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The Case of the Mammalian Vomeronasal System†

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The Case of the Mammalian Vomeronasal System† REVIEW ARTICLE published: 30 October 2009 NEUROANATOMY doi: 10.3389/neuro.05.022.2009 The risk of extrapolation in neuroanatomy: the case of the mammalian vomeronasal system† Ignacio Salazar* and Pablo Sánchez Quinteiro Unit of Anatomy and Embryology, Department of Anatomy and Animal Production, Faculty of Veterinary, University of Santiago de Compostela, Lugo, Spain Edited by: The sense of smell plays a crucial role in mammalian social and sexual behaviour, identifi cation Agustín González, Universidad of food, and detection of predators. Nevertheless, mammals vary in their olfactory ability. One Complutense de Madrid, Spain reason for this concerns the degree of development of their pars basalis rhinencephali, an Reviewed by: Alino Martinez-Marcos, anatomical feature that has been considered in classifying this group of animals as macrosmatic, Universidad de Castilla, Spain microsmatic or anosmatic. In mammals, different structures are involved in detecting odours: Enrique Lanuza, the main olfactory system, the vomeronasal system (VNS), and two subsystems, namely the Universidad de Valencia, Spain ganglion of Grüneberg and the septal organ. Here, we review and summarise some aspects of *Correspondence: the comparative anatomy of the VNS and its putative relationship to other olfactory structures. Ignacio Salazar, Department of Anatomy and Animal Production, Unit Even in the macrosmatic group, morphological diversity is an important characteristic of the of Anatomy and Embryology, Faculty of VNS, specifi cally of the vomeronasal organ and the accessory olfactory bulb. We conclude that Veterinary, University of Santiago de it is a big mistake to extrapolate anatomical data of the VNS from species to species, even in Compostela, Av Carballo Calero s/n, the case of relatively close evolutionary proximity between them. We propose to study other 27002 Lugo, Spain. e-mail: [email protected] mammalian VNS than those of rodents in depth as a way to clarify its exact role in olfaction. †In memoriam to Joaquin Camón, Our experience in this fi eld leads us to hypothesise that the VNS, considered for all mammalian Professor of Anatomy and Embryology, species, could be a system undergoing involution or regression, and could serve as one more Faculty of Veterinary, Universidad integrated olfactory subsystem. Complutense de Madrid. Keywords: morphology, olfaction, vomeronasal system, mammals, diversity INTRODUCTION In order to avoid any misinterpretation, this review will refer Most mammals have two mechanisms to detect odour. One is to the VNS consistent with the previous description. This means by means of the main olfactory system (MOS), with the main that a true VNS must have three structures with its corresponding olfactory receptors (MOrs) located in the posterior part of the nerves and connections. This anatomical defi nition is important mucosa of the nasal cavity. The olfactory nerves project to the because a critical point in the study of the VNS concerns its func- main olfactory bulb (MOB), from where the olfactory tracts tion (described furthering in subsequent sections), which histori- transmit their inputs to specifi c areas of the brain: the anterior cally takes into account the results and conclusions from studies olfactory nucleus, piriform cortex, olfactory tubercle, anterior conducted principally with mice, a species that possesses a very cortical amygdaloid nucleus, the lateral entorhinal cortex and well defi ned VNS. Many authors, ourselves included, consider the the periamygdaloid cortex. mouse VNS as the model of reference among mammals. The other option is through the accessory olfactory system As mentioned previously, the VNAg is an important VNS com- (AOS), commonly named the vomeronasal system (VNS). The ponent, but it will not be discussed in the present manuscript. The accessory olfactory bulb (AOB) is the fi rst relay station of the amygdala is a very complex area (Swanson and Petrovich, 1998) subsidiary system which is integrated by three different struc- that has led to confusion and controversy in the study of the VNS tures: the vomeronasal organ (VNO), the aforementioned AOB, (Meredith and Westberry, 2004), although contemporary models and the vomeronasal amygdala (VNAg). Inside the VNO are the have brought new clarity to this issue (Pro-Sistiaga et al., 2007; Fan vomeronasal receptors (VNrs), which project through the vome- and Luo, 2009; Kang et al., 2009; Martinez-Marcos, 2009). ronasal nerves to the AOB. From here, the accessory olfactory tract conveys the corresponding information to the VNAg, in this case ANTECEDENTS to the bed nucleus of the stria terminalis, the bed nucleus of the VOMERONASAL ORGAN accessory olfactory tract, and the medial and postero-medial cor- At the beginning of the nineteenth century the fi rst detailed infor- tical amygdaloid nucleus (Halpern, 1987; Halpern and Martinez- mation was published about the VNO in mammals (Jacobson, Marcos, 2003). 1813), but the existence of the AOB – also in mammals – was not confi rmed until several years later (Gudden, 1870). The American Abbreviations: AOB, accessory olfactory bulb; AOS, accessory olfactory system; anatomist Rollo McCotter (1912) demonstrated by micro- dissection DMs, domesticated mammals; GgG, ganglion of Grüneberg; LEA, Lycopersicum that both structures are directly connected, and this was the fi rst esculentum agglutinin; MOB, main olfactory bulb; MOrs, main olfactory receptors; step in identifying the VNS. However, the modern description of MOS, main olfactory system; SO, septal organ; UEA-I, Ulex europaeus agglutinin I; VNAg, vomeronasal amygdala; VNd, vomeronasal duct; VNO, vomeronasal organ; the VNS was developed several decades later when the presump- VNrs, vomeronasal receptors; VNS, vomeronasal system. tive and defi nitive projection from the AOB to a particular area of Frontiers in Neuroanatomy www.frontiersin.org October 2009 | Volume 3 | Article 22 | 1 Salazar and Sánchez Quinteiro Vomeronasal system in mammals the amygdala was identifi ed (Winans and Scalia, 1970; Scalia and posterior part is blind while its anterior part ends in the nasal Winans, 1975). Subsequently, it was assumed that the majority of cavity. The duct is surrounded by soft tissue containing a consid- mammals have two different systems to identify chemical signals erable amount of glands, vessels and nerves, as well as connective related to olfaction. tissue. Finally, a bone lamina encloses all of the elements (Figure 1). The existence of such an amazing accessory system attracted the Functionally, the VNO is closely related to the sexual behaviour of attention of the scientifi c community, which sought to identify a mammals (rodents). physiological role for the VNS. Several pieces of information con- tributed to some early insights. ACCESSORY OLFACTORY BULB The fi rst effort tried to determine whether the VNO was present At the beginning of the twentieth century, Santiago Ramón y Cajal in amphibians, reptiles and mammals, and to investigate whether it (1902) defi nitively clarifi ed the structural characteristics of the AOB was absent in fi sh and birds. These studies resulted in an exhaustive in mammals, and partially corroborated previous descriptions asso- revision of the defi nition of the VNO (Pearlman, 1934), including ciated with different animals (Gudden, 1870; Kölliker, 1877; Ganser, theories related to its function. However, more relevant data as to 1882; Gehuchten and Martin, 1891; Herrick, 1892). Once the fi rst VNS function came from experiments that dealt with the “physi- and most detailed description of the connection between the VNO ological effects on reproduction”. It became clear that substances and AOB (McCotter, 1912) was broadly accepted, the AOB was present in the urine of mice could modify sexual behaviour. Some considered as the fi rst relay station mediating olfactory cues dif- substances present in female urine delayed the onset of puberty in ferent from the MOS. Subsequently, the AOB has been studied for prepuberal females and suppressed oestrous cyclicity in grouped different reasons (Halpern, 1987; Halpern and Martinez-Marcos, females (Lee and Boot, 1955), while substances present in the urine 2003), although this review focuses only on its morphology. The of males induced oestrous in anoestrous females (Whitten, 1956), most controversial issue regarding the morphology of the AOB is prevented pregnancy in recently mated females (Bruce, 1960), and whether it can recognise mitral cells on it, or distinguish them from accelerated the onset of puberty (Vandenbergh, 1969). Almost tufted cells. However, different studies have suggested that the AOB simultaneously, Karlson and Lüscher (1959) coined the term “phe- has a mixed population of neurones, namely the “mitral/tufted” romones” to defi ne a class of biologically active substances secreted cells (Mori, 1987). by insects. It is certainly controversial whether the term pherom- Recently, the characteristics of the different cells included on the ones applies to mammals, but the VNS has been seen as a special- AOB of the rat have been studied in depth (Larriva-Sahd, 2008). ised system for mediating pheromonal communication (Johnston, Essentially, the structure of the AOB is similar to the MOB: 1998). The controversial theme of the mammalian pheromones groups of cells organised into strata, albeit with some peculiari- has been discussed extensively in the literature (Beauchamp et al., ties. The nervous or vomeronasal, glomerular, and granular layers 1976; Luo and Katz, 2004; Rodriguez,
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