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Animal Research International (2009) 6(3): 1093 – 1101 1093

THE ROLE OF MAIN OLFACTORY AND VOMERONASAL SYSTEMS IN ANIMAL BEHAVIOUR AND REPRODUCTION

IGBOKWE, Casmir Onwuaso Department of Veterinary Anatomy, University of Nigeria, Nsukka, Nigeria. Email: [email protected] Phone: +234 8034930393

ABSTRACT

In many terrestrial tetrapod, olfactory sensory communication is mediated by two anatomically and functionally distinct sensory systems; the main and vomeronasal system (accessory olfactory system). Recent anatomical studies of the central pathways of the olfactory and vomeronasal systems showed that these two systems converge on in the telencephalon providing an evidence for functional interaction. The combined anatomical, molecular, physiological and behavioural studies have provided new insights into the involvement of these systems in pheromonal and their influence on the neuroendocrine pathways. The olfactory and vomeronasal systems have overlapping functions and both are involved in responses to both and chemical odorants. Several studies in insects, amphibians, and have established the importance of pheromones in the astonishing influence exerted by the male on the reproductive activity of the . The great diversity of signals used in chemical communication indicates that this communication is not mediated exclusively by pheromones. A number of pheromonal responses are not dependent on the vomeronasal system, but on the main olfactory system. The dual olfactory systems also have overlapping functions. The importance of this organ in reproductive and social behaviours was the aim of carrying out the review on its basic morphology and functional correlations in order to encourage more future studies of this important organ of our local species and breeds of .

Keywords: Main olfactory system, Vomeronasal system, Pheromones, Behaviour, Mammals

INTRODUCTION olfactory systems. The recent resurgence of interest in smells and scents has considerably expanded The ability of mammalian olfactory and vomeronasal information and full understanding of the multiple systems to detect an enormous array of structurally chemoreceptive systems in the of mammals. diverse volatile and non-volatile stimuli with New techniques and more systematic approaches extraordinary sensitivity and specifity has fascinated have been steadily applied to this area of the philosophers, writers and scientists since the previous chemical ; olfactory and vomeronasal century. chemoreception (Evans, 2003).The main olfactory The current knowledge of how organ and have some common information from environment is perceived has features, but also significant differences in greatly advanced since the discovery of about 1000 types, primary structures of receptor proteins and genes for odorant receptors in mammalian genome. signal transduction(Firenstein, 2001). From the combination of anatomic, molecular- Pheromones are defined as those natural genetic, electrophysiological and optical imaging compounds secreted by one member of a social studies, a better understanding of the of smell group that can influence the neuroendocrine is emerging. The olfactory and vomeronasal system mechanisms underlying behaviour, fertility or detects and discriminates among large number of development of another group member, in which structurally diverse odorant molecules that carry they release a specific reaction (Mclintock, 2002). information about the environment and from amongst modifies various physiological functions con-specific species. A pivotal event in understanding including the reproductive activity, after being the mechanisms of olfaction came with identification processed by the vomeronasal system. Application of of genes encoding odorant receptors (Buck and Axel, such actions of pheromones to the control of 1991). In the past dozen years, these receptors have reproduction in domestic animals has long been created a new framework for anatomical and desired. Pheromone research in rodents has made electrophysiological studies that have challenged substantial advance, but is not the case for higher long-held views and presented new puzzles on both

ISSN: 159 – 3115 ARI 2009 6(3): 1093 – 1101 www.zoo-unn.org Igbokwe 1094 mammals, especially domestic food animal (Okamura concentration. Each of the olfactory sensory et al., 2004). neurons, which project to the main , Pheromones modify physiological functions expresses a single receptor type from a large family including the reproductive activity after being of olfactory receptors Also a second family of G- processed through the vomeronasal system. The protein-coupled receptors, the trace amine associated application of these effects of pheromone to the receptors (TAARS), which recognize volatile amines control of reproductive processes in domestic animals present in , has also been shown to be is quite important and is applied in biostimulation in expressed in olfactory sensory neurones (Liberies and several domestic food animals (Rekwot et al., 2001). Buck, 2006).The neurons in the main olfactory Chemosensory system and pheromonal research has system use distinct signaling components unlike that not made a great advance in our domestic animals. of vomeronasal system. In the main olfactory, the The aim of this article is to examine the role binding of the odorant to one of as many 1000 played by the two different but related olfactory different types of odorant receptors leads to systems in initiating several biological effects on activation of a second-messenger pathway involving mammals such as pheromonal effects, reproductive, olfactory-specific G-protein, which in turn activates parental, aggressive and marking behavoiur, adenyl cyclase to produce cyclic adenosine individual odor discrimination, prey trailing, flehmen monophosphate (cAMP). The cAMP opens a cyclic behaviour and other responses to chemosignals. It is nucleotide-gated cation channel in ciliary membrane believed that these biological reproductive behaviours allowing cations to flow into the cell, resulting in could help in the beneficial artificial management of gradual depolarization that travels down the dendrite reproductive processes. to the cell body of the neurones (Gold 1999; Lambrechts and Hossaert-Mckey, MATERIALS AND METHODS 2006).There is also evidence for another intracellular second messenger involving inositol 1,4,5- A comprehensive search was made from the Internet, triphosphate (IP3). It is thought to act separately or various journal articles and textbook reports on the with cAMP pathway. Current research supports a role role of the olfactory and vomeronasal systems in for cyclic guanosine monophosphate and carbon animal behaviour and reproduction. Such articles monoxide in olfactory signal transduction (Simpson were assembled and studied. and Sweazey, 2006). In addition to differences in

RESULTS AND DISCUSSION anatomical organization and transduction cascade, the molecular organization of the two chemosensory Functional Anatomy of the Olfactory System: systems differ; Mice possess around 1000 olfactory The olfactory organ is situated in the nose. In animals receptors and around 300 vomeronasal receptors, with a well-developed it consists of but these two sets of receptors share little relatively large area of covering the similarity(Zhang et al., 2006). lateral wall and ethmoidal concha (turbinates) in the In most , the olfactory sensory caudal part of the . The olfactory region is neurons in the periphery are the primary sensing said to be little more yellowish than the respiratory cells. They form a neuroepithelium that lines series of mucosa rostral to it. The olfactory region cannot be these conchas. The olfactory sensory neurones are certainly identified by gross inspection. The olfactory bipolar neurons with a single dendrite that reaches up neuroepithelium is a pseudostratified columnar to the surface of the tissue and ends in a knob-like . The specialized olfactory epithelial cells swelling from which project some 20 – 30 very fine are the only group of neurons capable of non motile cilia. These cilia, which actually lie in the regeneration. There six distinct cell types in the thin layer of mucous covering the tissue, are the site : bipolar sensory receptor of sensory transduction apparatus. A thin from neurons, microvillar cells, supporting cells, globose the proximal pole of the cell projects directly to the basal cells, horizontal basal cells, and cells lining the olfactory bulbs and to higher regions like the Bowman’s glands (Jing and Ryan, 2003).The and . Other signals from the neuroepithelial cells are characterized by ciliated olfactory bulbs are passed via the to dendrites which protrude from the surface of the the , which is associated with epithelium. The cilia are the site where interaction and (Deidre, 2001). The mucous layer of the with odorant occurs. The sense of smell is much olfactory epithelium is about 60 µm thick and is a better developed in domestic animals than in lipid- rich secretion containing mucopolysacharides, , this is particularly true of dog, which can immunoglobins, proteins, that bathes the surface of detect airborne substances in incredibly low the receptors at the epithelium surface. The mucous

Animal Research International (2009) 6(3): 1093 – 1101 The role of main olfactory and vomeronasal systems in animal behaviour and reproduction 1095

layer is produced by the Bowman’s glands which recognition could not come from normal reside in the olfactory epithelium. The mucous layer memorization of visual and or auditory cues(the assist in transporting the odorant molecule as only paper). Also female required only 5 minutes of volatile materials that are soluble in the mucous can initial contact immediately after birth to discriminate interact with the olfactory receptors and produce the their own kids from aliens after several hours of signals that the brain interprets as odor. separation. Offspring recognition through olfaction in most female animals is believed to emanate from its Importance of Olfaction in Animal Production body coat (Price et al., 1984).The olfactory system and Behaviour: Experimental removal of olfactory also mediates responses to pheromones. Blockage of structures have widely assigned the role of olfactory the vomeronasal duct has no effect on the system to the sense of smell, resulting in the behavioural detection of androstenone or elicitation detection of a large variety of volatile odorants, while of pheromone-induced mating postures (Dorries et the vomeronasal system is believed to mediate the al., 1995) indicating that this well-characterized detection of most gender and species-specific cues mammalian pheromonal effect is detected by the involved in the control of mating and aggressive olfactory system. behaviour (Dulac and Torello, 2003). Olfaction is Odours clearly play a role in food selection in defined as the capacity to detect airborne chemical several species of birds, such as kiwis, vultures, and compounds at a distance from their source shearwaters, and there are indications that some (Lambrechts and Hossaert-Mckey, 2006). In social behaviours of ducks may be influenced by mammals, olfactory cues play a preponderant role . Olfaction is also used in birds to find food. For since they can mimic most of the behavioural and instance procellariiform seabirds (e.g. great physiological changes provoked by social interaction. shearwaters) have well developed olfactory apparatus It has been reported in many species that chemical used for detecting food on the sea in the absence of signals serve as sexual attractants, as well as visual food cues (Verheyden and Jouventin, 1994). inducing sexual arousal, appetitive and precopulatory Olfaction in birds is also involved in courtship and postures, and mating behaviour in rat, mouse and mate recognition (Jacob et al., 1979), nest building (Brown ,1977; Johnston and Bronson, 1982; (Clark and Smeraski, 1990), nest relocation and Rasmussen et al., 1996).These chemosignals can also discrimination (Walraff, 2001). That olfaction is modify the and neuroendocrine state. involved in the control of reproduction is a long However it is unclear whether the olfactory cues recognized fact with respect to sexual behaviour. induce also behavioural changes (Gelez and Fabre- This is well established in both invertebrates (e.g. Nys, 2004). with discovery of sexual pheromones such as Olfactory cues are used extensively in many bombycol and in vertebrates, there is an intimate aspects of maternal care to ensure the coordination embryological relationship between the olfactory and of mother-infant interactions and consequently the the GnRH systems (Schanzel-Fukuda and Pfaff, normal development of the offspring. Outside the 1991), and the numerous modulations of sexual period of parturition and lactation, when the young behaviours or sexual hormone responses mediated by are not a behavioural priority, olfactory cues play an olfaction. inhibitory role on maternal responsiveness since in most mammalian species studied so far, non- Functional Morphology of the Vomeronasal pregnant find the odor of young aversive. It Organ: The presence of vomeronasal organ (VNO) is generally believed that recognition of opposite sex has been confirmed in most mammals (Figures 1 and involves the main olfactory pathway, and this has 2). It is also present in marsupials (It is well been demonstrated to be the case in pigs, monkeys, developed in some primates. The opinions concerning ferrets and rodents (Kervene, 2004). the presence and functioning of the organ in humans Apart from visual and auditory cues, the are controversial. The VNO is absent in fishes, birds, olfactory sense is the primary cue used by female chameleons and crocodiles and most marine animals to recognize their offspring during nursing mammals. The receptors for the accessory olfactory (Horrel and Hodgson, 1985; Dunn et al., 1987). system (vomeronasal system) are located within the Goats that are anosmic were unable to distinguish vomeronasal organ (VNO). This organ consists of their own kids from alien kids even though great paired cigar-shaped structures that are located variations in coat colour were apparent (Romeyer et medially, usually along the anterior (rostral) portion al., 1994). Blindfolded goats were unable to of the (Doving and Trotier, 1998). The distinguish their own offspring in a group of VNO sensory epithelium consists primarily of three nonbleating kids (Klopfer et al., 1964). These cell types; elongated cilia-like supporting cells, bipolar

Animal Research International (2009) 6(3): 1093 – 1101 Igbokwe 1096 sensory cells, called vomeronasal neurons, and basal hippocampus (Jansen et al., 1998). The organization stem cells. The vomeronasal neurons make up the of the vomeronasal system (VNS) is somewhat majority of the cells in the sensory epithelium and are different from the main olfactory epithelium, as at responsible for detection of chemostimuli. The VNO least some vomeronasal sensory neurons express opens at one end and forms a blind sac at the other. more than one receptor. Vomeronasal system The opening is variable. In rodents the opening is projects their to a caudal region of the into the nasal cavity (Figure 1); in it is into the olfactory bulb known as the accessory olfactory bulb. nasopalatine canal which connects with oral and VNS do not converge onto single glomeruli as the nasal cavities: in cows it opens directly into oral main bulb (Rodriguez et al., 1999; Leiders-Zuffal et cavity. al., 2000). In mammals, the neurons express genes encoding seven- transmembrane-domain receptors of either the V1R or the V2R family, which is coupled to different G N proteins (Halpern and Martinez-Marcos, 2003). A low degree of sequence similarity suggests that genes S encoding the olfactory, V1R and V2R receptors arose independently from within the larger family of G- protein coupled receptors evolved to detect different odorants from those detected by main olfactory Figure 1: Histological section system. Vomeronasal sensory neurons also have a of VNO in African giant rat: N- different transduction mechanism from olfactory nonsensory epithelium; S- sensory neurons; this involves a diacylglycerol- sensory epithelium (Igbokwe, 2009) activated cation channel, which depends in part on the transient-receptor potential channel 2 (Trpc2) genes (Lucas et al., 2003). The Trp2 channel is localized to the microvilli, the proposed site of pheromone transduction, suggesting the direct role in the VNO transduction cascade (Liman et al., 1999). The vomeronasal system mediates responses to N molecules of low volatility whereas the olfactory system mediates responses to more volatile S molecules (Wysocki and Meredith, 1987). Vaginal discharge of estrous female hamsters contains both volatile compounds that signal the presence of female Figure 2: Histological section of and nonvolatile compounds that elicit mating VNO of the Red Sokoto goats N- behaviours in males. In male hamsters lesions of the nonsensory epithelium; S-sensory olfactory reduce investigation of both females epithelium (Igbokwe, 2006) and vaginal discharge, suggesting that the olfactory The axons of the neuroreceptors of the VNO projects system detects the volatile components; lesions of to accessory olfactory bulb (AOB), which in turn the vomeronasal nerve impair initiation of mating projects to the media amygdala that has direct behaviour, suggesting that the vomeronasal system connections to the ventromedial hypothalamus and detects the components of lower volatility (O’connel the preoptic area. The VNO neurons covey the and Meredith, 1984). pheromone signal directly to parts of the brain’s -amygdala and several hypothalamic Functions of the Vomeronasal Organ: The VNO regions involved in primary motivated behaviour and plays a role in reproduction by detecting pheromones neuroendocrinology (Von Campenhausen and Mori, (Winnans and Powers, 1977).The VNO is widely 2000; Halpern and Martinez-Marcos, 2003). referred to as being the primary system for sensory Contrary to the accessory system, the main coding of pheromones. These chemical stimuli can olfactory system is linked to several cortical areas: induce hormonal changes, affect the success of The main olfactory projects to the cortical amygdala, , alter the timing of puberty and female to the which is connected via the ovulation, elicit courtship and attraction, and to the orbitofrontal and insular cortices, and modulate reproductive behaviour and aggression to the entorhinal cortex which is connected to the (Zuffal et al., 2002). The central feature of

Animal Research International (2009) 6(3): 1093 – 1101 The role of main olfactory and vomeronasal systems in animal behaviour and reproduction 1097

vomeronasal function is its ability to regulate the mammals were performed by Planel (Planel, 1953). activity of the gonads; this it does through the neural He showed that when this organ in guinea pigs was pathway influencing hypothalamic control over impaired the males failed to mount. Females with gonadotrophin secretion (Hypothalamic-Pituitary- impaired organs did not show lordosis, lost interest in Gonadal axis) (Martinez-Marcos and Halpern, 1999). their partner and seldom became pregnant. Mammalian pheromones have been shown to elicit Peripheral differentiation of the vomeronasal system both long-lasting effects that alter the endocrine state produces several sexual behaviour deficits in both of recipient animal, and short-term effects on its male and female hamsters (Powers and Winnans, behaviour--.For example, detection of male 1975). These authors found that the effects of pheromones by female mice results in an advance in removal or prevention of normal function of the the onset of puberty, induction of oestrus and vomeronasal organ were acute when the animal was termination of pregnancy, whereas detection of sexually naïve, but if the animal had experienced a female pheromones causes a delay in the onset of partner in sexual interplay, the effect of the removal puberty and suppression of oestrus. Modification of of the vomeronasal organ was less dramatic. the hypothalamic-pituitary axis regulates the release However injection of LHRH (gonadotrophin-releasing of luteinizing hormone (LH) and (PRL), two hormone) into experimental animals lacking a hormones that are important for regulating these vomeronasal organ re-established sexual behaviour. effects (Halpern, 1987). Most physiological responses Most of the work on vomeronasal functions to male pheromones seem to be linked to an increase has been in rodents and snakes. Early experiments in LH and a reduction in PRL, whereas physiological involve lesions (damage or removal) of the responses to female pheromones are usually vomeronasal or olfactory systems in order to reveal associated with increase in PRL. Therefore the deficits in behaviour or physiological function vomeronasal system provides a neural pathway that (Meredith and Fernandez-Fewell, 1994). More links the periphery to the hypothalamus, and recently researchers have detected genes thought to modulation of LH and PR release through this be involved with vomeronasal function and looked for pathway seems to provide the endocrine basis for deficits (Dulac and Axel, 1995). In other experiments ‘primer effect’ of mammalian pheromones (Dulac and the activation of brain areas receiving central Torello, 2003). The VNO by detecting mammalian vomeronasal projections has been investigated with pheromones also elicit behavioural responses. These other techniques (Takigami et al., 2000). include the regulation of inter-male aggression, The vomeronasal system has been courtship behaviours, aggressive responses in implicated in many behavioural/physiological lactating females, initiation of male ultrasonic responses to chemical signals in several species and vocalizations and copulatory behaviour, reinstatement both sexes. These responses may be of the type of lordosis in females, territorial marking, parental attributed to priming pheromones, where there is behaviour, individual odor discrimination and prey- some delayed physiological effects usually mediated trailing in snakes(Fernandez-Fewell and Meredith, by hormonal change or they may be the type 1995). These immediate behavioural responses are attributed to signaling pheromones, where rapid also modulated by the endocrine status of the animal, changes can be seen (Wysocki and Lepri, 1991). which is also under pheromonal control (Witt and However not all putative pheromone communication Wozniak, 2006). is mediated by the vomeronasal system, nor is all The experimental involvements of the VNO vomeronasal chemosensory function necessarily are in Bruce effect, Whitten and Vanderbergh effects related to pheromone communication. (Aron, 1979). In Bruce effect, newly mated female Communication between mother and young appears mice return to estrus if exposed to strange males to be mediated by olfactory and not vomeronasal prior to implantation. The is signaling. Vomeronasal organ removal did not disrupt the induction of estrus in female mice made anestrus odor-dependent nipple finding in young rabbits by group housing. This induction is caused by stimuli (Hudson and Distel, 1986). Also in pig, vomeronasal from males or their urine and is known to be duct occlusion did not prevent female “standing” dependent on a functional VNS. In Vanderbergh responses to male pheromone (Dorries et al., 1995; effect, there is puberty acceleration caused by 1997). exposure to male chemosignals during female Priming-type responses that are dependent development and occurs in several mammalian on an intact vomeronasal system in females are well species. documented. These include modulation of estrus in The first experiments indicating that mice by urine signals from males and females, vomeronasal organ played a role in reproduction in modulation of estrus in rats, the acceleration of

Animal Research International (2009) 6(3): 1093 – 1101 Igbokwe 1098 puberty in mice and voles and the block to pregnancy particularly following olfactory investigation of the in mice produced by strange males (Bruce effect). All anogenital area or freshly voided urine of a female these effects are mediated by signals in male urine (Ladewig and Hart, 1980). The perceptive and all are prevented by lesions of the vomeronasal identification of flehmen as key element in oestrus system. A similar dependence on intact vomeronasal detection was made by Estes (Estes, 1972). Intake of organs is seen in the induction of estrus in prairie non-volatiles is considered to be function of flehmen. voles (but not in meadow voles), in monodelphic Flehmen is a vomeronasal-specific sampling opossums and in induction of ovulation in light mechanism for oral and/or nasal uptake into the induced or estrogenized, persistence-estrus rats opening of the vomeronasal organ. The use of urine (Clancy et al., 1994). as signal vehicle is prevalent in many mammals/skin A signaling function is seen in lactating gland secretions. Faecal products are also involved as female mice, whose aggression toward intruders is is typical of South American ungulates and hyenas reduced or eliminated by vomeronasal lesions, (Altman, 1969). During flehmen most mammals show regardless of experience. Among males, there are jaw opening (gape or yawn) plus an elevated head clear examples of signaling functions mediated by posture and temporary stillness, there may also be vomeronasal organ but also examples of hormonal specific respiratory and tongue movement plus a modulation by vomeronasal input. Golden hamsters, degree of closure. Flehmen is conspicuous in mice and prairie voles are particularly dependent on ungulates and carnivores. The contribution of chemosensory input for normal reproductive flehmen to fertility is bound up with the role of the behaviour. vomeronasal system in reproductive patterns.

Chemosignals and Flehmen Behaviour: Conclusion: The advent of molecular studies has Chemosignals are usually volatile chemical revealed enormous information about the structure compounds (odorants) that elicit signals finally and function of the main olfactory and vomeronasal transmitted to higher brain centres and they generate systems particularly in small mammals. Vomeronasal various congnitive and emotional responses, (accessory) olfactory and main olfactory systems are measured thoughts and behaviours. In contrast, related structurally and both play significant roles in pheromones lead to innate and stereotyped detecting signals that have profound influence in behaviours that may result from a non-conscious behavioural and reproductive activities in mammals. perception of this class of odours. Chemosignals It seems that the VNO plays a pivotal role in which may be pheromones are obtained by touching, mediating pheromonal communication in mammals. licking and or close-range and sometimes The stimulation of this organ has profound influence flehmen response. Chemosensory responses initiate on the endocrine system which in turn influences sensory activity by sampling an odour source. Volatile reproductive functions and behaviour. When the VNO chemosignals taken in with respiratory airstream will fails to function in naïve mammals, mating behaviour arrive at the main olfactory mucosa. Chemosignals is affected, indicating the important role of this organ are rarely advantageous to the sender, although in some stages of reproduction. The main olfactory predator urine odours can repel prey species, while system is responsible for some pheromonal-triggered prey scent-trails can betray them to a predator unless behaviour. The olfactory and vomeronasal systems they too emit noxious odours (Cooper, 1997; Chizar have overlapping functions and these overlapping et al., 1999).The majority of the vomeronasal system functions which are well studied in rodents may be usage is carried out in conjunction with the main applicable to several other mammals. There are olfactory system. Some pheromones operate via the limited molecular-genetic studies of the vomeronasal system but some operate via the main chemosensory systems in our domesticated food olfactory system. Equally there also examples of VNO animals; perhaps vigorous attention on these species used for detecting nonpheromone chemicals in some particularly the ungulates may reveal the diverging species, particularly in snakes, which use the organ and complimentary roles of the dual olfactory for prey-trailing (Meredith, 2002). This combination of systems reproductive behaviour. information flow resulting from dual analysis of chemical input is bound to be advantageous in most REFERENCES circumstances. Flehmen which is the facial grin or grimace is a well known chemoreceptive investigative ALTMAN, J. (1969). Autoradiographic and histologic behaviour in terrestrial mammals. Flehmen is studies of the postnatal neurogenesis IV: displayed by most ungulates. The behaviour is seen Cell proliferation and migration in the much more frequently in males than females, anterior forebrain with special reference to

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