Convergence of olfactory and vomeronasal projections in the rat basal telencephalon

Pro-Sistiaga, Palma; Mohedano-Moriano, Alicia; Úbeda-Bañón, Isabel; Arroyo-Jiménez, M.M.; Marcos, Pilar; Artacho‐Pérula, Emilio; Crespo, Carlos; Insausti, Ricardo; Martı́nez-Marcos, Alino

doi:10.1002/cne.21455

Cited by 151 publications

(144 citation statements)

References 62 publications

(135 reference statements)

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“…In contrast, in the posteromedial nuclei (PMCo), c-fos was reduced in VNEx mice, but not in ΔD(dta) mice (Fig. 8C), consistent with findings from anatomical studies showing that the PLCo and PMCo receive direct inputs from the MOB and AOB, respectively (51).…”

Section: Altered Aversive Behaviors Induced By An Alarm Pheromone In δDsupporting

confidence: 88%

Genetic dissection of pheromone processing reveals main olfactory system-mediated social behaviors in mice

Matsuo¹,

Hattori

Asaba

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Most mammals have two major olfactory subsystems: the main olfactory system (MOS) and vomeronasal system (VNS). It is now widely accepted that the range of pheromones that control social behaviors are processed by both the VNS and the MOS. However, the functional contributions of each subsystem in social behavior remain unclear. To genetically dissociate the MOS and VNS functions, we established two conditional knockout mouse lines that led to either loss-of-function in the entire MOS or in the dorsal MOS. Mice with whole-MOS loss-of-function displayed severe defects in active sniffing and poor survival through the neonatal period. In contrast, when loss-of-function was confined to the dorsal MOB, sniffing behavior, pheromone recognition, and VNS activity were maintained. However, defects in a wide spectrum of social behaviors were observed: attraction to female urine and the accompanying ultrasonic vocalizations, chemoinvestigatory preference, aggression, maternal behaviors, and risk-assessment behaviors in response to an alarm pheromone. Functional dissociation of pheromone detection and pheromonal induction of behaviors showed the anterior olfactory nucleus (AON)-regulated social behaviors downstream from the MOS. Lesion analysis and neural activation mapping showed pheromonal activation in multiple amygdaloid and hypothalamic nuclei, important regions for the expression of social behavior, was dependent on MOS and AON functions. Identification of the MOS-AON-mediated pheromone pathway may provide insights into pheromone signaling in animals that do not possess a functional VNS, including humans.social behavior | pheromone processing | main olfactory system | vomeronasal system M ost mammals have two major olfactory subsystems-the main olfactory system (MOS) and vomeronasal system (VNS). The MOS comprises the main olfactory epithelium (MOE), in which olfactory sensory neurons detect odorants, and their projection target, the main olfactory bulb (MOB) (Fig. S1A). Although the MOS is thought to detect volatile odorants and the VNS is thought to be important for the detection of nonvolatile pheromones, evidence shows that the MOS is also involved in pheromone detection (1-8). Surgical blocking of odorant access to the MOE, but not surgical ablation of the vomeronasal epithelium (VNE), eliminates preference to odors from the opposite sex in ferrets (9, 10). In mice, chemical ablation of the MOE impairs male and female sexual behaviors (11,12). In these experiments in which the MOE was ablated, the function of the VNS is not directly disrupted, because the VNS is activated by direct application of urine to the nostril. Thus, these results indicate that the MOS also contributes to pheromone processing and related behaviors.Nonconditional disruption of genes encoding signal transduction proteins that are required for activation of olfactory neurons, such as cyclic nucleotide-gated channel (Cnga2) or adenylyl cyclase 3, impairs several social behaviors (11,(13)(14)(15). However, complete loss of MOS function causes a...

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Section: Altered Aversive Behaviors Induced By An Alarm Pheromone In δDsupporting

confidence: 88%

Genetic dissection of pheromone processing reveals main olfactory system-mediated social behaviors in mice

Matsuo¹,

Hattori

Asaba

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…More recently a small subset of MOB mitral cells was identified that extend axons directly to the medial amygdala (both the anterior and posteriordorsal subdivisions) (Kang et al, 2009). Similar results have been obtained in the rat in which MOB mitral cells targeting both the medial amygdala (Pro-Sistiaga et al, 2007) and the AOB itself (Larriva-Sahd, 2008) have been identified. In mice the MeA projecting MOB mitral cells also extend axon collaterals to a wide expanse of targets in piriform cortex (Kang et al, 2011a;Sosulski et al, 2011).…”

Section: Sex Differences In Vno-aob Responses To Pheromonessupporting

confidence: 82%

“…An early study (Kevetter and Winans, 1981b) demonstrated that a subset of MOB mitral cells also project to cortical amygdaloid nuclei ('olfactory amygdala'). However, more recent studies (Kang et al, 2009;Pro-Sistiaga et al, 2007;Thompson et al, 2012) showed that there is a subpopulation of MOB mitral cells that also project directly to the MeA ('vomeronasal amygdala'). There is considerable evidence from numerous studies conducted over the past 20 years that several volatile chemicals (including the androgenic steroid, androstenone) function as pheromones that influence aspects of behavior and neuroendocrine function after their detection by a specialized population of receptor neurons in the MOE.…”

Section: Introductionmentioning

confidence: 99%

Roles of sex and gonadal steroids in mammalian pheromonal communication

Baum

Bakker

2013

Frontiers in Neuroendocrinology

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a b s t r a c t A brain circuit (the accessory olfactory system) that originates in the vomeronasal organ (VNO) and includes the accessory olfactory bulb (AOB) plus additional forebrain regions mediates many of the effects of pheromones, typically comprised of a variety of non-volatile and volatile compounds, on aspects of social behavior. A second, parallel circuit (the main olfactory system) that originates in the main olfactory epithelium (MOE) and includes the main olfactory bulb (MOB) has also been shown to detect volatile pheromones from conspecifics. Studies are reviewed that point to specific roles of several different steroids and their water-soluble metabolites as putative pheromones. Other studies are reviewed that establish an adult, 'activational' role of circulating sex hormones along with sex differences in the detection and/or processing of non-steroidal pheromones by these two olfactory circuits. Persisting questions about the role of sex steroids in pheromonal processing are posed for future investigation.

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“…These results suggest that information from the two olfactory systems converges at a particular site between the AOB and the BNST. Although recent studies have hypothesized, based on anatomical evidence, that the medial amygdala is the candidate site for the convergence of information (57,58), there are other sites that receive direct projections from both the main olfactory bulb and the AOB in a similar manner (59). In addition, the absence of a good experimental model has prevented further assessment of this hypothesis from a functional point of view.…”

Section: Discussionmentioning

confidence: 99%

Identification of a pheromone that increases anxiety in rats

Inagaki

Kiyokawa

Tamogami³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Chemical communication plays an important role in the social lives of various mammalian species. Some of these chemicals are called pheromones. Rats release a specific odor into the air when stressed. This stress-related odor increases the anxiety levels of other rats; therefore, it is possible that the anxiety-causing molecules are present in the stress-related odorants. Here, we have tried to identify the responsible molecules by using the acoustic startle reflex as a bioassay system to detect anxiogenic activity. After successive fractionation of the stress-related odor, we detected 4-methylpentanal and hexanal in the final fraction that still possessed anxiogenic properties. Using synthetic molecules, we found that minute amounts of the binary mixture, but not either molecule separately, increased anxiety in rats. Furthermore, we determined that the mixture increased a specific type of anxiety and evoked anxiety-related behavioral responses in an experimental model that was different from the acoustic startle reflex. Analyses of neural mechanisms proposed that the neural circuit related to anxiety was only activated when the two molecules were simultaneously perceived by two olfactory systems. We concluded that the mixture is a pheromone that increases anxiety in rats. To our knowledge, this is the first study identifying a rat pheromone. Our results could aid further research on rat pheromones, which would enhance our understanding of chemical communication in mammals.stress-related odor | alarm pheromone | acoustic startle reflex | anxiety | rat C hemical communication plays an important role in the social lives of various mammalian species. Some of these chemicals are called "pheromones." Because the term pheromone was coined and defined based on findings in insects (1), there is still a debate as to whether the original definition can be applied to mammals (2). Researchers have proposed revised definitions by modifying the original definition and/or specifying additional requirements (3-6). On the basis of the original and revised definitions, we set a working definition of pheromone within this study as (i) substances that are secreted to the outside by an individual and received by a second individual of the same species, in which they cause a specific reaction; (ii) substances that are effective in minute amounts; (iii) substances that are released from living individuals; and (iv) substances that mediate communication for an evolutionarily adaptive function.Rats release a specific odor into the air when stressed (7). This stress-related odor increases anxiety levels (8, 9) and induces a variety of anxiety-related responses depending on their situation with other rats (9-18). Rats respond to their own stressrelated odor in a similar manner to odor released from the other rats, suggesting that the odor has general effects (10,19). In addition, the stress-related odor appears to be effective in minute amounts (20,21). Therefore, the molecules responsible for increasing anxiety levels should exist in the...

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Convergence of olfactory and vomeronasal projections in the rat basal telencephalon

Cited by 151 publications

References 62 publications

Genetic dissection of pheromone processing reveals main olfactory system-mediated social behaviors in mice

Genetic dissection of pheromone processing reveals main olfactory system-mediated social behaviors in mice

Roles of sex and gonadal steroids in mammalian pheromonal communication

Identification of a pheromone that increases anxiety in rats

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