Pheromone Sensing in Mammals: A Review of the Vomeronasal System

  1. Torres, Mateo V. 1
  2. Ortiz-Leal, Irene 1
  3. Sanchez-Quinteiro, Pablo 1
  1. 1 Department of Anatomy, Animal Production and Clinical Veterinary Sciences, Faculty of Veterinary, University of Santiago de Compostela, Av. Carballo Calero s/n, 27002 Lugo, Spain
Revista:
Anatomia

ISSN: 2813-0545

Ano de publicación: 2023

Volume: 2

Número: 4

Páxinas: 346-413

Tipo: Artigo

DOI: 10.3390/ANATOMIA2040031 GOOGLE SCHOLAR lock_openAcceso aberto editor

Outras publicacións en: Anatomia

Resumo

first_pagesettingsOrder Article ReprintsOpen AccessReviewPheromone Sensing in Mammals: A Review of the Vomeronasal Systemby Mateo V. Torres †ORCID,Irene Ortiz-Leal †ORCID andPablo Sanchez-Quinteiro *ORCIDDepartment of Anatomy, Animal Production and Clinical Veterinary Sciences, Faculty of Veterinary, University of Santiago de Compostela, Av. Carballo Calero s/n, 27002 Lugo, Spain*Author to whom correspondence should be addressed.†These authors contributed equally to this work.Anatomia 2023, 2(4), 346-413; https://doi.org/10.3390/anatomia2040031Submission received: 27 August 2023 / Revised: 14 October 2023 / Accepted: 7 November 2023 / Published: 9 November 2023(This article belongs to the Special Issue Advances in Anatomy and Its History)Downloadkeyboard_arrow_down Browse Figures Versions NotesAbstractThis review addresses the role of chemical communication in mammals, giving special attention to the vomeronasal system in pheromone-mediated interactions. The vomeronasal system influences many social and sexual behaviors, from reproduction to species recognition. Interestingly, this system shows greater evolutionary variability compared to the olfactory system, emphasizing its complex nature and the need for thorough research. The discussion starts with foundational concepts of chemocommunication, progressing to a detailed exploration of olfactory systems. The neuroanatomy of the vomeronasal system stands in contrast with that of the olfactory system. Further, the sensory part of the vomeronasal system, known as the vomeronasal organ, and the integration center of this information, called the accessory olfactory bulb, receive comprehensive coverage. Secondary projections of both the olfactory and vomeronasal systems receive attention, especially in relation to the dual olfactory hypothesis. The review concludes by examining the organization of the vomeronasal system in four distinct mammalian groups: rodents, marsupials, herpestids, and bovids. The aim is to highlight the unique morphofunctional differences resulting from the adaptive changes each group experienced.

Referencias bibliográficas

  • Stevens, M. (2013). Sensory Ecology, Behaviour, and Evolution, Oxford University Press.
  • Wyatt, T.D. (2003). Pheromones and Animal Behaviour: Communication by Smell and Taste, Cambridge University Press.
  • Wood, (1983), J. Chem. Educ., 60, pp. 531, 10.1021/ed060p531
  • Hudson, (2007), Vet. Mex., 38, pp. 105
  • Kokocińska-Kusiak, A., Woszczyło, M., Zybala, M., Maciocha, J., Barłowska, K., and Dzięcioł, M. (2021). Canine Olfaction: Physiology, Behavior, and Possibilities for Practical Applications. Animals, 11.
  • Iovino, (2019), Endocr. Metab. Immune Disord. Drug Targets, 19, pp. 472, 10.2174/1871530319666190131155310
  • Beruter, (1973), Biochem. Biophys. Res. Commun., 53, pp. 264, 10.1016/0006-291X(73)91429-0
  • Wilson, E.O. (1970). Chemical Ecology, Academic Press.
  • Surov, (2016), Biol. Bull. Russ. Acad. Sci., 43, pp. 1175, 10.1134/S1062359016110157
  • Villamayor, (2021), Sci. Rep., 11, pp. 8865, 10.1038/s41598-021-88317-1
  • Saraiva, (2015), Sci. Rep., 5, pp. 11487, 10.1038/srep11487
  • Meister, (2015), eLife, 4, pp. e07865, 10.7554/eLife.07865
  • Mollo, (2017), Nat. Prod. Rep., 34, pp. 496, 10.1039/C7NP00008A
  • Hepper, (2006), Chem. Senses, 31, pp. 207, 10.1093/chemse/bjj020
  • Weissburg, (2002), J. Chem. Ecol., 28, pp. 1953, 10.1023/A:1020741710060
  • Nordlund, (1976), J. Chem. Ecol., 2, pp. 211, 10.1007/BF00987744
  • Law, (1971), Annu. Rev. Biochem., 40, pp. 533, 10.1146/annurev.bi.40.070171.002533
  • Calcagnile, M., Tredici, S.M., Talà, A., and Alifano, P. (2019). Bacterial Semiochemicals and Transkingdom Interactions with Insects and Plants. Insects, 10.
  • Schulz, (2004), The Chemistry of Pheromones and Other Semiochemicals II, Volume 240, pp. 231, 10.1007/b98318
  • Apfelbach, (2015), Front. Neurosci., 9, pp. 263, 10.3389/fnins.2015.00263
  • Dicke, (1988), Funct. Ecol., 2, pp. 131, 10.2307/2389687
  • Breithaupt, T., and Thiel, M. (2010). Chemical Communication in Crustaceans, Springer.
  • Sbarbati, (2006), Cells Tissues Organs, 183, pp. 206, 10.1159/000096511
  • Blum, (1996), Annu. Rev. Entomol., 41, pp. 353, 10.1146/annurev.en.41.010196.002033
  • Gallie, (1997), Plant Physiol., 115, pp. 1461, 10.1104/pp.115.4.1461
  • Apfelbach, (2005), Neurosci. Biobehav. Rev., 29, pp. 1123, 10.1016/j.neubiorev.2005.05.005
  • Dunkelblum, (1996), Bioorg. Med. Chem., 4, pp. 489, 10.1016/0968-0896(96)00030-2
  • Cavill, (1965), Science, 149, pp. 1337, 10.1126/science.149.3690.1337
  • Mattiacci, (1994), J. Chem. Ecol., 20, pp. 2229, 10.1007/BF02033199
  • Stowe, (1995), Proc. Natl. Acad. Sci. USA, 92, pp. 23, 10.1073/pnas.92.1.23
  • Han, (2002), J. Chem. Ecol., 28, pp. 2203, 10.1023/A:1021045231501
  • Pernaa, (2011), J. Chem. Educ., 88, pp. 1644, 10.1021/ed900050g
  • Kasinger, H., Bauer, B., and Denzinger, J. (2008, January 20–24). The Meaning of Semiochemicals to the Design of Self-Organizing Systems. Proceedings of the 2008 Second IEEE International Conference on Self-Adaptive and Self-Organizing Systems, Venezia, Italy.
  • Karlson, (1959), Nature, 183, pp. 55, 10.1038/183055a0
  • Butenandt, (1959), Z. Naturforschg. B, 14, pp. 283
  • Wilson, (1965), Science, 149, pp. 1064, 10.1126/science.149.3688.1064
  • Conte, (2008), Annu. Rev. Entomol., 53, pp. 523, 10.1146/annurev.ento.52.110405.091434
  • Cork, (2003), Bangladesh J. Entomol., 13, pp. 1
  • Liberles, (2014), Annu. Rev. Physiol., 76, pp. 151, 10.1146/annurev-physiol-021113-170334
  • Brennan, (2006), Nature, 444, pp. 308, 10.1038/nature05404
  • Beauchamp, G.K., Doty, R.L., Moulton, D.G., and Mugford, R.A. (1976). Mammalian Olfaction, Reproductive Processes, and Behavior, Elsevier.
  • Brown, (1979), Advances in the Study of Behavior, Volume 10, pp. 103, 10.1016/S0065-3454(08)60094-7
  • Booth, (1992), Oxf. Rev. Reprod. Biol., 14, pp. 263
  • Schaal, (2003), Nature, 424, pp. 68, 10.1038/nature01739
  • Apps, (2015), Nat. Prod. Rep., 32, pp. 1131, 10.1039/C5NP00029G
  • Ferrero, (2013), Nature, 502, pp. 368, 10.1038/nature12579
  • Lin, (2005), Nature, 434, pp. 470, 10.1038/nature03414
  • Novotny, (1985), Proc. Natl. Acad. Sci. USA, 82, pp. 2059, 10.1073/pnas.82.7.2059
  • Singer, (1976), Science, 191, pp. 948, 10.1126/science.1251205
  • Dorries, (1995), Physiol. Behav., 57, pp. 255, 10.1016/0031-9384(94)00225-T
  • Rasmussen, (2003), Biochem. Soc. Trans., 31, pp. 137, 10.1042/bst0310137
  • Brown, (1970), BioScience, 20, pp. 21, 10.2307/1294753
  • Lass, (2002), Oecologia, 132, pp. 344, 10.1007/s00442-002-0982-9
  • Weldon, (1980), J. Chem. Ecol., 6, pp. 719, 10.1007/BF00987681
  • Pasteels, (1982), J. Chem. Ecol., 8, pp. 1079, 10.1007/BF00987889
  • Ruther, (2002), Chemoecology, 12, pp. 161, 10.1007/PL00012664
  • Ayelo, (2021), Front. Ecol. Evol., 9, pp. 641974, 10.3389/fevo.2021.641974
  • Schonewolf, (2006), J. Chem. Ecol., 32, pp. 1565, 10.1007/s10886-006-9070-7
  • Reinecke, (2002), Naturwissenschaften, 89, pp. 265, 10.1007/s00114-002-0314-2
  • Jones, (1971), Science, 173, pp. 842, 10.1126/science.173.3999.842
  • Acree, (1968), Science, 161, pp. 1346, 10.1126/science.161.3848.1346
  • Thibout, (1995), Experientia, 51, pp. 1073, 10.1007/BF01946919
  • Schoeppner, (2005), Ecol. Lett., 8, pp. 505, 10.1111/j.1461-0248.2005.00744.x
  • Arimura, (2004), Plant. Physiol., 135, pp. 1976, 10.1104/pp.104.042929
  • Reinecke, (2006), J. Appl. Entomol., 130, pp. 171, 10.1111/j.1439-0418.2006.01041.x
  • Briand, (2004), Peptides, 25, pp. 1545, 10.1016/j.peptides.2003.10.026
  • Altmann, (1987), Appl. Anim. Behav. Sci., 18, pp. 67, 10.1016/0168-1591(87)90255-3
  • Salazar, (1996), Anat. Histol. Embryol., 25, pp. 49, 10.1111/j.1439-0264.1996.tb00059.x
  • Barja, (2010), Biochem. Syst. Ecol., 38, pp. 1096, 10.1016/j.bse.2010.10.014
  • Surowiec, (2020), Sci. Rep., 10, pp. 5349, 10.1038/s41598-020-62280-9
  • Ewer, R.F. (1968). Ethology of Mammals, Springer.
  • Bradshaw, J.W.S., and Cameron-Beaumont, C.L. (2000). The Domestic Cat: The Biology of Its Behaviour, Cambridge University Press.
  • Miyazaki, (2006), Chem. Biol., 13, pp. 1071, 10.1016/j.chembiol.2006.08.013
  • Krzymowski, (2003), Reprod. Biol., 3, pp. 241
  • Booth, (1984), J. Endocrinol., 100, pp. 195, 10.1677/joe.0.1000195
  • Pietras, (1981), Chem. Senses, 6, pp. 391, 10.1093/chemse/6.4.391
  • Murphy, (1970), Science, 167, pp. 302, 10.1126/science.167.3916.302
  • Michael, (1970), Nature, 225, pp. 84, 10.1038/225084a0
  • Goodwin, (1979), Science, 203, pp. 559, 10.1126/science.569903
  • Rivard, (1989), Chem. Senses, 14, pp. 273, 10.1093/chemse/14.2.273
  • Hayes, (2002), J. Chem. Ecol., 28, pp. 2613, 10.1023/A:1021452623055
  • Thiessen, (1968), Science, 160, pp. 432, 10.1126/science.160.3826.432
  • (1971), Anim. Behav., 19, pp. 141, 10.1016/S0003-3472(71)80149-5
  • Singer, (1974), Science, 183, pp. 860, 10.1126/science.183.4127.860
  • Macdonald, (1984), J. Zool., 202, pp. 341, 10.1111/j.1469-7998.1984.tb05087.x
  • Beauchamp, (1974), Physiol. Zool., 47, pp. 130, 10.1086/physzool.47.2.30155630
  • (1965), Z. Vergl. Physiol., 50, pp. 151, 10.1007/BF00302702
  • Stumpf, (2004), Cell Tissue Res., 315, pp. 59, 10.1007/s00441-003-0815-0
  • Yager, (1988), Experientia, 44, pp. 79, 10.1007/BF01960256
  • Izard, M.K. (1983). Pheromones and Reproduction in Mammals, Academic Press.
  • Melrose, (1971), Br. Vet. J., 127, pp. 497, 10.1016/S0007-1935(17)37337-2
  • Gosling, (1982), Z. Tierpsychol., 60, pp. 89, 10.1111/j.1439-0310.1982.tb00492.x
  • Eisenberg, (1972), Annu. Rev. Ecol. Syst., 3, pp. 1, 10.1146/annurev.es.03.110172.000245
  • Johnson, (1973), Anim. Behav., 21, pp. 521, 10.1016/S0003-3472(73)80012-0
  • Jones, (1974), Anim. Learn. Behav., 2, pp. 141, 10.3758/BF03199141
  • Hayes, (2003), J. Chem. Ecol., 29, pp. 1051, 10.1023/A:1023836319677
  • Wirant, (2007), Appl. Anim. Behav. Sci., 106, pp. 161, 10.1016/j.applanim.2006.07.005
  • Manser, (2008), Ethology, 114, pp. 174, 10.1111/j.1439-0310.2007.01455.x
  • Bronson, (1968), Reproduction, 15, pp. 131, 10.1530/jrf.0.0150131
  • Bronson, (1971), Reproduction, 25, pp. 279, 10.1530/jrf.0.0250279
  • Seitz, (1969), Z. Tierpsychol., 26, pp. 73, 10.1111/j.1439-0310.1969.tb01938.x
  • Harrington, (1982), Can. J. Zool., 60, pp. 776, 10.1139/z82-107
  • Sun, (1997), Anim. Behav., 54, pp. 493, 10.1006/anbe.1996.0440
  • Jordan, (2013), Ethology, 119, pp. 644, 10.1111/eth.12105
  • Ferkin, (1995), Anim. Behav., 49, pp. 37, 10.1016/0003-3472(95)80151-0
  • (1985), J. Chem. Ecol., 11, pp. 241, 10.1007/BF00988206
  • Kiyokawa, (2004), Horm. Behav., 45, pp. 122, 10.1016/j.yhbeh.2003.09.007
  • Boissy, (1998), Physiol. Behav., 63, pp. 489, 10.1016/S0031-9384(97)00466-6
  • Aleksiuk, (1968), J. Mammal., 49, pp. 759, 10.2307/1378741
  • Bartecki, (1990), J. Zool., 220, pp. 87, 10.1111/j.1469-7998.1990.tb04295.x
  • Tschanz, (2010), Z. Tierpsychol., 27, pp. 47, 10.1111/j.1439-0310.1970.tb01860.x
  • Wakabayashi, (2000), J. Vet. Med. Sci., 62, pp. 1067, 10.1292/jvms.62.1067
  • Eisenberg, (1963), Behavior, 22, pp. 16, 10.1163/156853963X00284
  • Hayes, (2002), J. Chem. Ecol., 28, pp. 363, 10.1023/A:1017942426467
  • Laska, (2007), Primates, 48, pp. 160, 10.1007/s10329-006-0019-9
  • Xu, (1995), J. Mammal., 76, pp. 1238, 10.2307/1382617
  • Breer, (2006), Cell. Mol. Life Sci., 63, pp. 1465, 10.1007/s00018-006-6108-5
  • Munger, (2009), Nature, 459, pp. 521, 10.1038/459521a
  • Barrios, (2014), Microsc. Res. Tech., 77, pp. 1052, 10.1002/jemt.22436
  • (1906), Arch. Pedagog. Cienc. Afines, 1, pp. 216
  • Salazar, (2019), Handbook of Clinical Neurology, Volume 164, pp. 47, 10.1016/B978-0-444-63855-7.00004-6
  • McCotter, (1912), Anat. Rec., 6, pp. 299, 10.1002/ar.1090060802
  • Salazar, (2016), Anat. Rec., 299, pp. 1488, 10.1002/ar.23470
  • Barrios, (2014), Front. Neuroanat., 8, pp. 63, 10.3389/fnana.2014.00063
  • Fleischer, (2010), Histol. Histopathol., 25, pp. 909
  • Storan, (2006), J. Comp. Neurol., 494, pp. 834, 10.1002/cne.20858
  • Torres, (2020), J. Anat., 237, pp. 890, 10.1111/joa.13254
  • Ogura, T., Krosnowski, K., Zhang, L., Bekkerman, M., and Lin, W. (2010). Chemoreception Regulates Chemical Access to Mouse Vomeronasal Organ: Role of Solitary Chemosensory Cells. PLoS ONE, 5.
  • Juilfs, (1997), Proc. Natl. Acad. Sci. USA, 94, pp. 3388, 10.1073/pnas.94.7.3388
  • (2012), Front. Neuroanat., 6, pp. 23
  • Valverde, (1989), J. Comp. Neurol., 279, pp. 581, 10.1002/cne.902790407
  • Villamayor, (2020), Brain Struct. Funct., 225, pp. 203, 10.1007/s00429-019-01997-4
  • Torres, (2023), Front. Neuroanat., 16, pp. 1097467, 10.3389/fnana.2022.1097467
  • Menco, (1992), Microsc. Res. Tech., 22, pp. 215, 10.1002/jemt.1070220303
  • Dryer, (1999), Trends Pharmacol. Sci., 20, pp. 413, 10.1016/S0165-6147(99)01381-4
  • Zhang, (2002), Nat. Neurosci., 5, pp. 124, 10.1038/nn800
  • Malnic, (1999), Cell, 96, pp. 713, 10.1016/S0092-8674(00)80581-4
  • Crespo, (2019), Anat. Rec., 302, pp. 405, 10.1002/ar.23816
  • Mombaerts, (1996), Cell, 87, pp. 675, 10.1016/S0092-8674(00)81387-2
  • Price, (1971), J. Anat., 110, pp. 105
  • Shin, (2000), J. Neurocytol., 29, pp. 147, 10.1023/A:1026548020851
  • Salazar, (1995), Ann. Anat., 177, pp. 475, 10.1016/S0940-9602(11)80156-1
  • Villamayor, (2018), J. Anat., 233, pp. 814, 10.1111/joa.12884
  • (1984), Gegenbaurs Morphol. Jahrb., 130, pp. 501
  • Salazar, (2008), J. Anat., 212, pp. 686, 10.1111/j.1469-7580.2008.00889.x
  • Wysocki, (1979), Neurosci. Biobehav. Rev., 3, pp. 301, 10.1016/0149-7634(79)90015-0
  • Salazar, (2003), Brain Res., 979, pp. 15, 10.1016/S0006-8993(03)02835-X
  • Ressler, (1993), Cell, 73, pp. 597, 10.1016/0092-8674(93)90145-G
  • Zapiec, (2020), Cell Rep., 30, pp. 4220, 10.1016/j.celrep.2020.02.110
  • Trinh, (2003), Nat. Neurosci., 6, pp. 519, 10.1038/nn1039
  • Hohenbrink, P., Mundy, N.I., Zimmermann, E., and Radespiel, U. (2013). First Evidence for Functional Vomeronasal 2 Receptor Genes in Primates. Biol. Lett., 9.
  • Marcos, (2007), J. Comp. Neurol., 504, pp. 346, 10.1002/cne.21455
  • (1973), Z. Anat. Entwickl. Gesch., 140, pp. 39, 10.1007/BF00520716
  • Fleischer, (2007), Chem. Senses, 32, pp. 623, 10.1093/chemse/bjm032
  • Fleischer, (2006), J. Neurochem., 98, pp. 543, 10.1111/j.1471-4159.2006.03894.x
  • Schmid, (2010), J. Neurosci., 30, pp. 7563, 10.1523/JNEUROSCI.0608-10.2010
  • (1943), Arch. Ital. Anat. Embriol., 48, pp. 157
  • Tian, (2004), J. Neurosci., 24, pp. 8383, 10.1523/JNEUROSCI.2222-04.2004
  • Weiler, (2003), Chem. Senses, 28, pp. 581, 10.1093/chemse/bjg047
  • Ma, (2003), J. Neurosci., 23, pp. 317, 10.1523/JNEUROSCI.23-01-00317.2003
  • Marshall, (1986), Brain Res., 366, pp. 329, 10.1016/0006-8993(86)91312-0
  • Wysocki, (1980), Science, 207, pp. 781, 10.1126/science.7352288
  • Tizzano, M., Cristofoletti, M., Sbarbati, A., and Finger, T.E. (2011). Expression of Taste Receptors in Solitary Chemosensory Cells of Rodent Airways. BMC Pulm. Med., 11.
  • Silver, (1982), Physiol. Behav., 28, pp. 927, 10.1016/0031-9384(82)90216-5
  • Filoramo, (2009), J. Exp. Zool., 311, pp. 20, 10.1002/jez.492
  • Kondoh, (2023), J. Anat., 243, pp. 486, 10.1111/joa.13873
  • Reiss, J.O., and Eisthen, H.L. (2008). Sensory Evolution on the Threshold: Adaptations in Secondarily Aquatic Vertebrates, University of California Press.
  • Berliner, (1998), Ann. N. Y. Acad. Sci., 855, pp. 373, 10.1111/j.1749-6632.1998.tb10595.x
  • Tirindelli, (2021), Cell Tissue Res., 383, pp. 367, 10.1007/s00441-020-03376-6
  • Shinohara, (1992), J. Neurosci., 12, pp. 1275, 10.1523/JNEUROSCI.12-04-01275.1992
  • Dulac, (1995), Cell, 83, pp. 195, 10.1016/0092-8674(95)90161-2
  • Herrada, (1997), Cell, 90, pp. 763, 10.1016/S0092-8674(00)80536-X
  • Matsunami, (1997), Cell, 90, pp. 775, 10.1016/S0092-8674(00)80537-1
  • Ryba, (1997), Neuron, 19, pp. 371, 10.1016/S0896-6273(00)80946-0
  • Challet, (2009), Nature, 459, pp. 574, 10.1038/nature08029
  • Brennan, (2001), Cell. Mol. Life Sci., 58, pp. 546, 10.1007/PL00000880
  • Papes, (2010), Cell, 141, pp. 692, 10.1016/j.cell.2010.03.037
  • Halpern, (1984), Trends Neurosci., 7, pp. 472, 10.1016/S0166-2236(84)80258-1
  • Placyk, (2002), J. Chem. Ecol., 28, pp. 1017, 10.1023/A:1015213918739
  • Halpern, (2005), Nutr. Metab., 2, pp. 6, 10.1186/1743-7075-2-6
  • Dagg, (1970), Mammalia, 34, pp. 686, 10.1515/mamm.1970.34.4.686
  • Estes, (1972), Mammalia, 36, pp. 315, 10.1515/mamm.1972.36.3.315
  • Müller-Schwarze, D., and Silverstein, R.M. (1983). Chemical Signals in Vertebrates 3, Springer.
  • Hart, L.A., and Hart, B.L. (2023). Flehmen, Osteophagia, and Other Behaviors of Giraffes (Giraffa giraffa angolensis): Vomeronasal Organ Adaptation. Animals, 13.
  • Jacobson, (1813), Vet. Selsk. Skr., 2, pp. 209
  • Ruysch, F. (1703). Thesaurus Anatomicus Tertius, J. Wolters.
  • Dursy, E. (1869). Zur Entwicklungsgeschichte des Kopfes des Menschen und der höheren Wirbelthiere: Mit Holzschnitten und einem Atlas von neun Kupfertafeln mit erklärendem Texte, H. Laupp.
  • Kölliker, A. (1877). Festschrift zu dem 40 jährign Professoren-Jubiläum des Herrn Franz von Rinecker 31 März 1877, Wilhelm Engelmann.
  • Balogh, (1860), Akad. Der Wiss. Wien., 42, pp. 449
  • Klein, (1881), J. Cell Sci., 2, pp. 98, 10.1242/jcs.s2-21.81.98
  • Piana, (1882), Deusch. Zeitsch. f. Tiermedizin, 7, pp. 325
  • Retzius, (1894), Biol. Untersuch. Neue Folge, 6, pp. 48
  • Gudden, (1870), Arch. Psychiatr. Nervenkr., 2, pp. 693, 10.1007/BF02046772
  • (1902), Rev. Micros., 1, pp. 141
  • Vandenbergh, (1969), Endocrinology, 84, pp. 658, 10.1210/endo-84-3-658
  • Whitten, (1956), J. Endocrinol., 13, pp. 399, 10.1677/joe.0.0130399
  • Powers, (1975), Science, 187, pp. 961, 10.1126/science.1145182
  • Grus, (2006), Bioessays, 28, pp. 709, 10.1002/bies.20432
  • (2010), Front. Neuroanat., 4, pp. 130
  • Nakamuta, (2012), Anat. Rec., 295, pp. 481, 10.1002/ar.22415
  • Nakamuta, (2023), J. Comp. Neurol., 531, pp. 116, 10.1002/cne.25416
  • Wittmer, (2017), J. Morphol., 278, pp. 791, 10.1002/jmor.20673
  • Swaney, (2009), Behav. Brain Res., 200, pp. 239, 10.1016/j.bbr.2008.09.039
  • Thewissen, J.G.M. (2008). Sensory Evolution on the Threshold: Adaptations in Secondarily Aquatic Vertebrates, University of California Press.
  • Suzuki, (2018), Mol. Biol. Evol., 35, pp. 2928
  • Breathnach, (1960), Biol. Rev., 35, pp. 187, 10.1111/j.1469-185X.1960.tb01414.x
  • McGowen, (2008), Syst. Biol., 57, pp. 574, 10.1080/10635150802304787
  • Kishida, (2021), Cell Tissue Res., 383, pp. 353, 10.1007/s00441-020-03382-8
  • Halpern, (1992), Hormones, Brain, and Behaviour. Biology of the Reptilia, Volume 18, pp. 423
  • Schwenk, (1995), Trends Ecol. Evol., 10, pp. 7, 10.1016/S0169-5347(00)88953-3
  • Kondoh, (2010), J. Morphol., 271, pp. 1197, 10.1002/jmor.10864
  • Kondoh, (2012), Anat. Histol. Embryol., 41, pp. 41, 10.1111/j.1439-0264.2011.01101.x
  • Hatanaka, (1993), Brain Behav. Evol., 41, pp. 183, 10.1159/000113836
  • Parsons, (1959), Bull. Mus. Comp. Zool. Harv. Coll., 120, pp. 261
  • Parsons, (1967), Am. Zool., 7, pp. 397, 10.1093/icb/7.3.397
  • Houck, (2009), Annu. Rev. Physiol., 71, pp. 161, 10.1146/annurev.physiol.010908.163134
  • Eisthen, (2000), Philos. Trans. R. Soc. Lond. B, 355, pp. 1209, 10.1098/rstb.2000.0669
  • Silva, (2017), Annu. Rev. Anim. Biosci., 5, pp. 353, 10.1146/annurev-animal-022516-022801
  • Bhatnagar, (1998), Microsc. Res. Tech., 43, pp. 465, 10.1002/(SICI)1097-0029(19981215)43:6<465::AID-JEMT1>3.0.CO;2-1
  • Suárez, R., Fernández-Aburto, P., Manger, P.R., and Mpodozis, J. (2011). Deterioration of the Gαo Vomeronasal Pathway in Sexually Dimorphic Mammals. PLoS ONE, 6.
  • Kondoh, (2017), Brain Behav. Evol., 90, pp. 224, 10.1159/000479180
  • Tomiyasu, (2022), J. Anat., 241, pp. 809, 10.1111/joa.13671
  • Grus, (2007), Mol. Biol. Evol., 24, pp. 2153, 10.1093/molbev/msm157
  • Cartmill, (1974), Science, 184, pp. 436, 10.1126/science.184.4135.436
  • Heesy, (2001), J. Hum. Evol., 40, pp. 111, 10.1006/jhev.2000.0447
  • Wang, (2010), Genom. Biol. Evol., 2, pp. 277, 10.1093/gbe/evq020
  • Garrett, (2013), Anat. Rec., 296, pp. 1881, 10.1002/ar.22828
  • Smith, (2011), Anat. Rec., 294, pp. 2158, 10.1002/ar.21509
  • Smith, (2001), J. Anat., 198, pp. 77, 10.1046/j.1469-7580.2001.19810077.x
  • Smith, (2001), Anat. Rec., 265, pp. 176, 10.1002/ar.1152
  • Boehm, (1994), Dev. Brain Res., 82, pp. 175, 10.1016/0165-3806(94)90160-0
  • Hansen, (1996), Eur. J. Oral Sci., 104, pp. 34, 10.1111/j.1600-0722.1996.tb00043.x
  • Humphrey, (1940), J. Comp. Neurol., 73, pp. 431, 10.1002/cne.900730305
  • Moran, (1991), J. Steroid Biochem. Mol. Biol., 39, pp. 545, 10.1016/0960-0760(91)90251-Y
  • Hazem, (1998), Acta Otolaryngol., 118, pp. 409, 10.1080/00016489850183520
  • Witt, (2006), Int. Rev. Cytol., 248, pp. 209, 10.1016/S0074-7696(06)48004-9
  • Meredith, (2001), Chem. Senses, 26, pp. 433, 10.1093/chemse/26.4.433
  • Zhang, (2003), Proc. Natl. Acad. Sci. USA, 100, pp. 8337, 10.1073/pnas.1331721100
  • Smith, (2014), Anat. Rec., 297, pp. 2196, 10.1002/ar.23035
  • Negus, (1956), J. Anat., 90, pp. 515
  • Salazar, (1998), Microsc. Res. Tech., 41, pp. 492, 10.1002/(SICI)1097-0029(19980615)41:6<492::AID-JEMT5>3.0.CO;2-P
  • Trotier, (1998), J. Exp. Biol., 201, pp. 2913, 10.1242/jeb.201.21.2913
  • Menco, (1997), Chem. Senses, 22, pp. 295, 10.1093/chemse/22.3.295
  • Menco, (2001), J. Comp. Neurol., 438, pp. 468, 10.1002/cne.1329
  • Salazar, (2006), Anat. Rec., 288, pp. 1009, 10.1002/ar.a.20366
  • Jungblut, (2021), Cell Tissue Res., 383, pp. 289, 10.1007/s00441-020-03330-6
  • Mendoza, (1987), Cell Tissue Res., 247, pp. 457, 10.1007/BF00218328
  • Takami, (1995), Cell Tissue Res., 280, pp. 211, 10.1007/BF00307791
  • Kondoh, (2020), Acta Histochem., 122, pp. 151515, 10.1016/j.acthis.2020.151515
  • Salazar, (1997), Anat. Rec., 247, pp. 129, 10.1002/(SICI)1097-0185(199701)247:1<129::AID-AR15>3.0.CO;2-R
  • Meredith, (1979), J. Physiol., 286, pp. 301, 10.1113/jphysiol.1979.sp012620
  • Eccles, (1982), Physiol. Behav., 28, pp. 1011, 10.1016/0031-9384(82)90168-8
  • Meredith, (1994), Physiol. Behav., 56, pp. 345, 10.1016/0031-9384(94)90205-4
  • Halpern, (1998), Chem. Senses, 23, pp. 477, 10.1093/chemse/23.4.477
  • Kretschmer, (2018), Trends Immunol., 39, pp. 815, 10.1016/j.it.2018.08.005
  • Villamayor, (2021), Genomics, 113, pp. 2240, 10.1016/j.ygeno.2021.05.007
  • Liberles, (2009), Proc. Natl. Acad. Sci. USA, 106, pp. 9842, 10.1073/pnas.0904464106
  • Bufe, (2019), Nat. Commun., 10, pp. 4889, 10.1038/s41467-019-12842-x
  • Swain, (1983), Immunol. Rev., 74, pp. 129, 10.1111/j.1600-065X.1983.tb01087.x
  • Singh, (2001), Reproduction, 121, pp. 529, 10.1530/rep.0.1210529
  • Brennan, (2006), Philos. Trans. R. Soc. B, 361, pp. 2061, 10.1098/rstb.2006.1931
  • (2012), Self and Nonself, Volume 738, pp. 290, 10.1007/978-1-4614-1680-7_17
  • Yamazaki, (2007), Advances in Genetics, Volume 59, pp. 129, 10.1016/S0065-2660(07)59005-X
  • Brennan, (2004), Science, 306, pp. 1033, 10.1126/science.1102818
  • Konjević, D., Erman, V., Bujanić, M., Svetličić, I., Arbanasić, H., Lubura Strunjak, S., and Galov, A. (2022). Wild Boar (Sus scrofa)—Fascioloides Magna Interaction from the Perspective of the MHC Genes. Pathogens, 11.
  • Milinski, (2005), Proc. Natl. Acad. Sci. USA, 102, pp. 4414, 10.1073/pnas.0408264102
  • Lane, (2000), Nature, 405, pp. 792, 10.1038/35015572
  • Spehr, (2006), J. Neurosci., 26, pp. 1961, 10.1523/JNEUROSCI.4939-05.2006
  • Liman, (1999), Proc. Natl. Acad. Sci. USA, 96, pp. 5791, 10.1073/pnas.96.10.5791
  • Leypold, (2002), Proc. Natl. Acad. Sci. USA, 99, pp. 6376, 10.1073/pnas.082127599
  • Stowers, (2002), Science, 295, pp. 1493, 10.1126/science.1069259
  • Zhang, (2014), Science, 346, pp. 1311, 10.1126/science.1251385
  • Shi, (2007), Genome Res., 17, pp. 166, 10.1101/gr.6040007
  • Young, (2010), Genome Res., 20, pp. 10, 10.1101/gr.098913.109
  • Rodriguez, (2000), Nat. Genet., 26, pp. 18, 10.1038/79124
  • Baum, (2009), Annu. Rev. Physiol., 71, pp. 141, 10.1146/annurev.physiol.010908.163137
  • Omura, (2014), Cell Rep., 8, pp. 583, 10.1016/j.celrep.2014.06.010
  • Omura, (2015), Mol. Cell. Neurosci., 65, pp. 114, 10.1016/j.mcn.2015.02.012
  • Schneider, (2012), Chem. Senses, 37, pp. 567, 10.1093/chemse/bjs040
  • Mpodozis, (2009), Behav. Brain Res., 198, pp. 306, 10.1016/j.bbr.2008.11.009
  • Halpern, (1995), Brain Res., 677, pp. 157, 10.1016/0006-8993(95)00159-N
  • Young, (2007), Trends Genet., 23, pp. 212, 10.1016/j.tig.2007.03.004
  • Salazar, (2013), Anat. Rec., 296, pp. 146, 10.1002/ar.22617
  • Hayakawa, (2018), Gene, 642, pp. 343, 10.1016/j.gene.2017.11.048
  • Kishimoto, (1993), Brain Res., 610, pp. 325, 10.1016/0006-8993(93)91417-Q
  • Verhaagen, (1989), J. Neurosci., 9, pp. 683, 10.1523/JNEUROSCI.09-02-00683.1989
  • Salazar, (1998), Anat. Embryol., 198, pp. 331, 10.1007/s004290050188
  • Ichikawa, (1992), Neurosci. Res., 13, pp. 73, 10.1016/0168-0102(92)90035-B
  • Ibarra-Soria, X., Levitin, M.O., Saraiva, L.R., and Logan, D.W. (2014). The Olfactory Transcriptomes of Mice. PLoS Genet., 10.
  • Francia, (2015), Genom. Biol. Evol., 7, pp. 272, 10.1093/gbe/evu283
  • Yohe, (2019), Genom. Biol. Evol., 11, pp. 2741, 10.1093/gbe/evz179
  • Haga, (2010), Nature, 466, pp. 118, 10.1038/nature09142
  • Silva, (2020), Genomics, 112, pp. 2778, 10.1016/j.ygeno.2020.03.015
  • Oboti, L., Ibarra-Soria, X., Pérez-Gómez, A., Schmid, A., Pyrski, M., Paschek, N., Kircher, S., Logan, D.W., Leinders-Zufall, T., and Zufall, F. (2015). Pregnancy and Estrogen Enhance Neural Progenitor-Cell Proliferation in the Vomeronasal Sensory Epithelium. BMC Biol., 13.
  • Villamayor, (2022), Front. Mol. Neurosci., 15, pp. 1034254, 10.3389/fnmol.2022.1034254
  • Segovia, (1982), Dev. Brain Res., 5, pp. 209, 10.1016/0165-3806(82)90160-2
  • Segovia, (1997), Brain Res. Bull., 44, pp. 377, 10.1016/S0361-9230(97)00217-7
  • Maico, (2003), Acta Biol. Hung., 54, pp. 263, 10.1556/ABiol.54.2003.3-4.5
  • Tai, (2004), Acta Theriol., 49, pp. 33, 10.1007/BF03192506
  • Peretto, (2001), Cell Tissue Res., 306, pp. 385, 10.1007/s00441-001-0471-1
  • Broom, (1900), Trans. R. Soc. Edinb., 39, pp. 231, 10.1017/S0080456800034074
  • (1984), Anat. Anz., 157, pp. 137
  • (2001), Zool. J. Linn. Soc., 131, pp. 459, 10.1111/j.1096-3642.2001.tb01322.x
  • Vaccarezza, (1981), J. Anat., 132, pp. 167
  • Mechin, V., Pageat, P., Teruel, E., and Asproni, P. (2021). Histological and Immunohistochemical Characterization of Vomeronasal Organ Aging in Mice. Animals, 11.
  • Weiler, (1999), Eur. J. Neurosci., 11, pp. 700, 10.1046/j.1460-9568.1999.00476.x
  • Giacobini, (2000), Dev. Brain Res., 123, pp. 33, 10.1016/S0165-3806(00)00080-8
  • Ibokwe, (2009), Anim. Res. Int., 6, pp. 932, 10.4314/ari.v6i1.48096
  • Wang, (2021), Acta Theriol. Sin., 41, pp. 685
  • Oikawa, (1994), Exp. Anim., 43, pp. 487, 10.1538/expanim1978.43.4_487
  • Jurcisek, (2003), Cells Tissues Organs, 174, pp. 136, 10.1159/000071154
  • Smith, (2007), Am. J. Primatol., 69, pp. 74, 10.1002/ajp.20328
  • Dennis, (2020), Anat. Rec., 303, pp. 318, 10.1002/ar.24060
  • Luckhaus, (1969), Anat. Anz., 124, pp. 477
  • Mahdy, (2019), J. Adv. Vet. Res., 6, pp. 506, 10.5455/javar.2019.f375
  • Elgayar, (2014), Anat. Histol. Embryol., 43, pp. 282, 10.1111/ahe.12073
  • Schneider, (2008), J. Anat., 213, pp. 93, 10.1111/j.1469-7580.2008.00933.x
  • Poran, (1998), Microsc. Res. Tech., 43, pp. 500, 10.1002/(SICI)1097-0029(19981215)43:6<500::AID-JEMT3>3.0.CO;2-H
  • Schneider, (2011), J. Anat., 219, pp. 229, 10.1111/j.1469-7580.2011.01393.x
  • Ashwell, (2012), Brain Behav. Evol., 79, pp. 45, 10.1159/000332804
  • Kondoh, D., Tanaka, Y., Kawai, Y.K., Mineshige, T., Watanabe, K., and Kobayashi, Y. (2021). Morphological and Histological Features of the Vomeronasal Organ in African Pygmy Hedgehog (Atelerix albiventris). Animals, 11.
  • Aland, (2016), J. Morphol., 277, pp. 1517, 10.1002/jmor.20593
  • Dennis, (2003), J. Anat., 203, pp. 329, 10.1046/j.1469-7580.2003.00200.x-i1
  • Salazar, (1996), J. Anat., 188, pp. 445
  • Tomiyasu, (2017), J. Anat., 231, pp. 749, 10.1111/joa.12673
  • Kelliher, (2001), Anat. Rec., 263, pp. 280, 10.1002/ar.1097
  • Salazar, (1998), Ann. Anat., 180, pp. 181, 10.1016/S0940-9602(98)80023-X
  • Salazar, (1997), Anat. Histol. Embryol., 26, pp. 179, 10.1111/j.1439-0264.1997.tb00122.x
  • Salazar, (2007), Microsc. Res. Tech., 70, pp. 752, 10.1002/jemt.20461
  • Ichikawa, (1999), J. Rep. Dev., 45, pp. 81, 10.1262/jrd.45.81
  • Yang, (2021), Acta Histochem., 123, pp. 151684, 10.1016/j.acthis.2021.151684
  • Park, (2014), Acta Histochem., 116, pp. 258, 10.1016/j.acthis.2013.08.003
  • Vedin, (2010), Brain Res., 1306, pp. 53, 10.1016/j.brainres.2009.10.012
  • Kondoh, (2017), Microsc. Res. Tech., 80, pp. 652, 10.1002/jemt.22843
  • Smith, (2002), Anat. Rec., 267, pp. 166, 10.1002/ar.10095
  • Meisami, (1998), Microsc. Res. Tech., 43, pp. 476, 10.1002/(SICI)1097-0029(19981215)43:6<476::AID-JEMT2>3.0.CO;2-V
  • Takami, (1990), Brain Res., 510, pp. 339, 10.1016/0006-8993(90)91387-V
  • Nakajima, (2013), Brain Res., 1503, pp. 16, 10.1016/j.brainres.2013.01.053
  • Vassar, (1994), Cell, 79, pp. 981, 10.1016/0092-8674(94)90029-9
  • Puche, (2002), Neuron, 35, pp. 1057, 10.1016/S0896-6273(02)00904-2
  • Crosby, (1941), J. Comp. Neurol., 74, pp. 309, 10.1002/cne.900740209
  • Allison, (1953), J. Comp. Neurol., 98, pp. 309, 10.1002/cne.900980206
  • Salazar, (2011), Microsc. Res. Tech., 74, pp. 1109, 10.1002/jemt.21002
  • (2008), J. Comp. Neurol., 510, pp. 309, 10.1002/cne.21790
  • Switzer, (1980), Brain Behav. Evol., 17, pp. 339, 10.1159/000121808
  • Baker, (1988), Brain Res., 450, pp. 69, 10.1016/0006-8993(88)91545-4
  • Gouda, (1990), Brain Res., 512, pp. 339, 10.1016/0006-8993(90)90645-R
  • Serby, M.J., and Chobor, K.L. (1992). Science of Olfaction, Springer.
  • Frahm, (1984), J. Hirnforsch., 25, pp. 537
  • Bonfanti, (1997), Neuroscience, 81, pp. 489, 10.1016/S0306-4522(97)00090-0
  • Crespo, (2021), Stem Cells, 39, pp. 1253, 10.1002/stem.3393
  • Inaki, (2004), J. Comp. Neurol., 479, pp. 243, 10.1002/cne.20270
  • Broadwell, (1975), J. Comp. Neurol., 163, pp. 329, 10.1002/cne.901630306
  • Schwob, (1984), J. Comp. Neurol., 223, pp. 177, 10.1002/cne.902230204
  • Takami, (1992), Brain Res., 588, pp. 317, 10.1016/0006-8993(92)91593-4
  • Takami, (1991), J. Comp. Neurol., 311, pp. 65, 10.1002/cne.903110106
  • Hinds, (1968), J. Comp. Neurol., 134, pp. 287, 10.1002/cne.901340304
  • Rall, (1966), Exp. Neurol., 14, pp. 44, 10.1016/0014-4886(66)90023-9
  • Corona, (2012), Front. Neuroanat., 6, pp. 15
  • Jia, (1999), J. Neurophysiol., 81, pp. 345, 10.1152/jn.1999.81.1.345
  • (2000), Genom. Res., 10, pp. 1958, 10.1101/gr.140600
  • Segovia, (1984), Dev. Brain Res., 16, pp. 312, 10.1016/0165-3806(84)90036-1
  • Yokosuka, (2012), Exp. Anim., 61, pp. 13, 10.1538/expanim.61.13
  • Frahm, (1980), J. Anat., 130, pp. 349
  • Jia, (2004), J. Morphol., 259, pp. 271, 10.1002/jmor.10166
  • Torres, (2022), Ann. Anat., 240, pp. 151881, 10.1016/j.aanat.2021.151881
  • Bird, (2021), Anat. Rec., 304, pp. 139, 10.1002/ar.24518
  • Bird, (2018), Proc. R. Soc. B, 285, pp. 20180100, 10.1098/rspb.2018.0100
  • Wynn, E.H., Sánchez-Andrade, G., Carss, K.J., and Logan, D.W. (2012). Genomic Variation in the Vomeronasal Receptor Gene Repertoires of Inbred Mice. BMC Genom., 13.
  • Ortiz-Leal, I., Torres, M.V., López-Callejo, L.N., Fidalgo, L.E., López-Beceiro, A., and Sanchez-Quinteiro, P. (2022). Comparative Neuroanatomical Study of the Main Olfactory Bulb in Domestic and Wild Canids: Dog, Wolf and Red Fox. Animals, 12.
  • Szumny, (2020), Front. Vet. Sci., 7, pp. 159, 10.3389/fvets.2020.00159
  • (2023), Vet. Rec. Case Rep., 11, pp. e571, 10.1002/vrc2.571
  • Pageat, (2003), Vet. Clin. N. Am. Small Anim. Pract., 33, pp. 187, 10.1016/S0195-5616(02)00128-6
  • Puglisi, I., Masucci, M., Cozzi, A., Teruel, E., Navarra, M., Cirmi, S., Pennisi, M.G., and Siracusa, C. (2022). Effects of a Novel Gel Formulation of Dog Appeasing Pheromone (DAP) on Behavioral and Physiological Stress Responses in Dogs Undergoing Clinical Examination. Animals, 12.
  • Asproni, (2016), J. Feline Med. Surg., 18, pp. 997, 10.1177/1098612X15606493
  • Asproni, P., Mainau, E., Cozzi, A., Carreras, R., Bienboire-Frosini, C., Teruel, E., and Pageat, P. (2022). Is There a Link between Vomeronasalitis and Aggression in Stable Social Groups of Female Pigs?. Animals, 12.
  • Mechin, (2022), Front. Vet. Sci., 9, pp. 936838, 10.3389/fvets.2022.936838
  • Mechin, V., Pageat, P., Boutry, M., Teruel, E., Portalier, C., and Asproni, P. (2023). Does the Environmental Air Impact the Condition of the Vomeronasal Organ? A Mouse Model for Intensive Farming. Animals, 13.
  • Salazar, (1994), Funct. Dev. Morphol., 4, pp. 113
  • Salazar, (1998), Anat. Histol. Embryol., 27, pp. 297, 10.1111/j.1439-0264.1998.tb00197.x
  • Salazar, (2003), Microsc. Res. Tech., 61, pp. 438, 10.1002/jemt.10362
  • Tirindelli, (1998), Trends Neurosci., 21, pp. 482, 10.1016/S0166-2236(98)01274-0
  • Alonso, (2001), J. Comp. Neurol., 432, pp. 389, 10.1002/cne.1110
  • Weruaga, (2001), J. Comp. Neurol., 429, pp. 554, 10.1002/1096-9861(20010122)429:4<554::AID-CNE4>3.0.CO;2-T
  • Weruaga, (2001), Chem. Senses, 26, pp. 7, 10.1093/chemse/26.1.7
  • Smithson, (2009), Brain Res., 1284, pp. 41, 10.1016/j.brainres.2009.06.011
  • Dehmelt, L., and Halpain, S. (2005). The MAP2/Tau Family of Microtubule-Associated Proteins. Genome Biol., 6.
  • Benowitz, (1990), Progress in Brain Research, Volume 86, pp. 309, 10.1016/S0079-6123(08)63187-8
  • Shapiro, (1997), J. Morphol., 234, pp. 109, 10.1002/(SICI)1097-4687(199711)234:2<109::AID-JMOR1>3.0.CO;2-7
  • Mugnaini, (1984), Neurosci. Lett., 47, pp. 221, 10.1016/0304-3940(84)90517-2
  • Aubert, (1995), J. Chem. Neuroanat., 9, pp. 99, 10.1016/0891-0618(95)00070-N
  • Woo, (1995), J. Comp. Neurol., 352, pp. 1, 10.1002/cne.903520102
  • Huang, (2017), J. Physiol., 595, pp. 3515, 10.1113/JP273945
  • Matsutani, (1988), J. Comp. Neurol., 272, pp. 331, 10.1002/cne.902720304
  • Lundberg, (1988), Histochemistry, 90, pp. 9, 10.1007/BF00495700
  • Nacher, (2001), Eur. J. Neurosci., 14, pp. 629, 10.1046/j.0953-816x.2001.01683.x
  • Takami, (1992), Brain Res., 598, pp. 337, 10.1016/0006-8993(92)90204-M
  • Taniguchi, (1993), Neurosci. Lett., 158, pp. 185, 10.1016/0304-3940(93)90260-R
  • Shapiro, (1995), J. Morphol., 224, pp. 331, 10.1002/jmor.1052240307
  • Hovis, (2012), J. Neurosci., 32, pp. 7907, 10.1523/JNEUROSCI.2399-11.2012
  • Raisman, (1972), Exp. Brain Res., 14, pp. 395, 10.1007/BF00235035
  • Scalia, (1975), J. Comp. Neurol., 161, pp. 31, 10.1002/cne.901610105
  • Winans, (1970), Science, 170, pp. 330, 10.1126/science.170.3955.330
  • Shipley, (1984), Brain Res. Bull., 12, pp. 669, 10.1016/0361-9230(84)90148-5
  • Dulac, (2006), Annu. Rev. Genet., 40, pp. 449, 10.1146/annurev.genet.39.073003.093937
  • Price, (1985), Chem. Senses, 10, pp. 239, 10.1093/chemse/10.2.239
  • Courtiol, (2015), Front. Neural Circuits, 9, pp. 49, 10.3389/fncir.2015.00049
  • Lanuza, (2016), Brain Struct. Funct., 221, pp. 1033, 10.1007/s00429-014-0954-y
  • Devor, (1976), J. Comp. Neurol., 166, pp. 31, 10.1002/cne.901660104
  • (2009), Prog. Neurobiol., 87, pp. 21, 10.1016/j.pneurobio.2008.09.010
  • Lanuza, (2014), Eur. J. Neurosci., 39, pp. 141, 10.1111/ejn.12393
  • Stowers, (2016), Curr. Opin. Neurobiol., 38, pp. 74, 10.1016/j.conb.2016.04.001
  • Novejarque, (2012), Front. Neuroanat., 6, pp. 33
  • Lo, (2011), Neuron, 72, pp. 938, 10.1016/j.neuron.2011.12.002
  • Trotier, (2011), Eur. Ann. Otorhinolaryngol. Head Neck Dis., 128, pp. 184, 10.1016/j.anorl.2010.11.008
  • Cadiz, B., Martinez-Garcia, F., and Lanuza, E. (2013). Chemical Signals in Vertebrates 12, Springer.
  • Mohrhardt, (2018), Chem. Senses, 43, pp. 667, 10.1093/chemse/bjy061
  • Carlsen, (1986), J. Comp. Neurol., 243, pp. 488, 10.1002/cne.902430405
  • (2022), eLife, 11, pp. e71965, 10.7554/eLife.71965
  • Liberia, (2015), Front. Neuroanat., 9, pp. 28, 10.3389/fnana.2015.00028
  • Brunert, (2020), Sci. Rep., 10, pp. 10696, 10.1038/s41598-020-67276-z
  • Gomez, (1992), J. Comp. Neurol., 317, pp. 195, 10.1002/cne.903170208
  • Fan, (2009), Neuroscience, 161, pp. 489, 10.1016/j.neuroscience.2009.03.065
  • Inbar, (2022), J. Comp. Neurol., 530, pp. 648, 10.1002/cne.25236
  • Drabik, (2022), Front. Neuroanat., 16, pp. 988015, 10.3389/fnana.2022.988015
  • Keverne, (1996), J. Physiol., 90, pp. 399
  • Brennan, (1995), Neuroscience, 69, pp. 1075, 10.1016/0306-4522(95)00309-7
  • Brennan, (2004), Horm. Behav., 46, pp. 231, 10.1016/j.yhbeh.2004.01.010
  • Takahashi, (2010), Brain Res., 1339, pp. 26, 10.1016/j.brainres.2010.03.104
  • Wilson, (2006), Annu. Rev. Neurosci., 29, pp. 163, 10.1146/annurev.neuro.29.051605.112950
  • Grus, (2009), Mol. Biol. Evol., 26, pp. 407, 10.1093/molbev/msn262
  • Smith, (1994), Behav. Process., 32, pp. 79, 10.1016/0376-6357(94)90029-9
  • Catania, (2006), Nature, 444, pp. 1024, 10.1038/4441024a
  • Johnson, (2002), Anat. Rec., 267, pp. 252, 10.1002/ar.10112
  • Garrosa, (1998), Microsc. Res. Tech., 41, pp. 456, 10.1002/(SICI)1097-0029(19980615)41:6<456::AID-JEMT2>3.0.CO;2-L
  • Sugai, (1997), Neuroscience, 79, pp. 871, 10.1016/S0306-4522(96)00690-2
  • Fieni, (2003), J. Physiol., 552, pp. 425, 10.1113/jphysiol.2003.052035
  • Torres, (2020), Sci. Rep., 10, pp. 13304, 10.1038/s41598-020-69994-w
  • Salazar, (2003), J. Anat., 202, pp. 503, 10.1046/j.1469-7580.2003.00183.x
  • Salazar, (2004), Chem. Senses, 29, pp. 3, 10.1093/chemse/bjh001
  • Park, (2012), Acta Histochem., 114, pp. 24, 10.1016/j.acthis.2011.02.001
  • Parra, (2011), J. Anat., 218, pp. 558, 10.1111/j.1469-7580.2011.01357.x
  • Delgado, (2020), J. Anat., 236, pp. 612, 10.1111/joa.13126
  • Malz, (2002), Anat. Embryol., 205, pp. 83, 10.1007/s00429-002-0244-y
  • Brunjes, (1992), J. Comp. Neurol., 320, pp. 544, 10.1002/cne.903200411
  • Salazar, (2001), Chem. Senses, 26, pp. 645, 10.1093/chemse/26.6.645
  • (1964), Anat. Rec., 150, pp. 11, 10.1002/ar.1091500103
  • Pastor, (1992), Histochem. J., 24, pp. 727, 10.1007/BF01460825
  • Roslinski, (2000), Anat. Rec., 260, pp. 92, 10.1002/1097-0185(20000901)260:1<92::AID-AR100>3.0.CO;2-#
  • Pfaff, (1989), Nature, 338, pp. 161, 10.1038/338161a0
  • Pfaff, (1990), Experientia, 46, pp. 956, 10.1007/BF01939389
  • Pfaff, (1991), J. Steroid Biochem. Mol. Biol., 39, pp. 565, 10.1016/0960-0760(91)90254-3
  • Pfaff, (1994), Ann. Endocrinol., 55, pp. 235
  • Skeen, (1977), J. Comp. Neurol., 172, pp. 1, 10.1002/cne.901720102
  • Stephan, (1965), Cells Tissues Organs, 62, pp. 215, 10.1159/000142750
  • Schneider, (2009), Reproduction, 138, pp. 849, 10.1530/REP-09-0145
  • Wettschureck, (2005), Physiol. Rev., 85, pp. 1159, 10.1152/physrev.00003.2005
  • Kondoh, (2022), Tissue Cell, 77, pp. 101863, 10.1016/j.tice.2022.101863
  • Torres, (2022), Brain. Struct. Funct., 227, pp. 881, 10.1007/s00429-021-02425-2
  • Kondoh, (2017), Cells Tissues Organs, 203, pp. 20, 10.1159/000447009
  • Keller, (2022), Acta Histochem., 124, pp. 151877, 10.1016/j.acthis.2022.151877
  • Salazar, (2000), J. Anat., 196, pp. 15, 10.1046/j.1469-7580.2000.19610015.x
  • Mogi, (2007), Anat. Rec., 290, pp. 301, 10.1002/ar.20505
  • Sweet, (1906), J. Cell Sci., 2, pp. 547, 10.1242/jcs.s2-50.200.547
  • Broom, (1926), Proc. Zool. Soc. Lond., 96, pp. 419, 10.1111/j.1469-7998.1926.tb08104.x
  • Bock, (2009), J. Anat., 215, pp. 522, 10.1111/j.1469-7580.2009.01147.x
  • Salazar, (1994), Anat. Rec., 240, pp. 277, 10.1002/ar.1092400216
  • Torres, M.V., Ortiz-Leal, I., Ferreiro, A., Rois, J.L., and Sanchez-Quinteiro, P. (2021). Neuroanatomical and Immunohistological Study of the Main and Accessory Olfactory Bulbs of the Meerkat (Suricata suricatta). Animals, 12.
  • Bennett, (2000), Behav. Ecol. Sociobiol., 48, pp. 471, 10.1007/s002650000249
  • Leclaire, S., Nielsen, J.F., Thavarajah, N.K., Manser, M., and Clutton-Brock, T.H. (2013). Odour-Based Kin Discrimination in the Cooperatively Breeding Meerkat. Biol. Lett., 9.
  • Leclaire, (2017), Sci. Rep., 7, pp. 3240, 10.1038/s41598-017-03356-x
  • Grus, (2004), Gene, 340, pp. 303, 10.1016/j.gene.2004.07.037
  • Salazar, (2009), Front. Neuroanat., 3, pp. 22, 10.3389/neuro.05.022.2009
  • Nakajima, (1998), Anat. Rec., 252, pp. 393, 10.1002/(SICI)1097-0185(199811)252:3<393::AID-AR7>3.0.CO;2-T
  • Hughes, L. (2023, October 13). Meerkats: Essential Wildlife; Character-19: 2020. Available online: https://www.amazon.com/Meerkats-Essential-Wildlife-Lisa-Hughes-ebook/dp/B08GY42Z76.
  • Broom, (1898), J. Anat. Physiol., 32, pp. 709
  • Yohe, (2023), Anat. Rec., 306, pp. 2765, 10.1002/ar.25290
  • (1991), Zool. Jb. Anat., 121, pp. 71
  • Shnayder, (1993), NeuroReport, 5, pp. 193, 10.1097/00001756-199312000-00001
  • Kondoh, (2018), Cell Tissue Res., 373, pp. 361, 10.1007/s00441-018-2819-9
  • Tiwari, (2014), J. Vet. Sci. Tech., 3, pp. 15
  • Rekwot, (2001), Anim. Reprod. Sci., 65, pp. 157, 10.1016/S0378-4320(00)00223-2
  • Ungerfeld, (2023), Anim. Reprod. Sci., 248, pp. 107154, 10.1016/j.anireprosci.2022.107154
  • Torres, (2023), Microsc. Res. Tech., 86, pp. 1206, 10.1002/jemt.24392
  • Hart, (1988), Physiol. Behav., 42, pp. 155, 10.1016/0031-9384(88)90291-0
  • Meredith, (1980), Science, 207, pp. 1224, 10.1126/science.7355286
  • Krishna, (1995), J. Neurosci. Res., 40, pp. 54, 10.1002/jnr.490400107
  • Takigami, (2000), Chem. Senses, 25, pp. 387, 10.1093/chemse/25.4.387
  • Matsubara, (2019), Jpn. J. Zoo Wildl. Med., 24, pp. 115, 10.5686/jjzwm.24.115