The neural mechanisms of mate choice: a hypothesis

Scientists have described many physical and behavioral traits in avian and mammalian species that evolved to attract mates. But the brain mechanisms by which conspecifics become attracted to these traits is unknown. This paper maintains that two aspects of mate choice evolved in tandem: 1) traits that evolved in the "display producer" to attract mates and, 2) corresponding neural mechanisms in the "display chooser" that enable them to become attracted to these display traits. Then it discusses our (in-progress) fMRI brain scanning project on human romantic attraction, what we believe is a developed form of "courtship attraction" common to avian and mammalian species as well as the primary neural mechanism underlying avian and mammalian mate choice. The paper hypothesizes that courtship attraction is associated with elevated levels of central dopamine and norepinephrine and decreased levels of central serotonin in reward pathways of the brain. It also proposes that courtship attraction is part of a triune brain system for mating, reproduction and parenting. 1)The sex drive evolved to motivate birds and mammals to court any conspecifics. 2) The attraction system evolved to enable individuals to discriminate among potential mating partners and focus courtship activities on particular individuals, thereby conserving mating time and energy. 3) The neural circuitry for attachment evolved to enable individuals to complete species-specific parental duties.     

Lust, attraction, and attachment in mammalian reproduction

This paper proposes that mammals exhibit three primary emotion categories for mating and reproduction: (1) the sex drive, or lust, characterized by the craving for sexual gratification; (2) attraction, characterized by increased energy and focused attention on one or more potential mates, accompanied in humans by feelings of exhilaration, “intrusive thinking” about a mate, and the craving for emotional union with this mate or potential mate; and (3) attachment, characterized by the maintenance of close social contact in mammals, accompanied in humans by feelings of calm, comfort, and emotional union with a mate. Each emotion category is associated with a discrete constellation of neural correlates, and each evolved to direct a specific aspect of reproduction. The sex drive is associated primarily with the estrogens and androgens; it evolved to motivate individuals to seek sexual union. The attraction system is associated primarily with the catecholamines; it evolved to facilitate mate choice, enabling individuals to focus their mating effort on preferred partners. The attachment system is associated primarily with the peptides, vasopressin, and oxytocin; it evolved to motivate individuals to engage in positive social behaviors and assume species-specific parental duties. During the evolution of the genus Homo, these emotion systems became increasingly independent of one another, a phenomenon that contributes to human mating flexibility and the wide range of contemporary human mating and reproductive strategies.     

The neurobiology of love

Romantic and maternal love are highly rewarding experiences. Both are linked to the perpetuation of the species and therefore have a closely linked biological function of crucial evolutionary importance. The newly developed ability to study the neural correlates of subjective mental states with brain imaging techniques has allowed neurobiologists to learn something about the neural bases of both romantic and maternal love. Both types of attachment activate regions specific to each, as well as overlapping regions in the brain's reward system that coincide with areas rich in oxytocin and vasopressin receptors. Both deactivate a common set of regions associated with negative emotions, social judgment and 'mentalizing' that is, the assessment of other people's intentions and emotions. Human attachment seems therefore to employ a push-pull mechanism that overcomes social distance by deactivating networks used for critical social assessment and negative emotions, while it bonds individuals through the involvement of the reward circuitry, explaining the power of love to motivate and exhilarate. Yet the biological study of love, and especially romantic love, must go beyond and look for biological insights that can be derived from studying the world literature of love, and thus bring the output of the humanities into its orbit.     

The neural basis of human female mate copying: An empathy-based social learning process

We used functional magnetic resonance imaging (fMRI) to investigate the neural basis of human female mate copying. Consistent with previous mate copying effects, women's attractiveness ratings for target males increased significantly greater after the males were observed paired with romantic partners versus ordinary friends, and this was mainly accounted for by males being paired with attractive romantic partners. Attractiveness ratings for male targets were lower when they were paired with an attractive opposite-sex friend. The fMRI data showed that the observational learning process in mate copying recruited brain regions including the putamen, the inferior frontal gyrus, the middle cingulate, the SMA, the insula, and the thalamus – areas overlapped with brain regions involved in empathy. The blood-oxygen-level-dependent (BOLD) signals in higher cognitive functions including the parieto-frontal network, as well as visual areas, were significantly more activated when women evaluated males in the friend versus romantic-partner context, whereas brain regions were not more active in the reverse comparison, suggesting that less cognitive functions or as least no more functions were involved in evaluating the quality of target males in the romantic-partner context than in the friend context. Further analysis indicated that specific brain regions related to the evaluation process of mate copying were associated with bilateral fusiform gyrus (FFA). Thus, results are consistent with a view that mate copying is a domain-specific adaptation involving an empathy-based social-learning process that is also associated with reduced cognition.     

Intense passionate love attenuates cigarette cue-reactivity in nicotine-deprived smokers: an FMRI study

Self-expanding experiences like falling in love or engaging in novel, exciting and interesting activities activate the same brain reward mechanism (mesolimbic dopamine pathway) that reinforces drug use and abuse, including tobacco smoking. This suggests the possibility that reward from smoking is substitutable by self-expansion (through competition with the same neural system), potentially aiding cessation efforts. Using a model of self-expansion in the context of romantic love, the present fMRI experiment examined whether, among nicotine-deprived smokers, relationship self-expansion is associated with deactivation of cigarette cue-reactivity regions. Results indicated that among participants who were experiencing moderate levels of craving, cigarette cue-reactivity regions (e.g., cuneus and posterior cingulate cortex) showed significantly less activation during self-expansion conditions compared with control conditions. These results provide evidence that rewards from one domain (self-expansion) can act as a substitute for reward from another domain (nicotine) to attenuate cigarette cue reactivity.     

Viewing pictures of a romantic partner reduces experimental pain: involvement of neural reward systems

The early stages of a new romantic relationship are characterized by intense feelings of euphoria, well-being, and preoccupation with the romantic partner. Neuroimaging research has linked those feelings to activation of reward systems in the human brain. The results of those studies may be relevant to pain management in humans, as basic animal research has shown that pharmacologic activation of reward systems can substantially reduce pain. Indeed, viewing pictures of a romantic partner was recently demonstrated to reduce experimental thermal pain. We hypothesized that pain relief evoked by viewing pictures of a romantic partner would be associated with neural activations in reward-processing centers. In this functional magnetic resonance imaging (fMRI) study, we examined fifteen individuals in the first nine months of a new, romantic relationship. Participants completed three tasks under periods of moderate and high thermal pain: 1) viewing pictures of their romantic partner, 2) viewing pictures of an equally attractive and familiar acquaintance, and 3) a word-association distraction task previously demonstrated to reduce pain. The partner and distraction tasks both significantly reduced self-reported pain, although only the partner task was associated with activation of reward systems. Greater analgesia while viewing pictures of a romantic partner was associated with increased activity in several reward-processing regions, including the caudate head, nucleus accumbens, lateral orbitofrontal cortex, amygdala, and dorsolateral prefrontal cortex--regions not associated with distraction-induced analgesia. The results suggest that the activation of neural reward systems via non-pharmacologic means can reduce the experience of pain.     

The Neurobiology of Love

Love is a complex neurobiological phenomenon, relying on trust, belief, pleasure and reward activities within the brain, i.e., limbic processes. These processes critically involve oxytocin, vasopressin, dopamine, and serotonergic signaling. Moreover, endorphin and endogenous morphinergic mechanisms, coupled to nitric oxide autoregulatory pathways, play a role. Naturally rewarding or pleasurable activities are necessary for survival and appetitive motivation, usually governing beneficial biological behaviors like eating, sex, and reproduction. Yet, a broad basis of common signaling and beneficial neurobiological features exists with connection to the love concept, thereby combining physiological aspects related to maternal, romantic or sexual love and attachment with other healthy activities or neurobiological states. Medical practice can make use of this concept, i.e., mind/body or integrative medicine. Thus, love, pleasure, and lust have a stress-reducing and health-promoting potential, since they carry the ability to heal or facilitate beneficial motivation and behavior. In addition, love and pleasure ensure the survival of individuals and their species. After all, love is a joyful and useful activity that encompasses wellness and feelings of well-being.     

Non‐verbal mate retention behaviour in women and its relation to couple's relationship adjustment and satisfaction

The function of mate retention strategies is to preserve the bond between romantic partners and to prevent desertion, which is also why such behaviours are often elicited by the presence of a potential rival. Most existing studies on mate retention are based on self‐reports, which are prone to various biases. In this study, we observed non‐verbal behaviour of 47 long‐term romantic heterosexual couples during their interview with a female experimenter, whom the women in the couples may have perceived as a potential rival. We measured non‐verbal displays of mate retention tactics (direct guarding, intimacy inducement, appearance enhancement, and love and care display), as well as relationship maintenance strategies of openness and positivity. We expected that relationship quality as reported by both partners in the couple would be positively associated with ‘benefit‐provisioning’ mate retention behaviours and negatively associated with a ‘cost‐inflicting’ mate retention tactic (direct guarding). Relationship quality was assessed by Spanier's Dyadic Adjustment Scale using both the total score of dyadic adjustment and a Dyadic Satisfaction subscale. We found a significant association between both partners' dyadic adjustment and satisfaction and woman's appearance enhancement behaviours (such as self‐touch, hair flip and primp) in the presence of her partner and a potential rival. We also found a negative association between partner's dyadic adjustment and woman's direct guarding of partner using short looks, and a positive association between woman's intimacy‐inducing behaviour using long gaze and her own dyadic satisfaction and her partner's dyadic adjustment. Our results highlight the specific role of female attractiveness in later stages of romantic relationships within the context of mate retention and draw attention to the significance of the use of observational techniques in addition to self‐reports.     

Simultaneously hermaphroditic shrimp use lipophilic cuticular hydrocarbons as contact sex pheromones

Successful mating is essentially a consequence of making the right choices at the correct time. Animals use specific strategies to gain information about a potential mate, which is then applied to decision-making processes. Amongst the many informative signals, odor cues such as sex pheromones play important ecological roles in coordinating mating behavior, enabling mate and kin recognition, qualifying mate choice, and preventing gene exchange among individuals from different populations and species. Despite overwhelming behavioral evidence, the chemical identity of most cues used in aquatic organisms remains unknown and their impact and omnipresence have not been fully recognized. In many crustaceans, including lobsters and shrimps, reproduction happens through a cascade of events ranging from initial attraction to formation of a mating pair eventually leading to mating. We examined the hypothesis that contact pheromones on the female body surface of the hermaphroditic shrimp Lysmata boggessi are of lipophilic nature, and resemble insect cuticular hydrocarbon contact cues. Via chemical analyses and behavioural assays, we show that newly molted euhermaphrodite-phase shrimp contain a bouquet of odor compounds. Of these, (Z)-9-octadecenamide is the key odor with hexadecanamide and methyl linoleate enhancing the bioactivity of the pheromone blend. Our results show that in aquatic systems lipophilic, cuticular hydrocarbon contact sex pheromones exist; this raises questions on how hydrocarbon contact signals evolved and how widespread these are in the marine environment.     

The (bidirectional) associations between romantic attachment orientations and mate retention behavior in male-female romantic couples

Attachment orientations of anxiety and avoidance are associated with many important romantic relationship outcomes. An evolutionary perspective has informed research on the associations between attachment orientations and mate retention behaviors, which individuals perform to retain their romantic partner and maintain their relationship. In the current article, we report two dyadic studies (n = 104, United States; n = 978, Germany, Switzerland, Austria) that evaluated: (1) whether bivariate associations between attachment orientations and mate retention domains are replicable; (2) whether an individual's attachment orientation predicts their partner's mate retention behaviors; and (3) whether, over time, mate retention behaviors predict attachment orientations within couples. Results of both studies replicated previous bivariate associations between attachment anxiety and cost-inflicting mate retention behaviors. Longitudinal dyadic data from Study 2 demonstrated that cost-inflicting mate retention behaviors, specifically, predict future attachment anxiety in romantic partners. These results contribute to the emerging body of research addressing the associations between attachment orientations and mate retention behaviors, and suggest an important (bidirectional) role of attachment anxiety in predicting negative partner-directed behaviors in romantic relationships.     

Reward-related FMRI activation of dopaminergic midbrain is associated with enhanced hippocampus-dependent long-term memory formation

Long-term potentiation in the hippocampus can be enhanced and prolonged by dopaminergic inputs from midbrain structures such as the substantia nigra. This improved synaptic plasticity is hypothesized to be associated with better memory consolidation in the hippocampus. We used a condition that reliably elicits a dopaminergic response, reward anticipation, to study the relationship between activity of dopaminergic midbrain areas and hippocampal long-term memory in healthy adults. Pictures of object drawings that predicted monetary reward were associated with stronger fMRI activity in reward-related brain areas, including the substantia nigra, compared with non-reward-predicting pictures. Three weeks later, recollection and source memory were better for reward-predicting than for non-reward-predicting pictures. FMRI activity in the hippocampus and the midbrain was higher for reward-predicting pictures that were later recognized compared with later forgotten pictures. These data are consistent with the hypothesis that activation of dopaminergic midbrain regions enhances hippocampus-dependent memory formation, possibly by enhancing consolidation.     

Adaptive mating strategies and the problem of mate retention

"Adaptations" are evolved solutions to the problems posed by survival and reproduction. The evolutionary psychologists believe that as well as the physical adaptations so the adaptations in human mind evolved, called "strategies". The "mating strategies" are adaptive solutions to successful mating. The mating strategies, designed to preserve access to a mate by preventing encroachment of intrasexual rivals and by preventing a mate from defecting from the mateship for a prospective better partner, are called "mate guarding strategies". The previous research found that humans do use a wide variety of behavioural tactics of mate guarding, ranging from vigilance to violence. Our research group explores the type and the intensity of behavioural tactics of mate guarding used in several contexts. Presently, the link between the woman's fertility status across her menstrual cycle and the man's mate guarding is examined. Discussing the preliminary results, a more intensive man's mate guarding of his partner around the ovulation when her fertility peaks may be assumed. These outcomes could be explained as an adaptive prevention to shift in woman's preferences to increase her extra-pair sexual attempts and following to a possible genetic cuckoldry at that most fertile time.     

Mate preferences and choices for facial and body hair in heterosexual women and homosexual men: influence of sex,population, homogamy,and imprinting-like effect

Recent research has reported that male body and facial hair influence women's mate preferences. However, it is not clear whether such preferences are typical for women or for individuals who prefer males as sexual partners. Here we explored body and facial hair in preferred and actual partners among men and women who prefer men as sexual partners. Including homosexual individuals provides a unique opportunity to investigate whether evolved mating psychologies are specific to the sex of the individual or sex of the partner. Based on an online survey of 1577 participants from Brazil and the Czech Republic, we found that, on average, homosexual men preferred hairier stimuli than heterosexual women, supporting past findings that homosexual men have strong preferences for masculine traits. Preferences for facial and body hair appear to be influenced less by sex of the preferred partner than sex of the individual, pointing to a possible sex-specific mating psychology. Further, Brazilians preferred bigger beards than Czechs, which was positively associated with the self-reported amount of beardedness in Brazil, suggesting that familiarity effects underpin cross-cultural differences in preferences for facial hair. Moreover, homosexual men preferred a self-similar degree of beardedness, and Czech women preferred a similar degree of beardedness as their fathers had during their childhood. However, these effects were not associated with the level of facial hair in their actual partners; in general, mate preferences and actual mate choices for facial and body hair differed. Thus, individual differences in some self-reported characteristics, cultural factors, and aspects of personal experience may modulate differences in preferences for masculine traits.     

Same-Sex Gaze Attraction Influences Mate-Choice Copying in Humans

Mate-choice copying occurs when animals rely on the mating choices of others to inform their own mating decisions. The proximate mechanisms underlying mate-choice copying remain unknown. To address this question, we tracked the gaze of men and women as they viewed a series of photographs in which a potential mate was pictured beside an opposite-sex partner; the participants then indicated their willingness to engage in a long-term relationship with each potential mate. We found that both men and women expressed more interest in engaging in a relationship with a potential mate if that mate was paired with an attractive partner. Men and women''s attention to partners varied with partner attractiveness and this gaze attraction influenced their subsequent mate choices. These results highlight the prevalence of non-independent mate choice in humans and implicate social attention and reward circuitry in these decisions.     

Romantic love modulates women's identification of men's body odors

Romantic love is one of our most potent and powerful emotions, but very little is known with respect to the hormonal and psychological mechanisms in play. Romantic love is thought to help intimate partners stay committed to each other and two mechanisms have been proposed to mediate this commitment: increased attention towards one's partner or deflected attention away from other potential partners. Both mechanisms find support in the literature. We explored the potential influence of each of these mechanisms by assessing women's ability to identify (ID) body odors originating from their boyfriend, a same-sex friend, and an opposite-sex friend and the relationship between this ability and the degree of romantic love expressed towards their boyfriend. We hypothesized that an increase in attention towards one's partner would render a positive correlation between ID of a boyfriend's body odor and degree of romantic love; conversely, we hypothesized that attention deflected away from other potential partners would render a negative correlation between ID of an opposite-sex friend's body odor and degree of romantic love for the boyfriend. Our results supported the deflection theory as we found a negative correlation between the degree of romantic love for the subjects' boyfriends and their ability to ID the body odor of an opposite-sex friend but not of their boyfriend or same-sex friend. Our results indicate that romantic love deflects attention away from potential new partners rather than towards the present partner. These changes are likely mediated by circulating neuropeptides and a testable model is suggested.     

Reverse Correlating Love: Highly Passionate Women Idealize Their Partner’s Facial Appearance

A defining feature of passionate love is idealization—evaluating romantic partners in an overly favorable light. Although passionate love can be expected to color how favorably individuals represent their partner in their mind, little is known about how passionate love is linked with visual representations of the partner. Using reverse correlation techniques for the first time to study partner representations, the present study investigated whether women who are passionately in love represent their partner’s facial appearance more favorably than individuals who are less passionately in love. In a within-participants design, heterosexual women completed two forced-choice classification tasks, one for their romantic partner and one for a male acquaintance, and a measure of passionate love. In each classification task, participants saw two faces superimposed with noise and selected the face that most resembled their partner (or an acquaintance). Classification images for each of high passion and low passion groups were calculated by averaging across noise patterns selected as resembling the partner or the acquaintance and superimposing the averaged noise on an average male face. A separate group of women evaluated the classification images on attractiveness, trustworthiness, and competence. Results showed that women who feel high (vs. low) passionate love toward their partner tend to represent his face as more attractive and trustworthy, even when controlling for familiarity effects using the acquaintance representation. Using an innovative method to study partner representations, these findings extend our understanding of cognitive processes in romantic relationships.     

Influence of Dopaminergically Mediated Reward on Somatosensory Decision-Making

Reward-related dopaminergic influences on learning and overt behaviour are well established, but any influence on sensory decision-making is largely unknown. We used functional magnetic resonance imaging (fMRI) while participants judged electric somatosensory stimuli on one hand or other, before being rewarded for correct performance at trial end via a visual signal, at one of four anticipated financial levels. Prior to the procedure, participants received either placebo (saline), a dopamine agonist (levodopa), or an antagonist (haloperidol). Principal findings: higher anticipated reward improved tactile decisions. Visually signalled reward reactivated primary somatosensory cortex for the judged hand, more strongly for higher reward. After receiving a higher reward on one trial, somatosensory activations and decisions were enhanced on the next trial. These behavioural and neural effects were all enhanced by levodopa and attenuated by haloperidol, indicating dopaminergic dependency. Dopaminergic reward-related influences extend even to early somatosensory cortex and sensory decision-making.     

Human face processing is tuned to sexual age preferences

Human faces can motivate nurturing behaviour or sexual behaviour when adults see a child or an adult face, respectively. This suggests that face processing is tuned to detecting age cues of sexual maturity to stimulate the appropriate reproductive behaviour: either caretaking or mating. In paedophilia, sexual attraction is directed to sexually immature children. Therefore, we hypothesized that brain networks that normally are tuned to mature faces of the preferred gender show an abnormal tuning to sexual immature faces in paedophilia. Here, we use functional magnetic resonance imaging (fMRI) to test directly for the existence of a network which is tuned to face cues of sexual maturity. During fMRI, participants sexually attracted to either adults or children were exposed to various face images. In individuals attracted to adults, adult faces activated several brain regions significantly more than child faces. These brain regions comprised areas known to be implicated in face processing, and sexual processing, including occipital areas, the ventrolateral prefrontal cortex and, subcortically, the putamen and nucleus caudatus. The same regions were activated in paedophiles, but with a reversed preferential response pattern.     

Neural responses during anticipation of a primary taste reward

The aim of this study was to determine the brain regions involved in anticipation of a primary taste reward and to compare these regions to those responding to the receipt of a taste reward. Using fMRI, we scanned human subjects who were presented with visual cues that signaled subsequent reinforcement with a pleasant sweet taste (1 M glucose), a moderately unpleasant salt taste (0.2 M saline), or a neutral taste. Expectation of a pleasant taste produced activation in dopaminergic midbrain, posterior dorsal amygdala, striatum, and orbitofrontal cortex (OFC). Apart from OFC, these regions were not activated by reward receipt. The findings indicate that when rewards are predictable, brain regions recruited during expectation are, in part, dissociable from areas responding to reward receipt.     

Elimination of the vesicular acetylcholine transporter in the striatum reveals regulation of behaviour by cholinergic-glutamatergic co-transmission

Cholinergic neurons in the striatum are thought to play major regulatory functions in motor behaviour and reward. These neurons express two vesicular transporters that can load either acetylcholine or glutamate into synaptic vesicles. Consequently cholinergic neurons can release both neurotransmitters, making it difficult to discern their individual contributions for the regulation of striatal functions. Here we have dissected the specific roles of acetylcholine release for striatal-dependent behaviour in mice by selective elimination of the vesicular acetylcholine transporter (VAChT) from striatal cholinergic neurons. Analysis of several behavioural parameters indicates that elimination of VAChT had only marginal consequences in striatum-related tasks and did not affect spontaneous locomotion, cocaine-induced hyperactivity, or its reward properties. However, dopaminergic sensitivity of medium spiny neurons (MSN) and the behavioural outputs in response to direct dopaminergic agonists were enhanced, likely due to increased expression/function of dopamine receptors in the striatum. These observations indicate that previous functions attributed to striatal cholinergic neurons in spontaneous locomotor activity and in the rewarding responses to cocaine are mediated by glutamate and not by acetylcholine release. Our experiments demonstrate how one population of neurons can use two distinct neurotransmitters to differentially regulate a given circuitry. The data also raise the possibility of using VAChT as a target to boost dopaminergic function and decrease high striatal cholinergic activity, common neurochemical alterations in individuals affected with Parkinson's disease.