amplitudes were not significantly different between the always-open and previously plugged sides of the nasal cavity suggesting that this form of plasticity is reversible. Taken together, these results suggest that compensatory plasticity is a constitutive mechanism of olfactory receptor neurons that allows these cells to recalibrate their stimulus-response relationship to fit the statistics of their current odor environment.
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Mackay-Sim, A., and P. Kittel. "Cell dynamics in the adult mouse olfactory epithelium: a quantitative autoradiographic study." Journal of Neuroscience 11, no. 4 (April 1, 1991): 979–84. http://dx.doi.org/10.1523/jneurosci.11-04-00979.1991.

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Suh, Kyung Shik, So Yeun Kim, Yong Chul Bae, Gabriele V. Ronnett, and Cheil Moon. "Effects of unilateral naris occlusion on the olfactory epithelium of adult mice." NeuroReport 17, no. 11 (July 2006): 1139–42. http://dx.doi.org/10.1097/01.wnr.0000224762.54336.7d.

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36

Féron, F., A. Mackay-Sim, J. L. Andrieu, K. I. Matthaei, A. Holley, and G. Sicard. "Stress induces neurogenesis in non-neuronal cell cultures of adult olfactory epithelium." Neuroscience 88, no. 2 (January 1999): 571–83. http://dx.doi.org/10.1016/s0306-4522(98)00233-4.

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37

Whelan, J. P., C. J. Wysocki, and L. A. Lampson. "Distribution of beta 2-microglobulin in olfactory epithelium: a proliferating neuroepithelium not protected by a blood-tissue barrier." Journal of Immunology 137, no. 8 (October 15, 1986): 2567–71. http://dx.doi.org/10.4049/jimmunol.137.8.2567.

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Abstract The olfactory neuroepithelium is unique in adult vertebrates in that bipolar sensory neurons are constantly dying and being replaced. The sensory neurons are also unusual because they are directly exposed to the external environment via their dendritic processes in the nasal cavity. Surveillance of this tissue by major histocompatibility complex (MHC) class I-restricted cytotoxic T cells would presumably serve as an important means of defense against foreign pathogens. Although adult brain shows a lack of class I molecules, it has not been reported if either proliferating neurons or sensory neurons in olfactory neuroepithelium also lack class I. To examine olfactory neuroepithelium, an antiserum against beta 2-microglobulin (beta 2-m), the invariant light chain associated with all class I molecules, was employed as a general probe in an immunocytochemical assay. beta 2-m was detected in columnar respiratory epithelium, blood vessel walls, and a small population of interstitial cells in the lamina propria, but no cell in the olfactory neuroepithelium stained for beta 2-m. Parallel patterns were obtained in the vomeronasal organ. These results suggest that lack of beta 2-m, and presumably class I, may be a general phenotype of neuronal cells regardless of their mitotic state or exposure to environmental antigens.
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Li, Ke, Cory O. Brant, Mar Huertas, Edward J. Hessler, Gellert Mezei, Anne M. Scott, Thomas R. Hoye, and Weiming Li. "Fatty-acid derivative acts as a sea lamprey migratory pheromone." Proceedings of the National Academy of Sciences 115, no. 34 (July 30, 2018): 8603–8. http://dx.doi.org/10.1073/pnas.1803169115.

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Olfactory cues provide critical information for spatial orientation of fish, especially in the context of anadromous migrations. Born in freshwater, juveniles of anadromous fish descend to the ocean where they grow into adults before migrating back into freshwater to spawn. The reproductive migrants, therefore, are under selective pressures to locate streams optimal for offspring survival. Many anadromous fish use olfactory cues to orient toward suitable streams. However, no behaviorally active compounds have been identified as migratory cues. Extensive studies have shown that the migratory adult sea lampreys (Petromyzon marinus), a jawless fish, track a pheromone emitted by their stream-dwelling larvae, and, consequently, enter streams with abundant larvae. We fractionated extracts of larval sea lamprey washings with guidance from a bioassay that measures in-stream migratory behaviors of adults and identified four dihydroxylated tetrahydrofuran fatty acids, of which (+)-(2S,3S,5R)-tetrahydro-3-hydroxy-5-[(1R)-1-hydroxyhexyl]-2-furanoctanoic acid was shown as a migratory pheromone. The chemical structure was elucidated by spectroscopies and confirmed by chemical synthesis and X-ray crystallography. The four fatty acids were isomer-specific and enantiomer-specific in their olfactory and behavioral activities. A synthetic copy of the identified pheromone was a potent stimulant of the adult olfactory epithelium, and, at 5 × 10−13 M, replicated the extracts of larval washings in biasing adults into a tributary stream. Our results reveal a pheromone that bridges two distinct life stages and guides orientation over a large space that spans two different habitats. The identified molecule may be useful for control of the sea lamprey.
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Lv, Maolin, Xiuli Chen, Xin Huang, Ning Liu, Weimin Wang, and Han Liu. "Transcriptome Analysis Reveals Sexual Disparities between Olfactory and Immune Gene Expression in the Olfactory Epithelium of Megalobrama amblycephala." International Journal of Molecular Sciences 22, no. 23 (December 1, 2021): 13017. http://dx.doi.org/10.3390/ijms222313017.

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The olfactory organ is an important chemoreceptor in vertebrates. However, the sexual disparities in gene expression patterns in the olfactory organ in fish remain unstudied. Here, we conducted a transcriptome analysis of the olfactory epithelium (OE) of male and female blunt snout bream (Megalobrama amblycephala) to identify the differences. The histological analysis showed that there were 22 leaf-like olfactory lamellaes on one side of the OE of the adult blunt snout bream. The sensory area of OE is enriched with ciliated receptor cells and microvilli receptor cells. The transcriptome analysis showed that only 10 out of 336 olfactory receptor genes (224 ORs, 5 V1Rs, 55 V2Rs, and 52 TAARs) exhibited significant expression differences between males and females, and most of the differentially expressed genes were related to the immune system. We also validated these results using qPCR: 10 OR genes and 6 immunity-related genes significantly differed between males and females. The FISH analysis results indicated that the ORs were mainly expressed at the edge of the olfactory lamellae. Collectively, our study reveals that gender is not an important factor influencing the expression of olfactory receptors, but the expression of immune genes varies greatly between the genders in blunt snout bream.
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40

Workman, Alan D., Aria Jafari, Roy Xiao, and Benjamin S. Bleier. "Airborne aerosol olfactory deposition contributes to anosmia in COVID-19." PLOS ONE 16, no. 2 (February 5, 2021): e0244127. http://dx.doi.org/10.1371/journal.pone.0244127.

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Introduction Olfactory dysfunction (OD) affects a majority of COVID-19 patients, is atypical in duration and recovery, and is associated with focal opacification and inflammation of the olfactory epithelium. Given recent increased emphasis on airborne transmission of SARS-CoV-2, the purpose of the present study was to experimentally characterize aerosol dispersion within olfactory epithelium (OE) and respiratory epithelium (RE) in human subjects, to determine if small (sub 5μm) airborne aerosols selectively deposit in the OE. Methods Healthy adult volunteers inhaled fluorescein-labeled nebulized 0.5–5μm airborne aerosol or atomized larger aerosolized droplets (30–100μm). Particulate deposition in the OE and RE was assessed by blue-light filter modified rigid endoscopic evaluation with subsequent image randomization, processing and quantification by a blinded reviewer. Results 0.5–5μm airborne aerosol deposition, as assessed by fluorescence gray value, was significantly higher in the OE than the RE bilaterally, with minimal to no deposition observed in the RE (maximum fluorescence: OE 19.5(IQR 22.5), RE 1(IQR 3.2), p<0.001; average fluorescence: OE 2.3(IQR 4.5), RE 0.1(IQR 0.2), p<0.01). Conversely, larger 30–100μm aerosolized droplet deposition was significantly greater in the RE than the OE (maximum fluorescence: OE 13(IQR 14.3), RE 38(IQR 45.5), p<0.01; average fluorescence: OE 1.9(IQR 2.1), RE 5.9(IQR 5.9), p<0.01). Conclusions Our data experimentally confirm that despite bypassing the majority of the upper airway, small-sized (0.5–5μm) airborne aerosols differentially deposit in significant concentrations within the olfactory epithelium. This provides a compelling aerodynamic mechanism to explain atypical OD in COVID-19.
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Sosnowski, J. S., M. Gupta, K. H. Reid, and F. J. Roisen. "Chemical traumatization of adult mouse olfactory epithelium in situ stimulates growth and differentiation of olfactory neurons in vitro." Brain Research 702, no. 1-2 (December 1995): 37–48. http://dx.doi.org/10.1016/0006-8993(95)00960-7.

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42

Marioni, G., G. Ottaviano, A. Staffieri, M. Zaccaria, V. J. Lund, E. Tognazza, S. Coles, P. Pavan, E. Brugin, and A. Ermolao. "Nasal functional modifications after physical exercise: olfactory threshold and peak nasal inspiratory flow." Rhinology journal 48, no. 3 (September 1, 2010): 277–80. http://dx.doi.org/10.4193/rhino09.141.

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Statement of problem: The respiratory nasal effects of physical exercise have been extensively investigated; on the other hand there are no data regarding olfactory threshold modification after aerobic physical exercise. Methods: The present prospective study investigated the modifications in nasal respiratory flows and olfactory thresholds after controlled aerobic physical exercise in a cohort of 15 adult, healthy volunteers. The Peak Nasal Inspiratory Flow (PNIF), and the Sniffin’ Sticks olfactory threshold test were used for our determinations. Main results: The mean PNIF after physical exercise was significantly higher than the mean PNIF value found before physical exercise. Statistical analysis ruled out any significant difference between mean olfactory thresholds pre vs post physical exercise. Principal conclusions: These outcomes confirmed PNIF sensitivity and reliability also in determining the changes in nasal patency occurring after physical exercise. The active vasoconstriction of nasal mucosa associated with the reduction of blood flow to the olfactory epithelium due to physical exercise may be compensated for by the increase of olfactory molecules that reach the olfactory mucosa because of nasal mucosal shrinkage: this mechanism could explain the stability of mean olfactory threshold after physical exercise.
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Fishelson, L., D. Golani, B. Galil, and M. Goren. "Comparison of the Nasal Olfactory Organs of Various Species of Lizardfishes (Teleostei: Aulopiformes: Synodontidae) with Additional Remarks on the Brain." International Journal of Zoology 2010 (2010): 1–8. http://dx.doi.org/10.1155/2010/807913.

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The olfactory organs of lizardfishes (Synodontidae) are situated in two capsules connected to the outside by incurrent and excurrent openings. The olfactory epithelium is in form of petal rosettes each composed of lamellae and a rephe, and bear olfactory receptor neurons, supporting cells and cells with kinocillia. The dimension of rosettes and lamellae, as well as the number of lamellae, increase with growth of the fish; until in adult fish these parameters remaine constant, species specific. In adultSynodusspp. andTrachinocephalus myopsthe rosettes are 3.5–4.0 mm long, with 5–8 lamellae, whereas inSauridaspp. they are 8.0 mm and possess up tp 22 lamellae. The number of ORN ranges from 2,600 on the smaller lamellae to 20,000 on the largest ones. The number of ORN/m of olfactory is ca. 30,000 inSauridaspp. Thus the rosettes ofS. macrolepiswith 20 lamellae possess a total of ca. 170,000 ORN, whereas those ofSy. variegatusandT. myopswith the average of six lamellae possess only ca. 50,000–65,000 ORN. The olfactory nerves lead from the rosettes to the olfactory balbs situated on the olfactory lobes. The differences among the species in olfactory organs are discussed in correlation with their distribution.
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Iwai, Naomi, Zhijian Zhou, Dennis R. Roop, and Richard R. Behringer. "Horizontal Basal Cells Are Multipotent Progenitors in Normal and Injured Adult Olfactory Epithelium." Stem Cells 26, no. 5 (May 2008): 1298–306. http://dx.doi.org/10.1634/stemcells.2007-0891.

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Heron, Paula M., Arnold J. Stromberg, Patrick Breheny, and Timothy S. McClintock. "Molecular events in the cell types of the olfactory epithelium during adult neurogenesis." Molecular Brain 6, no. 1 (2013): 49. http://dx.doi.org/10.1186/1756-6606-6-49.

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46

Franco, Marie-dominique, Jonathan Bohbot, Kenny Fernandez, Jayd Hanna, James Poppy, and Richard Vogt. "Sensory Cell Proliferation within the Olfactory Epithelium of Developing Adult Manduca sexta (Lepidoptera)." PLoS ONE 2, no. 2 (February 14, 2007): e215. http://dx.doi.org/10.1371/journal.pone.0000215.

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47

Sicard, G., F. Feron, J. L. Andrieu, A. Holley, and A. Mackaysim. "Generation of Neurons from a Nonneuronal Precursor in Adult Olfactory Epithelium in Vitro." Annals of the New York Academy of Sciences 855, no. 1 OLFACTION AND (November 1998): 223–25. http://dx.doi.org/10.1111/j.1749-6632.1998.tb10570.x.

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48

Hsu, Pi-en, Fu Yu, François Féron, James O. Pickles, Kyra Sneesby, and Alan Mackay-Sim. "Basic fibroblast growth factor and fibroblast growth factor receptors in adult olfactory epithelium." Brain Research 896, no. 1-2 (March 2001): 188–97. http://dx.doi.org/10.1016/s0006-8993(01)02173-4.

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49

Choi, Rhea, and Bradley J. Goldstein. "Olfactory epithelium: Cells, clinical disorders, and insights from an adult stem cell niche." Laryngoscope Investigative Otolaryngology 3, no. 1 (February 2018): 35–42. http://dx.doi.org/10.1002/lio2.135.

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Parisi, Valentina, Maria C. Guerrera, Francesco Abbate, Olivia Garcia-Suarez, Eliseo Viña, Jose A. Vega, and Antonino Germanà. "Immunohistochemical characterization of the crypt neurons in the olfactory epithelium of adult zebrafish." Annals of Anatomy - Anatomischer Anzeiger 196, no. 4 (July 2014): 178–82. http://dx.doi.org/10.1016/j.aanat.2014.01.004.

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