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Structural, morphometric and immunohistochemical study of the rabbit accessory olfactory bulb

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Abstract

The accessory olfactory bulb (AOB) is the first neural integrative centre of the vomeronasal system (VNS), which is associated primarily with the detection of semiochemicals. Although the rabbit is used as a model for the study of chemocommunication, these studies are hampered by the lack of knowledge regarding the topography, lamination, and neurochemical properties of the rabbit AOB. To fill this gap, we have employed histological stainings: lectin labelling with Ulex europaeus (UEA-I), Bandeiraea simplicifolia (BSI-B4), and Lycopersicon esculentum (LEA) agglutinins, and a range of immunohistochemical markers. Anti-G proteins Gαi2/Gαo, not previously studied in the rabbit AOB, are expressed following an antero-posterior zonal pattern. This places Lagomorpha among the small groups of mammals that conserve a double-path vomeronasal reception. Antibodies against olfactory marker protein (OMP), growth-associated protein-43 (GAP-43), glutaminase (GLS), microtubule-associated protein-2 (MAP-2), glial fibrillary-acidic protein (GFAP), calbindin (CB), and calretinin (CR) characterise the strata and the principal components of the BOA, demonstrating several singular features of the rabbit AOB. This diversity is accentuated by the presence of a unique organisation: four neuronal clusters in the accessory bulbar white matter, two of them not previously characterised in any species (the γ and δ groups). Our morphometric study of the AOB has found significant differences between sexes in the numerical density of principal cells, with larger values in females, a pattern completely opposite to that found in rats. In summary, the rabbit possesses a highly developed AOB, with many specific features that highlight the significant role played by chemocommunication among this species.

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References

  • Apfelbach R, Blanchard CD, Blanchard RJ et al (2005) The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosci Biobehav Rev 29:1123–1144

    PubMed  Google Scholar 

  • Barrios AW, Nuñez G, Sanchez-Quinteiro P et al (2014) Anatomy, histochemistry, and immunohistochemistry of the olfactory subsystems in mice. Front Neuroanat 8:63

    PubMed  PubMed Central  Google Scholar 

  • Ben-Shaul Y, Katz LC, Mooney R et al (2010) In vivo vomeronasal stimulation reveals sensory encoding of conspecific and allospecific cues by the mouse accessory olfactory bulb. PNAS 107:5172–5177

    CAS  PubMed  Google Scholar 

  • Bernhardt R, Matus A (1984) Light and electron microscopic studies of the distribution of microtubule-associated protein 2 in rat brain: a difference between dendritic and axonal cytoskeletons. J Comp Neurol 226:203–221

    CAS  PubMed  Google Scholar 

  • Bock P, Rohn K, Beineke A et al (2006) Site-specific population dynamics and variable olfactory marker protein expression in the postnatal canine olfactory epithelium. J Anat 215:522–535

    Google Scholar 

  • Boehm U (2006) The vomeronasal system in mice: from the nose to the hypothalamus- and back! Semin Cell Dev Biol 17:471–479

    PubMed  Google Scholar 

  • Bouvier AC, Jacquinet C (2008) Pheromone in rabbits. Preliminary technical results on farm use in France. In: Xiccato G, Trocino A, Lukefahr SD (eds) 9th World rabbit congress. Verona, 2008. Proceedings, pp 303–308

  • Brennan PA, Zufall F (2006) Pheromonal communication in vertebrates. Nature 444:308–315

    CAS  PubMed  Google Scholar 

  • Briñón JG, Weruaga E, Crespo C et al (2001) Calretinin-, neurocalcin-, and parvalbumin-immunoreactive elements in the olfactory bulb of the hedgehog (Erinaceus europaeus). J Comp Neurol 429:554–570

    PubMed  Google Scholar 

  • Brown RE (1985) Effects of social isolation in adulthood on odor preferences and urine-marking in male rats. Behav Neural Biol 44:139–143

    CAS  PubMed  Google Scholar 

  • Charra R, Datiche F, Casthano A et al (2012) Brain processing of the mammary pheromone in newborn rabbits. Behav Brain Res 226:179–188

    CAS  PubMed  Google Scholar 

  • Chehrehasa F, Ekberg JA, St John JA (2014) A novel method using intranasal delivery of EdU demonstrates that accessory olfactory ensheathing cells respond to injury by proliferation. Neurosci Lett 563:90–95

    CAS  PubMed  Google Scholar 

  • Dehmelt L, Halpain S (2005) The MAP2/Tau family of microtubule-associated proteins. Genome Biol 6:204

    PubMed  Google Scholar 

  • Dennis JC, Smith TD, Bhatnagar KP et al (2004) Expression of neuron-specific markers by the vomeronasal neuroepithelium in six species of primates. Anat Rec 281:1190–1200

    Google Scholar 

  • Dennis JC, Stilwell NK, Smith TD et al (2019) Is the mole rat vomeronasal organ functional? Anat Rec. https://doi.org/10.1002/ar.24060

    Article  Google Scholar 

  • Dulac C, Torello AT (2003) Molecular detection of pheromone signals in mammals: from genes to behaviour. Nat Rev Neurosci 4:551–562

    CAS  PubMed  Google Scholar 

  • Farbman AI, Margolis FL (1980) Olfactory marker protein during ontogeny: immunohistochemical localization. Dev Biol 74:205–215

    CAS  PubMed  Google Scholar 

  • Frahm HD, Bhatnagar KP (1980) Comparative morphology of the accessory olfactory bulb in bats. J Anat 130:349–365

    CAS  PubMed  PubMed Central  Google Scholar 

  • González-Mariscal G, Caba M, Martínez-Gómez M et al (2016) Mothers and offspring: the rabbit as a model system in the study of mammalian maternal behavior and sibling interactions. Horm Behav 77:30–41

    PubMed  Google Scholar 

  • Grus WE, Shi P, Zhang Y et al (2005) Dramatic variation of the vomeronasal pheromone receptor gene repertoire among five orders of placental and marsupial mammals. PNAS 102:5767–5772

    CAS  PubMed  Google Scholar 

  • Gudden B (1870) Experimental untersuchungen über das peripherische und centrale nervensystem. Arch Psychiatr Nervenkr 11:693–723

    Google Scholar 

  • Guillamón A, Segovia S (1997) Sex differences in the vomeronasal system. Brain Res Bull 44:377–382

    PubMed  Google Scholar 

  • Halpern M (1987) The organization and function of the vomeronasal system. Annu Rev Neurosci 10:325–362

    CAS  PubMed  Google Scholar 

  • Halpern M, Martínez-Marcos A (2003) Structure and function of the vomeronasal system: an update. Prog Neurobiol 70:245–318

    CAS  PubMed  Google Scholar 

  • Halpern M, Shapiro LS, Jia C (1995) Differential localization of G proteins in the opossum vomeronasal system. Brain Res 677:157–161

    CAS  PubMed  Google Scholar 

  • Hasui K, Takatsuka T, Sakamoto R et al (2003) Double autoimmunostaining with glycine treatment. J Histochem Cytochem 51:1169–1176

    CAS  PubMed  Google Scholar 

  • Holy TE (2018) The accessory olfactory system: innately specialized or microcosm of mammalian circuitry? Annu Rev Neurosci 41:501–525

    CAS  PubMed  Google Scholar 

  • Ihara S, Yoshikawa K, Touhara K (2013) Chemosensory signals and their receptors in the olfactory neural system. Neuroscience 254:45–60

    CAS  PubMed  Google Scholar 

  • Isogai S, Si S, Pont-Lezica L et al (2011) Molecular organization of vomeronasal chemoreception. Nature 478:241–245

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jacobowitz DM, Winsky L (1991) Immunocytochemical localization of calretinin in the forebrain of the rat. J Comp Neurol 304:198–218

    CAS  PubMed  Google Scholar 

  • Jessell TM, Hynes MA, Dodd J (1990) Carbohydrates and carbohydrate-binding proteins in the nervous system. Annu Rev Neurosci 13:227–255

    CAS  PubMed  Google Scholar 

  • Jia C, Halpern M (1996) Subclasses of vomeronasal receptor neurons: differential expression of G proteins (Gi alpha 2 and G (o alpha)) and segregated projections to the accessory olfactory bulb. Brain Res 719:117–128

    CAS  PubMed  Google Scholar 

  • Jia C, Halpern M (2003) Calbindin D28 k immunoreactive neurons in vomeronasal organ and their projections to the accessory olfactory bulb in the rat. Brain Res 977:261–269

    CAS  PubMed  Google Scholar 

  • Jia C, Halpern M (2004) Calbindin D28k, parvalbumin, and calretinin immunoreactivity in the main and accessory olfactory bulbs of the gray short-tailed opossum, Monodelphis domestica. J Morphol 259:271–280

    PubMed  Google Scholar 

  • Keverne EB (2002) Pheromones, vomeronasal function, and gender-specific behavior. Cell 108:735–738

    CAS  PubMed  Google Scholar 

  • Kinzinger JH, Johnson EW, Bhatnagar KP et al (2005) Comparative study of lectin reactivity in the vomeronasal organ of human and nonhuman primates. Anat Rec 284:550–560

    Google Scholar 

  • Kondoh D, Kamikawa A, Sasaki M et al (2017) Localization of α1-2 fucose glycan in the mouse olfactory pathway. Cells Tissues Organs 203:20–28

    CAS  PubMed  Google Scholar 

  • Kream RM, Davis BJ, Kawano T et al (1984) Substance P and catecholaminergic expression in neurons of the hamster main olfactory bulb. J Comp Neurol 222:140–154

    CAS  PubMed  Google Scholar 

  • Larriva-Sahd J (2008) The accessory olfactory bulb in the adult rat: a cytological study of its cell types, neuropil, neuronal modules, and interactions with the main olfactory system. J Comp Neurol 510:309–350

    PubMed  Google Scholar 

  • Larriva-Sahd J (2012) Cytological organization of the alpha component of the anterior olfactory nucleus and olfactory limbus. Front Neuroanat 6:23

    PubMed  PubMed Central  Google Scholar 

  • Lazzari M, Bettini S, Franceschini V (2016) Immunocytochemical characterisation of ensheathing glia in the olfactory and vomeronasal systems of Ambystoma mexicanum (Caudata: Ambystomatidae). Brain Struct Funct 221:955–967

    CAS  PubMed  Google Scholar 

  • Lohman AHM (1963) The anterior olfactory lobe of the guinea pig. Acta Anat 45:9–109

    Google Scholar 

  • Mackay-Sim A, Duvall D, Graves BM (1985) The West Indian manatee (Trichechus manatus) lacks a vomeronasal organ. Brain Behav Evol 27:186–194

    CAS  PubMed  Google Scholar 

  • Mandiyan VS, Coats JK, Shah NM (2005) Deficits in sexual and aggressive behaviors in Cnga2 mutant mice. Nat Neurosci 8:1660–1662

    CAS  PubMed  Google Scholar 

  • Martínez-Marcos A, Lanuza E, Halpern M (2002) Neural substrates for processing chemosensory information in snakes. Brain Res Bull 57:543–546

    PubMed  Google Scholar 

  • Martín-López E, Corona R, López-Mascaraque L (2012) Postnatal characterization of cells in the accessory olfactory bulb of wild type and reeler mice. Front Neuroanat 6:15

    PubMed  PubMed Central  Google Scholar 

  • Meisami E, Bhatnagar KP (1998) Structure and diversity in mammalian accessory olfactory bulb. Microsc Res Tech 43:476–499

    CAS  PubMed  Google Scholar 

  • Melo AI, González-Mariscal G (2010) Communication by olfactory signals in rabbits: its role in reproduction. Vitam Horm 83:351–371

    CAS  PubMed  Google Scholar 

  • Mohrhardt J, Nagel M, Fleck D et al (2018) Signal detection and coding in the accessory olfactory system. Chem Senses 43:667–695

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mombaerts P (2004) Genes and ligands for odorant, vomeronasal and taste receptors. Nat Rev Neurosci 5:263–278

    CAS  PubMed  Google Scholar 

  • Mori K (1983) Mitral cells in the rabbit accessory olfactory bulb: their morphology and response to LOT stimulation. Soc Neurosci Abst 9:1020

    Google Scholar 

  • Mori K (1987) Monoclonal antibodies (2C5 and 4C9) against lactoseries carbohydrates identify subsets of olfactory and vomeronasal receptor cells and their axons in the rabbit. Brain Res 408:215–221

    CAS  PubMed  Google Scholar 

  • Mori K, Imamura K, Fujita SC et al (1987) Projections of two subclasses of vomeronasal nerve fibers to the accessory olfactory bulb in the rabbit. Neuroscience 20:259–278

    CAS  PubMed  Google Scholar 

  • Mouton PR (2002) Principles and practices of unbiased stereology. An introduction for bioscientists. John Hopkins University Press, Baltimore

    Google Scholar 

  • Murphy WJ, Eizirik E, O’Brien SJ et al (2001) Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294:2348–2351

    CAS  PubMed  Google Scholar 

  • Nakajima T, Sakaue M, Kato M et al (1998) Immunohistochemical and enzyme-histochemical study on the accessory olfactory bulb of the dog. Anat Rec 252:393–402

    CAS  PubMed  Google Scholar 

  • Ngwenya A, Patzke N, Ihunwo AO et al (2011) Organisation and chemical neuroanatomy of the African elephant (Loxodonta africana) olfactory bulb. Brain Struct Funct 216:403–416

    CAS  PubMed  Google Scholar 

  • Pardo-Bellver C, Martínez-Bellver S, Martínez-García F et al (2017) Synchronized activity in the main and accessory olfactory bulbs and vomeronasal amygdala elicited by chemical signals in freely behaving mice. Sci Rep 7:9924

    PubMed  PubMed Central  Google Scholar 

  • Park C, Ahn M, Lee JY et al (2014) A morphological study of the vomeronasal organ and the accessory olfactory bulb in the Korean roe deer, Capreolus pygargus. Acta Histochem 116:258–264

    PubMed  Google Scholar 

  • Porteros A, Arévalo R, Crespo C et al (1995) Calbindin D-28k immunoreactivity in the rat accessory olfactory bulb. Brain Res 689:93–100

    CAS  PubMed  Google Scholar 

  • Pro-Sistiaga P, Mohedano-Moriano A, Ubeda-Bañon I et al (2007) Convergence of olfactory and vomeronasal projections in the rat basal telencephalon. J Comp Neurol 504:346–362

    PubMed  Google Scholar 

  • Quaglino E, Giustetto M, Panzanelli P et al (1999) Immunocytochemical localization of glutamate and gamma-aminobutyric acid in the accessory olfactory bulb of the rat. J Comp Neurol 408:61–72

    CAS  PubMed  Google Scholar 

  • Ramakers GJ, Verhaagen J, Oestreicher AB et al (1992) Immunolocalization of B-50 (GAP-43) in the mouse olfactory bulb: predominant presence in preterminal axons. J Neurocytol 21:853–869

    CAS  PubMed  Google Scholar 

  • Ramón y Cajal S (1904) Corteza Olfativa. In: Textura del Sistema Nervioso Central del Hombre y los Vertebrados, vol 2. Imprenta y Librería Nicolas Moya, Spain, pp 913–941

  • Ramos-Vara JA, Miller MA (2006) Comparison of two polymers based immunohistochemical detection systems: ENVISION + and ImmPRESS. J Microsc 224:135–139

    CAS  PubMed  Google Scholar 

  • Rodewald A, Gisder D, Gebhart VM et al (2016) Distribution of olfactory marker protein in the rat vomeronasal organ. J Chem Neuroanat 77:19–23

    CAS  PubMed  Google Scholar 

  • Rodriguez I, Feinstein P, Mombaerts P (1999) Variable patterns of axonal projections of sensory neurons in the mouse vomeronasal system. Cell 97:199–208

    CAS  PubMed  Google Scholar 

  • Rodriguez I, Greer CA, Mok MY et al (2000) A putative pheromone receptor gene expressed in human olfactory mucosa. Nat Genet 26:18–19

    CAS  PubMed  Google Scholar 

  • Salazar I, Sanchez-Quinteiro P (1998) Lectin binding patterns in the vomeronasal organ and accessory olfactory bulb of the rat. Anat Embryol 198:331–339

    CAS  PubMed  Google Scholar 

  • Salazar I, Sanchez-Quinteiro P (2011) A detailed morphological study of the vomeronasal organ and the accessory olfactory bulb of cats. Microsc Res Tech 74:1109–1120

    PubMed  Google Scholar 

  • Salazar I, Sanchez-Quinteiro P, Cifuentes JM et al (1998) The accessory olfactory bulb of the mink, Mustela vison: a morphological and lectin histochemical study. Anat Histol Embryol 27:297–300

    CAS  PubMed  Google Scholar 

  • Salazar I, Sanchez-Quinteiro P, Lombardero M et al (2000) A descriptive and comparative lectin histochemical study of the vomeronasal system in pigs and sheep. J Anat 196:15–22

    PubMed  PubMed Central  Google Scholar 

  • Salazar I, Sanchez-Quinteiro P, Lombardero M et al (2001) Histochemical identification of carbohydrate moieties in the accessory olfactory bulb of the mouse using a panel of lectins. Chem Senses 26:645–652

    CAS  PubMed  Google Scholar 

  • Salazar I, Sanchez-Quinteiro P, Cifuentes JM et al (2006) General organization of the perinatal and adult accessory olfactory bulb in mice. Anat Rec 288:1009–1025

    Google Scholar 

  • Salazar I, Sanchez-Quinteiro P, Alemañ N et al (2007) Diversity of the vomeronasal system in mammals: the singularities of the sheep model. Microsc Res Tec 70:752–762

    Google Scholar 

  • Salazar I, Cifuentes JM, Sanchez-Quinteiro P (2013) Morphological and immunohistochemical features of the vomeronasal system in dogs. Anat Rec 296:146–155

    CAS  Google Scholar 

  • Sam M, Vora S, Malnic B et al (2001) Odorants may arouse instinctive behaviours. Nature 412:142

    CAS  PubMed  Google Scholar 

  • Schaal B, Coureaud G, Langlois D et al (2003) Chemical and behavioural characterization of the rabbit mammary pheromone. Nature 424:68–72

    CAS  PubMed  Google Scholar 

  • Schneider NY, Fletcher TP, Shaw G et al (2012) Goα expression in the vomeronasal organ and olfactory bulb of the tammar wallaby. Chem Senses 37:567–577

    PubMed  Google Scholar 

  • Schneider NY, Piccin C, Datiche F et al (2016) Spontaneous brain processing of the mammary pheromone in rabbit neonates prior to milk intake. Behav Brain Res 313:191–200

    CAS  PubMed  Google Scholar 

  • Schneider NY, Datiche F, Coureaud G (2018) Brain anatomy of the 4-day-old European Rabbit. J Anat 232:747–767

    PubMed  Google Scholar 

  • Segovia S, Garcia-Falgueras A, Carrillo B et al (2006) Sexual dimorphism in the vomeronasal system of the rabbit. Brain Res 1102:52–62

    CAS  PubMed  Google Scholar 

  • Shapiro LS, Ee PL, Halpern M (1995) Lectin histochemical identification of carbohydrate moieties in opossum chemosensory systems during development, with special emphasis on VVA-identified subdivisions in the accessory olfactory bulb. J Morphol 224:331–349

    CAS  PubMed  Google Scholar 

  • Shinohara H, Asano T, Kato K (1992) Differential localization of G-proteins Gi and Go in the accessory olfactory bulb of the rat. J Neurosci 12:1275–1279

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shnayder L, Schwanzel-Fukuda M, Halpern M (1993) Differential OMP expression in opossum accessory olfactory bulb. NeuroReport 5:193–196

    CAS  PubMed  Google Scholar 

  • Skeen LC, Hall WC (1977) Efferent projections of the main and the accessory olfactory bulb in the tree shrew (Tupaia glis). J Comp Neurol 172:1–35

    CAS  PubMed  Google Scholar 

  • Slotnick B (2001) Animal cognition and the rat olfactory system. Trends Cogn Sci 5:216–222

    CAS  PubMed  Google Scholar 

  • Smithson LJ, Kawaja MD (2009) A comparative examination of biomarkers for olfactory ensheathing cells in cats and guinea pigs. Brain Res 1284:41–53

    CAS  PubMed  Google Scholar 

  • Sterio DC (1984) The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc 134:127–136

    CAS  PubMed  Google Scholar 

  • Suarez R, Mpodozis J (2009) Heterogeneities of size and sexual dimorphism between the subdomains of the lateral-innervated accessory olfactory bulb (AOB) of Octodon degus (Rodentia: Hystricognathi). Behav Brain Res 198:306–312

    PubMed  Google Scholar 

  • Suarez R, Villalón A, Künzle H et al (2009) Transposition and Intermingling of Galphai2 and Galphao afferences into single vomeronasal glomeruli in the Madagascan lesser Tenrec Echinops telfairi. PLoS ONE 4:e8005

    PubMed  PubMed Central  Google Scholar 

  • Suarez R, Fernández-Aburto P, Manger RR et al (2011a) Deterioration of the Gαo vomeronasal pathway in sexually dimorphic mammals. PLoS One 6:e2643

    Google Scholar 

  • Suarez R, Santibáñez R, Parra D et al (2011b) Share and differential traits in the accessory olfactory bulb of caviomorph rodents with particular reference to the semiaquatic capybara. J Anat 218:558–565

    PubMed  PubMed Central  Google Scholar 

  • Swaney WT, Keverne EB (2009) The evolution of pheromonal communication. Behav Brain Res 200:239–247

    CAS  PubMed  Google Scholar 

  • Switzer RC 3rd, Johnson JI, Kirsch JA (1980) Phylogeny through brain traits. Relation of lateral olfactory tract fibers to the accessory olfactory formation as a palimpsest of mammalian descent. Brain Behav Evol 17:339–363

    PubMed  Google Scholar 

  • Szendrő Z, Szendrő K, Zotte AD (2012) Management of reproduction on small, medium and large rabbit farms: a review. Asian-Australas J Anim Sci 25:738–748

    PubMed  PubMed Central  Google Scholar 

  • Szendrő Z, Mikó A, Odermatt M et al (2013) Comparison of performance and welfare of single-caged and group-housed rabbit does. Animal 7:463–468

    PubMed  Google Scholar 

  • Takami S, Graziadei PP (1991) Light microscopic Golgi study of mitral/tufted cells in the accessory olfactory bulb of the adult rat. J Comp Neurol 311:65–83

    CAS  PubMed  Google Scholar 

  • Takigami S, Mori Y, Ichikawa M (2000) Projection pattern of vomeronasal neurons to the accessory olfactory bulb in goats. Chem Senses 25:387–393

    CAS  PubMed  Google Scholar 

  • Takigami S, Mori Y, Tanioka Y et al (2004) Morphological evidence for two types of Mammalian vomeronasal system. Chem Senses 29:301–310

    PubMed  Google Scholar 

  • Tolivia J, Tolivia D, Navarro A (1998) New technique for differential staining of myelinated fibers and nerve cells on paraffin sections. Anat Rec 222:437–440

    Google Scholar 

  • Trinh K, Storm DR (2003) Vomeronasal organ detects odorants in absence of signaling through main olfactory epithelium. Nat Neurosci 6:519–525

    CAS  PubMed  Google Scholar 

  • Trotier D, Eloit C, Wassef M et al (2000) The vomeronasal cavity in adult humans. Chem Senses 25:369–380

    CAS  PubMed  Google Scholar 

  • Trouillet AC, Keller M, Weiss J et al (2019) Central role of G protein Gαi2 and Gαi2 + vomeronasal neurons in balancing territorial and infant-directed aggression of male mice. PNAS 116:5135–5143

    CAS  PubMed  Google Scholar 

  • Valverde F, López-Mascaraque L, De Carlos JA (1989) Structure of the nucleus olfactorius anterior of the hedgehog (Erinaceus europaeus). J Comp Neurol 279:581–600

    CAS  PubMed  Google Scholar 

  • Vega MD, Barrio M, Quintela LA et al (2012) Evolución del manejo reproductivo en cunicultura. ITEA 108:172–190

    Google Scholar 

  • Verga M, Luzi F, Carenzi C (2007) Effects of husbandry and management systems on physiology and behavior of farmed and laboratory rabbits. Horm Behav 52:122–129

    PubMed  Google Scholar 

  • Verhaagen J, Oestreicher AB, Gispen WH et al (1989) The expression of the growth associated protein B50/GAP43 in the olfactory system of neonatal and adult rats. J Neurosci 9:683–691

    CAS  PubMed  PubMed Central  Google Scholar 

  • Villamayor PR, Cifuentes JM, Fdz-de-Troconiz P et al (2018) Morphological and immunohistochemical study of the rabbit vomeronasal organ. J Anat 233:814–827

    CAS  PubMed  Google Scholar 

  • Wagner S, Gresser AL, Torello AT et al (2006) A multireceptor genetic approach uncovers an ordered integration of VNO sensory inputs in the accessory olfactory bulb. Neuron 50:697–709

    CAS  PubMed  Google Scholar 

  • Wharton Young M (1936) The nuclear pattern and fiber connections of the non-cortical centers of the telencephalon of the rabbit (Lepus cuniculus). J Comp Neurol 65:295–401

    Google Scholar 

  • Wyatt TD (2003) Pheromones and animal behaviour: communication by smell and taste. Cambridge University Press, Cambridge

    Google Scholar 

  • Wysocki CJ (1979) Neurobehavioral evidence for the involvement of the vomeronasal system in mammalian reproduction. Neurosci Biobehav Rev 3:301–341

    CAS  PubMed  Google Scholar 

  • Yokosuka M (2012) Histological properties of the glomerular layer in the mouse accessory olfactory bulb. Exp Anim 61:13–24

    CAS  PubMed  Google Scholar 

  • Yoon H, Enquist LW, Dulac C (2005) Olfactory inputs to hypothalamic neurons controlling reproduction and fertility. Cell 123:669–682

    CAS  PubMed  Google Scholar 

  • Zufall F, Leinders-Zufall T (2007) Mammalian pheromone sensing. Curr Opin Neurobiol 17:483–489

    CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank COGAL SL (Pontevedra, Spain) for providing most of the animals employed in this study. Special thanks are due to Alejandro García MD, DVM for his artistic drawing of the AOB topography. We also thank Professor Ignacio Salazar, for his support and constant encouragement during his fruitful period as Head of the Department of Anatomy.

Funding

This work was supported by a University of Santiago de Compostela grant [1551-8179] to PSQ.

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Correspondence to Pablo Sanchez-Quinteiro.

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All procedures performed in this study involving living animals were in accordance with the ethical standards of the Institutional Animal Care Committee of the Universidad de Santiago de Compostela under procedure number MR110250.

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Villamayor, P.R., Cifuentes, J.M., Quintela, L. et al. Structural, morphometric and immunohistochemical study of the rabbit accessory olfactory bulb. Brain Struct Funct 225, 203–226 (2020). https://doi.org/10.1007/s00429-019-01997-4

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