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Pheromone Processing in Relation to Sex and Sexual Orientation
Abstract
Whether pheromone signaling exists in humans is still a matter of intense discussion. Emerging brain imaging studies suggest sexually dimorphic neuronal response to certain chemosignals, which, according to psychophysical data, possess pheromone-like properties. There are also indications that the neuronal response to these compounds depends on sexual orientation. Furthermore, our brain seems to be able to extract kin-specific signals, and processes body odors differently than other perceptually similar odors. Together, this data sheds new light on the chemosensory perception in humans and the implications thereof are discussed.
... Pour ces raisons, les phéromones n'ont plus qu'un effet résiduel chez les hominidés ( Doty, 2010). Même si on observe encore des activations cérébrales ( Savic, 2014), les effets affectifs et comportementaux sont faibles chez l'être humain ( Doty, 2014). Ces altérations de plusieurs types de gènes olfactifs ne sont pas des faits isolés. ...
... Au niveau olfactif, comme déjà indiqué, les processus spécifiques de l'orientation sexuelle sont grandement altérés chez les hominidés et l'être humain (organe voméronasal non fonctionnel et altération d'environ 90 % des gènes des récepteurs aux phéromones Zhang et Webb, 2003 ;Nei et al., 2008). Néanmoins il existe encore des effets de type phéromonaux ( Savic, 2014), mais résiduels ( Doty, 2014). Au niveau physiologique, l'influence des hormones diminue : à partir des primates simiens, on observe la disparition progressive des inhibitions pubertaires, saisonnières et oestrales ( Dixson, 2012), et chez l'être humain la sexualité peut s'exprimer à toutes les périodes de l'année et des cycles hormonaux. ...
L’objectif de cet article est d’identifier, chez les mammifères et l’être humain, les processus neurobiologiques de l’orientation sexuelle et de la formation des préférences sexuelles, puis d’évaluer leur importance respective. Les données ont été recueillies à partir d’une revue de la littérature qui concerne la neurobiologie de l’orientation et des préférences sexuelles. Chez les mammifères non primates (rongeurs, canidés, félidés, bovidés, équidés…), il existe différents types de processus et de situations à l’origine de la formation de préférences pour certains partenaires. Il existe également des processus neurobiologiques qui sont spécifiquement organisés pour l’orientation hétérosexuelle, et qui seraient, principalement, les circuits olfactifs qui détectent et traitent les phéromones sexuelles. Mais chez les hominidés (orangs-outans, gorilles, chimpanzés, bonobos, humains), les gènes des récepteurs aux phéromones sont altérés, diminuant ainsi l’importance fonctionnelle de ces processus de l’orientation sexuelle. Par contre, les processus à l’origine des préférences sexuelles deviennent plus importants. Pour ces raisons, chez l’être humain, les processus olfactifs altérés et les phéromones sexuelles n’auraient plus qu’une influence secondaire, et seraient combinés avec plusieurs autres facteurs (gènes, hormones, conditionnements, préférences sexuelles, émotions, processus cognitifs, contexte culturel). L’importance relative de chacun de ces facteurs dépendrait à la fois de caractéristiques physiologiques individuelles, du vécu singulier et des caractéristiques du contexte socioculturel. Cette combinaison complexe de plusieurs facteurs en interactions (incluant l’activité résiduelle des processus olfactifs de l’orientation sexuelle) serait à l’origine du développement de préférences sexuelles, propres à chaque personne.
... While the responses of other animals' functioning VNO to sex pheromones are robust and unmistakable, no such chemicals nor such responses have been found in humans (Savic, 2014a). ...
The biology of sexual orientations has intrigued people for generations. Many models have been providing insights to that topic, but there are still unanswered questions. In humans, sexual orientation has a learned component. Humans have to learn cues by which they identify the sex of their mates, and cues of the emotional messages that those mates broadcast. Many of those cues depend on arbitrary societal conventions. The cues are learned automatically and subconsciously during childhood, based on non-sexual experiences. When sexual orientation emerges at puberty, the youngsters cannot tell how and when they have acquired it. A model that deals with those phenomena is presented. A basic tenet of the model is that a sexual orientation is determined by the innate wirings of the brain. The model describes how the brain learns cues for identifying the sex of the mate, and cues for identifying emotional messages that the mate broadcasts. The learning mechanism is conditioning. The unconditioned stimulus is human voice. The unconditioned responses are the triggers of the physical and emotional manifestations of sexual activity. The model suggests that innate connections from auditory detectors of men’s and women’s voice onto brain centers that trigger sexual activities, such as the hypothalamus, determine the sexual orientation that emerges at puberty. Innate connections from those auditory centers to emotional centers, such as the amygdala, determine the learned emotional cues. It is also proposed that during evolution, the roles of the chemosensory system in identifying mates were taken over by the auditory system.
The sensitivity to androstenone and possible factors, determining the sensitivity were investigated for the large sample of inhabitants of central Russia (n = 860). Specific anosmia was detected in 48.8% of subjects. Women were more sensitive to androstenone than men. The proportion of men, but not women perceiving the smell of androstenone as a strong one in the concentration used decreased with age. Smoking, blood group, or ethnicity had no significant effect on the expression of specific anosmia and the perception of androstenone odor intensity.
Nonverbal communication is essential for human social interaction, either through static physical cues, such as phenotypic traits, facial and body appearance, or dynamic cues, such as faces and bodies in motion. Communication may be via touching, i.e., haptic communication, or at the spatial distance, i.e., proxemic communication. Communication among animals is most commonly mediated by olfactory signals. In many primates, sense of smell is significantly reduced compared to the smell of other vertebrates, while the visual modality is critical for social communication. About a quarter of the cortex is devoted to human visual perception and analysis. Visual modality provides a large amount of information about the identity of other individuals, their social status, emotional state and intended actions. The importance of face processing for survival is reflected in the extraordinary memory abilities of facial features and expressions in humans and other primates, as well as expressed powers of observation of subtle differences between faces.
Chemosensory-based communication is a vital signaling tool in most species, and evidence has recently emerged in support of the notion that humans also use social chemosignals (so-called pheromones) to communicate. An ongoing controversy does exist, however, concerning the receptor organ through which these chemicals are processed. There is a widespread belief that the vomeronasal organ (VNO) is responsible for processing social chemosignals in humans. Here we demonstrate that functional occlusion of the VNO does not change the percept of, sensitivity toward, or functional neuronal processing of a putative human pheromone. Perithreshold and suprathreshold perception of the endogenous chemical androstadienone (AND) were compared, as were positron emission tomography brain activations evoked by AND when the VNO was either occluded or left open. In addition, we compared sensitivity to AND in subjects with an identifiable VNO to those in whom no VNO could be detected. Thus we could examine the effects of the VNO at several different levels of processing. Occlusion or absence of the VNO did not affect either the perceptual measurements or the functional processing of the putative human pheromone, AND. These results provide strong evidence that the human VNO has no obvious function. Pheromonal communication in humans may be conveyed via the main olfactory system.
In contrast to many lower vertebrates, the vomeronasal epithelium (VNE) in humans has long been regarded as absent or functionally irrelevant. For example, the neural connection between the VNE and the accessory olfactory bulb has been reported to degenerate during the second half of pregnancy and its presence has not been demonstrated in adults. Further, reports on the organ's occurrence in adult humans have been contradictory. The aims of this study were to collect immunohistochemical data on the neurogenic or epithelial character of the VNE [for example, with antibodies against protein gene product 9.5 (PGP 9.5), olfactory marker protein (OMP), beta-tubulin, and cytokeratin], determine its proliferative capacity (for example, proliferating cell nuclear antigen), as well as to examine the differentiation activity of VNE cells and their interactions with extracellular matrix components (for example, hyaluronan receptor CD44, galectins, and caveolin). To this end, we studied the vomeronasal organs (VNOs) of 22 human cadavers, three adult biopsies, one embryo (week 8) and one fetus (week 13) by means of immunohistochemistry. The histology of the VNE appeared extremely heterogeneous. There were sections of stratified, respiratory, and typical "pseudostratified" vomeronasal epithelia consisting of slender bipolar cells. Mostly negative immunohistochemical results for OMP indicated that the human VNE does not function like the mature olfactory epithelium. In addition, the investigations did not support the hypothesis that neural connections between the VNE and central brain structures might be present. On the other hand, the presence of some bipolar cells positive for both PGP 9.5 and soybean lectin (SBA) pointed to a neuron-like activity of a small subset of VNE cells. Proliferation antigens located in the nuclei of basally located cells of the VNE were not regularly expressed. However, positive reactions for CD44 demonstrated a high activity of VNE cells in terms of differentiation and migration. Some bipolar cells showed immunoreactivity for caveolin indicating its possible role in signal transduction and differentiation. In summary, the reaction patterns of most antibodies in the adult human VNE are different from those obtained in the olfactory epithelium and the VNO of the rat. However, the VNE shows a specific pattern of activity unique to the mucosa of the nasal cavity. Considering the histologically well differentiated epithelium and its steady maintenance, the VNE of the adult human appears to be a highly differentiated structure the function of which remains unclear.
Prey species show specific adaptations that allow recognition, avoidance and defense against predators. For many mammalian species this includes sensitivity towards predator-derived odors. The typical sources of such odors include predator skin and fur, urine, feces and anal gland secretions. Avoidance of predator odors has been observed in many mammalian prey species including rats, mice, voles, deer, rabbits, gophers, hedgehogs, possums and sheep. Field and laboratory studies show that predator odors have distinctive behavioral effects which include (1) inhibition of activity, (2) suppression of non-defensive behaviors such as foraging, feeding and grooming, and (3) shifts to habitats or secure locations where such odors are not present. The repellent effect of predator odors in the field may sometimes be of practical use in the protection of crops and natural resources, although not all attempts at this have been successful. The failure of some studies to obtain repellent effects with predator odors may relate to (1) mismatches between the predator odors and prey species employed, (2) strain and individual differences in sensitivity to predator odors, and (3) the use of predator odors that have low efficacy. In this regard, a small number of recent studies have suggested that skin and fur-derived predator odors may have a more profound lasting effect on prey species than those derived from urine or feces. Predator odors can have powerful effects on the endocrine system including a suppression of testosterone and increased levels of stress hormones such as corticosterone and ACTH. Inhibitory effects of predator odors on reproductive behavior have been demonstrated, and these are particularly prevalent in female rodent species. Pregnant female rodents exposed to predator odors may give birth to smaller litters while exposure to predator odors during early life can hinder normal development. Recent research is starting to uncover the neural circuitry activated by predator odors, leading to hypotheses about how such activation leads to observable effects on reproduction, foraging and feeding.
Because humans seem to lack neuronal elements in the vomeronasal organ (VNO), many scientists believe that humans are unable to detect pheromones. This view is challenged by the observations that pheromone-like compounds, 4,16-androstadien-3-one (AND) and oestra-1,3,5(10),16-tetraen-3-ol (EST), activate the human hypothalamus. Whether these activations are mediated via VNO, venous blood or olfactory mucosa is presently unknown. To disentangle between the three alternatives, we conducted activation studies in 12 heterosexual males with chronic anosmia because of nasal polyps. Polyposis hampers signal transduction via the olfactory mucosa without interfering with the VNO or the pheromone transport via venous blood. Twelve healthy men served as controls. Subjects were investigated with (15)O-H(2)O PET during smelling of odorless air (base line), AND, EST, vanillin, and acetone. Smelling of EST activated the anterior hypothalamus in controls, but not anosmics. Neither did the anosmics display cerebral activations with AND or vanillin. Clusters were detected only with the trigeminal odorant acetone, and only in the thalamus, brainstem, the anterior cingulate, and parts of the sensorimotor cortex. Direct comparisons with controls (controls-anosmics) showed clusters in the olfactory cortex (amygdala and piriform cortex) with AND, vanillin, and acetone, and in the anterior hypothalamus with EST. The observed absence of olfactory and presence of trigeminal activations in anosmics indicates that polyposis primarily affected signal processing via the olfactory mucosa. The anosmics inability to activate the hypothalamus with EST, therefore, suggests that in healthy men EST signals were primarily transmitted via the olfactory system.
The main olfactory system, like the accessory olfactory system, responds to pheromones involved in social communication. Whereas pheromones detected by the accessory system are transmitted to the hypothalamus via the medial ('vomeronasal') amygdala, the pathway by which pheromones are detected and transmitted by the main system is not well understood. We examined in female mice whether a direct projection from mitral/tufted (M/T) cells in the main olfactory bulb (MOB) to the medial amygdala exists, and whether medial amygdala-projecting M/T cells are activated by volatile urinary odors from conspecifics or a predator (cat). Simultaneous anterograde tracing using Phaseolus vulgaris leucoagglutinin and Fluoro-Ruby placed in the MOB and accessory olfactory bulb (AOB), respectively, revealed that axons of MOB M/T cells projected to superficial laminae of layer Ia in anterior and posterodorsal subdivisions of the medial amygdala, whereas projection neurons from the AOB sent axons to non-overlapping, deeper layer Ia laminae of the same subdivisions. Placement of the retrograde tracer cholera toxin B into the medial amygdala labeled M/T cells that were concentrated in the ventral MOB. Urinary volatiles from male mice, but not from female conspecifics or cat, induced Fos in medial amygdala-projecting MOB M/T cells of female subjects, suggesting that information about male odors is transmitted directly from the MOB to the 'vomeronasal' amygdala. The presence of a direct MOB-to-medial amygdala pathway in mice and other mammals could enable volatile, opposite-sex pheromones to gain privileged access to diencephalic structures that control mate recognition and reproduction.
Mammalian vomeronasal receptors respond to pheromones conveying information on gender, reproductive status and individual recognition. The question arises as to how this information is coded, which parts of the code require combinatorial activity and whether or not there are specific receptor neurons committed to sex discrimination. Are there receptor neurons that are committed to responding for female or male pheromones? Is there a sex difference for the proportion of these receptors, bearing in mind that it is very much in the male's interest to distinguish the restricted oestrous phase of the female's cycle in order to successfully mate? Perhaps more intriguing is the complexity of individual recognition and whether or not the vomeronasal receptors actually possess this capacity. A recent paper in Science by Ron Yu and colleagues addresses these issues by literally visualising patterns of activity in VNO slices and determining what information is common across different individuals and what distinguishes them.
Various lines of evidence indicate that men generally experience greater sexual arousal (SA) to erotic stimuli than women. Yet, little is known regarding the neurobiological processes underlying such a gender difference. To investigate this issue, functional magnetic resonance imaging was used to compare the neural correlates of SA in 20 male and 20 female subjects. Brain activity was measured while male and female subjects were viewing erotic film excerpts. Results showed that the level of perceived SA was significantly higher in male than in female subjects. When compared to viewing emotionally neutral film excerpts, viewing erotic film excerpts was associated, for both genders, with bilateral blood oxygen level dependent (BOLD) signal increases in the anterior cingulate, medial prefrontal, orbitofrontal, insular, and occipitotemporal cortices, as well as in the amygdala and the ventral striatum. Only for the group of male subjects was there evidence of a significant activation of the thalamus and hypothalamus, a sexually dimorphic area of the brain known to play a pivotal role in physiological arousal and sexual behavior. When directly compared between genders, hypothalamic activation was found to be significantly greater in male subjects. Furthermore, for male subjects only, the magnitude of hypothalamic activation was positively correlated with reported levels of SA. These findings reveal the existence of similarities and dissimilarities in the way the brain of both genders responds to erotic stimuli. They further suggest that the greater SA generally experienced by men, when viewing erotica, may be related to the functional gender difference found here with respect to the hypothalamus.
The vomeronasal organ (VNO) of mammals plays an essential role in the perception of chemical stimuli of social nature including pheromone-like signals but direct evidence for the transduction of pheromones by vomeronasal sensory neurons has been lacking. The recent development of electrophysiological and optical imaging methods using confocal microscopy has enabled researchers to systematically analyze sensory responses in large populations of mouse vomeronasal neurons. These experiments revealed that vomeronasal neurons are surprisingly sensitive and highly discriminative detectors of volatile, urinary metabolites that have pheromonal activity in recipient mice. Functional mapping studies of pheromone receptor activation have uncovered the basic principles of sensory processing by vomeronasal neurons and revealed striking differences in the neural mechanisms by which chemosensory information is detected by receptor neurons in the VNO and the main olfactory epithelium. These advances offer the opportunity to decipher the logic of mammalian pheromonal communication.
Whether different odorous compounds (odorants) are processed by different cerebral circuits is presently unknown. A first step to address this complicated issue is to investigate how the cerebral regions mediating signals from olfactory (i.e., unimodal) odorants, differ from those mediating the olfactory + trigeminal (i.e., bimodal) odorants. [15O]-H2O-PET scans were conducted in 12 healthy females during three separate conditions: birhinal, passive smelling of: 1) the unimodal odorant vanillin; 2) the bimodal odorant acetone; and 3) odorless air. Significant activations were calculated contrasting vanillin to air, acetone to air, and deactivations, running these contrasts in the opposite direction. Smelling of vanillin activated bilaterally the amygdala and piriform cortex. These regions were only engaged slightly by acetone. Instead, strong activations were found in the anterior and central insula and claustrum, the posterior portion of anterior cingulate, the somatosensory cortex (SI for face), cerebellum, ventral medial (VMPo) and dorsal medial (MDvc) thalamus, the lateral hypothalamus, and pons/medulla. In parallel, the somatosensory (SI, below central representation of face), secondary visual and auditory cortices, as well as the supplementary motor area and the parahippocampal gyri were deactivated. No deactivations were observed with vanillin, although the odor components of acetone and vanillin were rated similarly intense (75 +/- 17 mm vs. 61 +/- 22 mm, NS). The differentiated pattern of cerebral activation during odorant perception seems to be dependent on the signal transducing cranial nerves involved. In contrast to vanillin, which solely activates the olfactory cortex, acetone engages predominantly trigeminal projections from the nasal mucosa. Acetone's limited activation of the olfactory cortex may result from a cross-modal interaction, with inhibition of acetone's odor component by its trigeminal component.
The role of genetic and environmental influences on age of initiation of first sexual relations and engaging in sexual activity with multiple partners (10 or more partners in 1 year) was investigated in male twins (N = 6,744) from the Vietnam Era Twin Registry. Individual differences in both types of sexual behaviors were heritable, but only age of onset of sexual relations was significantly influenced by the environment shared by the twins. There was a moderate negative correlation between age of initiation of sexual relations and the multiple partners variable; initiating sexual relations earlier was associated with a higher probability of having multiple partners. The additive genetic influence on age of initiation also influenced the multiple partners variable. The substantial unique environmental influences on each variable were uncorrelated with each other. The data suggest that the observed association between age of initiation of sexual relations and having multiple partners is due to genetic influences common to both behaviors.
Vomeronasal organ (VNO) morphology varies markedly across primate taxa. Old World monkeys display no postnatal VNO. Humans and at least some apes retain a vestigial VNO during postnatal life, whereas the strepsirrhines and New World Monkeys present a morphologically well-defined VNO that, in many species, is presumed to function as an olfactory organ. Available microanatomical and behavioral studies suggest that VNO function in these species does not precisely duplicate that described in other mammalian taxa. The questions of which species retain a functional VNO and what functions they serve require inquiry along diverse lines but, to be functional, the vomeronasal epithelium must be neuronal and olfactory. We used immunohistochemistry to establish these criteria in six primate species. We compared the expression of two neuronal markers, neuron-specific beta-tubulin (BT) and protein gene product 9.5, and olfactory marker protein (OMP), a marker of mature olfactory sensory neurons, in paraffin-embedded VNO sections from two strepsirrhine and four haplorhine species, all of which retain morphologically well-defined VNOs during postnatal life. The infant Eulemur mongoz, adult Otolemur crassicaudatus, neonatal Leontopithicus rosalia, and adult Callithrix jacchus express all three proteins in their well-defined vomeronasal neuroepithelia. The infant Tarsius syrichta showed some BT and OMP immunoreactivity. We establish that two strepsirrhine species and at least some New World haplorhines have mature sensory neurons in the VNO. In contrast, at all ages examined, Saguinus geoffroyi VNO expresses these markers in only a few cells.