The human vomeronasal system

doi:10.1016/0306-4530(94)90049-3

Psychoneuroendocrinology

Volume 19, Issues 5–7, 1994, Pages 673-686

https://doi.org/10.1016/0306-4530(94)90049-3 Get rights and content

Abstract

We studied the functional characteristics of the vomeronasal system in clinically normal adult subjects of both sexes (ages 20–45). Chemosensory substances were administered in punctate pulses in a continuous air stream from the tip of a multifunctional miniprobe, which contained a nonpolarizable electrode. Negative potentials with the characteristics of receptor potentials were recorded from the surface of the vomeronasal organ (VNO) and olfactory epithelium (OE) in response to certain substances defined here as vomeropherins (see definition in the introduction of the main text) and to olfactants. Stimulation of the VNO with femtomole amounts of vomeropherins produced a local depolarization with the characteristics of a receptor potential. The same substances produced only a small response from the OE, and no response from the nasal respiratory mucosa. Three vomeropherins PH15, PH78, and PH84 were particularly well recognized by the VNO of most male subjects (p < .01; n = 30). Substances PH30, PH56, and PH94B, produced similar effects in the VNO of most female subjects (p < .01; n = 30). Responses to virtually all vomeropherins exhibited a sexual dimorphism. Stimulation of the OE with the same quantity of odorants 1,8-cineole and l-carvone produced depolarization of 6.8 ± 2.6 mV, but little or no response in the VNO. Therefore, the human VNO seems to have a unique specificity for certain chemosensory substances when compared to the OE. Administration of PH15 and PH78 to the VNO of male subjects (but not to female subjects) significantly increased electrodermal activity (p < .02) and skin temperature (p < .01). On the other hand, administration of PH84 to the VNO of male subjects decreased skin temperature but had little effect on electrodermal activity. Autonomic changes were accompanied by an increased percentage of α-cortical activity for all three vomeropherins. In female subjects (but not in male subjects) vomeropherins PH56 and PH94B significantly increased electrodermal activity (p < .01), skin temperature (p < .01), and α-cortical activity (p < .01). Local application of the olfactants 1,8-cineole and l-carvone to the VNO did not trigger autonomic responses or significant changes in the electroencephalographic pattern in male or in female subjects. Our studies indicate the adult human VNO is a functional chemosensory organ with a sexually dimorphic specificity and the ability to transduce signals which modulate certain autonomic parameters.

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In mammals, and even in some primates, the VNO is involved in the detection of social chemosignals. In contrast to some reports (Berliner et al., 1996; Monti-Bloch and Grosser, 1991; Monti-Bloch et al., 1994), the human VNO, if existing at all, is not a functional sensory organ. In humans, the adult vomeronasal duct does not comprise sensory cells (Boehm and Gasser, 1993; Boehm et al., 1994), and an accessory olfactory bulb, at which a vomeronasal nerve would terminate, does not exist (Meisami and Bhatnagar, 1998).
This article is part of a Special Issue “Chemosignals and Reproduction”
Across phyla, chemosensory communication is crucial for mediating a variety of social behaviors, which form the basis for ontogenetic and phylogenetic survival. In the present paper, evidence on chemosensory communication in humans, with special reference to reproduction and survival, will be presented. First, the impact of chemosignals on human reproduction will be reviewed. Work will be presented, showing how chemosensory signals are involved in mate choice and partnership formation by communicating attractiveness and facilitating a partner selection, which is of evolutionary advantage, and furthermore providing information about the level of sexual hormones. In addition to direct effects on phylogenetic survival, chemosignals indirectly aid reproductive success by fostering harm protection. Results will be presented, showing that chemosensory communication aids the emotional bond between mother and child, which in turn motivates parental caretaking and protection, leading to infant survival. Moreover, the likelihood of group survival can be increased through the use of stress-related chemosignals. Stress-related chemosignals induce a stress-related physiology in the perceiver, thereby priming a fight–flight-response, which is necessary for an optimum adaption to environmental harm. Finally, effects of sexual orientation on chemosensory communication will be discussed in terms of their putative role in stabilizing social groups, which might indirectly provide harm protection and foster survival. An integrative model of the presented data will be introduced. In conclusion, an outlook, focusing on the involvement of chemosensory communication in human social behavior and illustrating a novel approach to the significance of chemosensory signals in human survival, will be given.
D'scent of man: A comparative survey of primate chemosignaling in relation to sex
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Strepsirrhines or ‘wet-nosed’ primates, as their name implies, retain mammalian anatomical features associated with olfactory reliance, such as a well-developed rhinarium, numerous turbinates, and a functional vomeronasal organ (VNO) (Fleagle, 2013), as well as a large repertoire of functional olfactory receptor (OR) genes (Hohenbrink et al., 2013). By contrast, haplorhines or ‘dry-nosed’ primates are characterized by greater visual elaboration (e.g. enhanced binocular vision: Martin, 1990; routine trichromacy: Surridge et al., 2003), as well as by loss of a functional VNO (Liman and Innan, 2003; Zhang and Webb, 2003; but see: Monti-Bloch et al., 1994; T.D. Smith et al., 2001) and by greater OR pseudogenization (Gilad et al., 2003, 2004; Matsui et al., 2010). Based historically on the relative size of olfactory brain structures, the presence of an accessory olfactory system (AOS), and more recently on the representation of functional OR genes, strepsirrhine primates and certain New World (or platyrrhine) species have been widely considered to be ‘macrosmatic,’ whereas Old World primates (catarrhines), including humans, have been generally considered to be ‘microsmatic,’ having a poor sense of smell.
This article is part of a Special Issue (Chemosignals and Reproduction).
As highly visual animals, primates, in general, and Old World species (including humans), in particular, are not immediately recognized for reliance in their daily interactions on olfactory communication. Nevertheless, views on primate olfactory acuity and the pervasiveness of their scent signaling are changing, with increased appreciation for the important role of body odors in primate social and sexual behavior. All major taxonomic groups, from lemurs to humans, are endowed with scent-producing organs, and either deposit or exude a wealth of volatile compounds, many of which are known semiochemicals. This review takes a comparative perspective to illustrate the reproductive context of primate signaling, the relevant information content of their signals, the sexually differentiated investigative responses generated, and the behavioral or physiological consequences of message transmission to both signaler and receiver. Throughout, humans are placed alongside their relatives to illustrate the evolutionary continuum in the sexual selection of primate chemosignals. This ever-growing body of evidence points to a critical role of scent in guiding the social behavior and reproductive function throughout the primate order.
Pheromones in sex and reproduction: Do they have a role in humans?
2012, Journal of Advanced Research
Citation Excerpt :
In humans, the vomeronasal organ (VNO) was regarded as vestigial, but different researchers assumed its function to have a distinct sensory passage to detect pheromones. It is reported that nasal receptors near the entrance of the nose had the strongest reaction to air containing pheromones, transferring it to stimulate the hypothalamus with a signal of attraction, sexual desire, arousal etc. [15–18]. Jahnke and Merker [19] described the ultrastructure of the adult human VNO having a duct-like invagination of the epithelium surrounded by numerous exocrine glands with short ducts.
Pheromones are found throughout the living world and are a primal form of communication. These chemical messengers are transported outside the body and have a direct developmental effect on hormone levels and/or behaviour. This review article aims to highlight the role of human pheromones in sex and reproduction. A review of published articles was carried out, using PubMed, medical subject heading (MSH) databases and the Scopus engine. Key words used to assess exposure, outcome, and estimates for the concerned associations, were; olfaction; sex; pheromones; libido; behaviour; reproduction; humans; and smell. Although there are studies to support this phenomenon, they are weak because they were not controlled; others have proposed that human olfactory communication is able to perceive certain pheromones that may play a role in behavioural as well as reproductive biology. Unfolding the mysteries of smells and the way they are perceived requires more time and effort as humans are not systems that instinctively fall into a behaviour in response to an odour, they are thinking individuals that exercise judgment and subjected to different motivations.
Electrical responses to chemosensory stimulation recorded from the vomeronasal duct and the respiratory epithelium in humans
2011, International Journal of Psychophysiology
Citation Excerpt :
Total flow rate was 8 L/min. Based on studies published by Monti-Bloch et al. (1994) estra-1,3,5(10),16-tetraen-3ol (“estra” (Monti-Bloch et al., 1998)) and androsta-4,16-dien-3-on (“andro”) were used for stimulation (10 μM solutions in mineral oil) (odorants supplied by Firmenich, Basel, Switzerland). In addition, gaseous CO2 was used as a non-odorous, specific stimulant of the trigeminal nerve (50% v/v) (Fröhlich, 1851; Thürauf et al., 1991).
The physiological significance of the human vomeronasal duct (VND) is still unclear. The aim of the present study was to investigate the question whether mucosal responses obtained from the VND are different from those obtained from the respiratory epithelium. There were 15 healthy subjects (8 male, 7 female; age range 19–45 years; 14 normosmic subjects, 1 anosmic subject). All subjects participated in two sessions whereby the first session was used to acquaint them with the experimental conditions. For chemical stimulation, an olfactometer was used which delivered chemical stimulants without altering mechanical or thermal conditions at the stimulated nasal mucosa. For stimulation we used substances previously reported to produce vomeronasal activation (“estra” = estra-1,3,5(10),16-tetraen-3ol and “andro” = androsta-4,16-dien-3-on); in addition, gaseous CO₂ was used as a non-odorous, relatively specific stimulant of the trigeminal nerve. Placement of electrodes either in the VND or on the respiratory epithelium was performed under endoscopical guidance. Subjects rated the overall intensity of the stimuli, the strength of trigeminally mediated sensations, and the hedonic tone of the stimulants. Responses could not be recorded from all subjects. For the remaining 7 subjects, intensity was strongest for CO₂ stimuli (p < 0.001), whereas no significant difference was observed between “andro” and “estra” (p = 0.33). All three stimulants produced responses at the respiratory epithelium with largest responses obtained after stimulation with CO₂. Similar findings were made for recordings inside the VND. Due to the small sample size sexual dimorphisms could not be addressed. In summary, these results seem to indicate that the presently used stimulants produce similar responses at the respiratory epithelium and in the VND which argues against a specific responsiveness of the VND epithelium to chemosensory stimuli although it has to be kept in mind that the effective sample size was small.
Roles of insect and mammal pheromones: Vomeronasal receptors
2008, Studies in Natural Products Chemistry
Hypothesis: do homeopathic medicines exert their action in humans and animals via the vomeronasal system?
2007, Homeopathy
There is significant debate on the nature of the active therapeutic ingredient in homeopathic medicines and whether the effect of homeopathic medicines is exerted locally. This paper accepts that there is an active therapeutic ingredient in homeopathic medicines that acts pharmacologically in the body and proposes a possible receptor site.
The vomeronasal organ (Jacobson's organ) is the receptor site for the detection of non-odorant molecules, eg pheromones, in reptiles, amphibians and mammals. The organ forms the main part of a chemoreceptor system known as the vomeronasal system. This paper proposes that it is this system that constitutes the receptor for homeopathic medicines in both animal and human subjects.

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Sensory, somatosensory, and social stimulationThe human vomeronasal system

Abstract

Brain Res

Auris-Nasus-Larynx

J Steroid Biochem Mol Biol

Brain Res

Brain Res

J Steroid Biochem Mol Biol

Neuroscience

Horm Behav

Mol Brain Res

J Steroid Biochem Mol Biol

J Steroid Biochem Mol Biol

Neurosci Biobehav Rev

Synchronized discharges of the organ of Jacobsen

J Physiol

Chemical communication: The language of pheromones

Release of LH in the female rat by olfactory stimuli

The nervus terminalis in adult man

J Comp Neurol

Peripheral mechanisms of olfaction: Biochemistry and neurophysiology

The organization and function of the vomeronasal system

Annu Rev Neurosci

Chemical signals and reproductive behavior

Sensory, somatosensory, and social stimulation
The human vomeronasal system