In anthropomorphic terms we could say that the female rat invites the male to copulate, i.e. she expresses her consent to having sex, and the male can accept or not accept that invitation by pursuing or not pursuing the female

Sexual incentive motivation, sexual behavior, and general arousal: Do rats and humans tell the same story? Anders Ågmo, Ellen Laan. Neuroscience & Biobehavioral Reviews, February 26 2022, 104595. https://doi.org/10.1016/j.neubiorev.2022.104595

Highlights

• Sexual motivation is activated by external stimuli called sexual incentives

• Exposure to sexual incentives leads also to enhanced general arousal

• General arousal enhances activity in the sexual central motive state

• Activity in the sexual central motive state requires the presence of gonadal hormones

• The determinants of interindividual differences in sexual motivation are unclear

Abstract: Sexual incentive stimuli activate sexual motivation and heighten the level of general arousal. The sexual motive may induce the individual to approach the incentive, and eventually to initiate sexual acts. Both approach and the ensuing copulatory interaction further enhance general arousal. We present data from rodents and humans in support of these assertions. We then suggest that orgasm is experienced when the combined level of excitation surpasses a threshold. In order to analyze the neurobiological bases of sexual motivation, we employ the concept of a central motive state. We then discuss the mechanisms involved in the long- and short-term control of that state as well as those mediating the momentaneous actions of sexual incentive stimuli. This leads to an analysis of the neurobiology behind the interindividual differences in responsivity of the sexual central motive state. Knowledge is still fragmentary, and many contradictory observations have been made. Nevertheless, we conclude that the basic mechanisms of sexual motivation and the role of general arousal are similar in rodents and humans.

Keywords: Sexual motivationgeneral arousalcentral motive stategonadal hormonespituitary hormoneshypothalamic hormonestransmittersdopamineorgasmgenital arousal

5.3. Viscerosomatic responses and general arousal

Visceral responses, mainly genital blood flow, to sexual stimuli have been the subject of much research. It is possible that these responses are associated with enhanced general arousal. This could easily be shown by calculating correlations between the magnitude of the genital response (erection and vaginal lubrication) and typical indicators of general arousal such as blood pressure, heart rate, respiration frequency or the galvanic skin response. Although all these variables have been recorded in the same individuals in many studies (e.g. Suschinsky and Lalumière, 2012), reports of correlations are exceptional. In fact, there is only one study in which correlations between the genital response and heart rate and the galvanic skin response were calculated (Laan et al., 1995). Contrary to what could be expected, both vaginal pulse amplitude and vaginal blood volume during exposure to a pornographic movie segment were unrelated to heart rate and the skin response. This observation suggest that the intensity of genital arousal is not a main determinant of general arousal in women. The possible relationship between the intensity of the viscerosomatic response of erection and the level of general arousal has not been studied.

Whereas the effects of genital responses on general arousal is unclear, there are many observations regarding the inverse relationship, i.e. the effects of general arousal on genital responses. In fact, there is a reasonable amount of data available from studies that have employed objective measures of genital responses to explicit sexual stimuli after manipulations of the level of general arousal. In an elegant experiment by Cindy Meston (Meston, 2000) women were shown a sexual stimulus (pornographic movie segment) either when rested or after intense physical exercise. It is well known that exercise increases general arousal. The vaginal response to the movie segment was enhanced in the women having engaged in physical exercise, i.e. women with enhanced general arousal. Similar effects were found after treatment with ephedrine, an agonist at postsynaptic adrenergic α and β receptors (Meston and Heiman, 1998). Stimulation of these receptors enhances activity in the sympathetic nervous system, another arousal-producing event. Anxiety has also been found to increase the vaginal response to sexual stimuli (Hoon et al., 1977, Palace and Gorzalka, 1990), and anxiety is thought to enhance arousal (Ramsey, 1943). Studies in men have also shown that enhanced general arousal, because of conditioned fear, leads to enhanced penile response to a sexually relevant stimulus (Barlow et al., 1983). Likewise, an emotionally arousing, non-sexual video fragment enhances the penile response to an ensuing pornographic video segment (Wolchik et al., 1980). Since enhanced response to a constant stimulus must be due to increased motivation, it can tentatively be concluded that increasing general arousal stimulates the activity of the sexual central motive state, hence sexual motivation, in men and women.

Although there are many studies supporting the conclusion above, it must be mentioned that an extensive review of the effects of anxiety on sexual responses found that the relationship may be more complicated (e.g. Bradford and Meston, 2006). Several studies have failed to find any effect at all of anxiety on genital responses (e.g. Elliott & O'Donohue, 1997; Sipski et al., 2004) while others have reported decreased response (Masters & Johnson, 1970). Consequently, it is premature to make any firm affirmation concerning the influence of general arousal on genital responses in men and women.

Pupil dilation is a non-sexual response to many kinds of stimuli (reviewed in Einhäuser, 2017). When recorded during exposure to a sexual stimulus, it might be considered a visceral response to this stimulus. If young men and women are stressed and concurrently exposed to pictures with erotic content, the pupil dilation are larger than in the absence of stress, and the stress effect is larger for erotic pictures than for neutral pictures (Finke et al., 2018). The stress-induction procedure was found to increase blood pressure and heart rate, showing that general arousal indeed was enhanced. This study suggests that general arousal not only enhances sexual visceral responses to sexual stimuli, but also non-sexual visceral responses to such stimuli. We propose that this action is mediated by the sexual central motive state, and that the heightened pupillary response is indicative of facilitated cognitive processing of sexual stimuli.

The role of general arousal for the viscerosomatic responses in rodents is poorly known. Only one study has evaluated the consequences of enhanced general arousal for penile erection. Rats were subjected to an anxiety-inducing procedure, and erections stimulated by apomorphine were quantified. The anxiety procedure enhanced heart rate and mean arterial pressure, confirming increased arousal. The number of erections observed in these animals was reduced compared to controls (Brien et al., 2002). Even if these data are not conclusive, they suggest that there might be a negative relationship between increased general arousal and erection. Nevertheless, it is probably prudent to abstain from any conclusion until more data have become available.

A curious illustration of a possible relationship between general arousal and sexual responses is found in the association between yawning and penile erection in male rats. Prolonged observation has revealed that erection and yawning often coincides (Holmgren et al., 1985). A major function of yawning is to enhance general arousal in environments providing little stimulation (Baenninger, 1997), such as a rat’s home cage. The momentarily enhanced arousal leads to a genital response, suggesting activation of the central motive state. Whether the association between yawning and sexual activation also is present in humans is not known. Regardless of this, there are probably other, equally likely, explanations for the temporal coincidence of yawning and erection.

We know of no data concerning vaginal responses and general arousal in rodents. In the absence of more experimental evidence in favor of effects of general arousal on genital responses in males and females we propose that rats are different from humans in the way that variations in general arousal have variable effects on genital responses to sexual incentives.

There is an indirect way in which general arousal could affect human genital responses. The level of arousal is known to be a determinant of the efficiency of cognitive processing, in the way that moderate arousal facilitates processing whereas very low or very high arousal have deleterious effects (e.g. Lambourne and Tomporowski, 2010). The importance of cognitive processes for genital responses in men and women has been well established (Tavares et al., 2020). Interference with cognitive processing of sexual stimuli leads to reduced genital response. For example, while women were watching a pornographic movie, they were asked to perform tasks of increasing difficulty. The lowest level of difficulty were no task, and the highest level was a requirement to classify pairs of digits according to complex rules, and verbalize the result aloud (Salemink and van Lankveld, 2006). The classification rules were complex indeed: together the digits form a number; odd numbers under 50 are classified as A; even numbers under 50 are classified as B; odd numbers over 50 are classified as B; even numbers over 50 are classified as A (Salemink and van Lankveld, 2006, p. 182). The more difficult the task, the larger the reduction of the genital response. Similar data have been reported from a male sample (van Lankveld & van den Hout, 2004). Manipulations facilitating attention to sexual stimuli enhanced responses in men and women (Both et al., 2011, Farkas et al., 1979). Perhaps the somewhat variable effects of arousal-enhancing procedures on human genital responses can be explained by their unintended, equally variable, effects on cognitive processing.

5.4. Transition from approach to copulation

In humans, the transition involves a conscious decision about whether to proceed with sexual activities or not to proceed. Decision-making is known to enhance general arousal (Johnson, 1963) as manifested in increased heart rate and galvanic skin response. Likewise, pupil dilation, an exquisite indicator of general arousal (Bradley et al., 2008) occurs during the decision process (de Gee et al. (2014) and references therein). It seems likely that the decision to pass from sexual approach behaviors to sexual activity leads to enhanced general arousal as other decisions do. The same should be the case for the contrary decision, not to proceed with sex. Even though the cognitive processes underlying the decision to engage in sexual activities are poorly known, some informed speculation is possible.

It seems that most humans will not initiate partnered sex without explicit or implicit consent from the partner. In fact, in Western societies, and probably in many others, sexual approaches and ensuing sexual activities are socially acceptable only between consenting individuals. Predictions about obtaining consent for sexual interaction are probably an important part of the initial transition from approach to further sexual activity. However important such predictions may be at early stages of sexual approach, these predictions must be confirmed before manifest sexual activities start. Thus, the approaching individual needs to determine whether the approached individual is consenting to sexual activity or not. There seems to have existed conflicting views on how consent or lack thereof is communicated to a potential partner. It now appears that the consenting individual uses direct or indirect verbal expressions as well as direct and indirect non-verbal cues to communicate consent (reviewed in Fenner, 2017). These strategies are also used in pornographic movies (Willis et al., 2020), which may be important since, for many young people, such movies have become the main source of sex education.

Men and women communicate consent in similar ways, and both sexes understand their partner’s communication equally well (Hickman and Muehlenhard, 1999), even in casual encounters (Beres, 2010). The fact that men accused of rape or sexual harassment frequently argue that they misunderstood the message from the non-consenting party can be considered a kind of unfounded self-justification (Maruna and Mann, 2006).

Provided consent is obtained, direct physical interaction between the approaching and approached individuals will usually ensue. This will further enhance general arousal (see below). The contrary outcome, the potential partner’s refusal of consent, may also lead to enhanced arousal, perhaps because of frustration. Even the act of refusing further interaction may lead to enhanced arousal. There is some indirect evidence for this (Chen et al., 2014, Zhou et al., 2009). Thus, whatever the outcome, the transition process probably enhances general arousal, and consequently contributes to the activity in the central motive state. Possible consequences are that the rejected individual persists in approach behaviors even if the partner has declined, or that these behaviors become directed towards another individual. There is, however, no direct evidence for any of these alternatives. Enhanced arousal in the rejecting individual will probably reinforce some central motive state different from the sexual.

In rodents, the search for consent before initiating copulation does not seem to be of major concern. One reason for this may be that rodents are not sexually attracted to other individuals unless these others show unequivocal signs of being ready for copulation. We have carefully analyzed the sexual interactions between male and female rats in a seminatural environment, and we have found that sexually experienced males rarely approach a non-receptive female (Chu and Ågmo, 2015a, Chu and Ågmo, 2015b, Le Moëne et al., 2020a). An example is shown in Fig. 3. Furthermore, a male almost never mount a female not showing paracopulatory behavior (Bergheim et al., 2015). Thus, the execution of copulatory acts on part of the male depends on the female’s behavior. Likewise, males need almost always to pursue the female before they come into position for executing a mount. In anthropomorphic terms we could say that the female rat invites the male to copulate, i.e. she expresses her consent to having sex, and the male can accept or not accept that invitation by pursuing or not pursuing the female. It appears, then, that sexual interactions among rats are limited to consensual sexual activities. This is not true in standard observation procedures, in which the experimenter subjects the rats to forced sexual interaction, but it is true in ecologically valid procedures, like the seminatural environment. In any case, whereas the transition from approach to copulation in humans is based on a conscious decision, there is no reason to believe that something similar occurs in rats. There, the transition appears to be an automatic process. Thus, there is no arousal-enhancing decision making involved.

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7. Sexual and general arousal are intrinsically associated

In the preceding overview, we have tried to ascertain the potential role of several compounds in the long- and short-term control of sexual motivation, i.e. the activity of the sexual central motive state. Furthermore, we have described how these compounds may be affected by general arousal. One purpose was to find out whether there is a bidirectional relationship between actions on sexual motivation and actions on general arousal. Table 2 summarizes the results of this analysis. It appears that there is not any necessary coincidence between release caused by general arousal and effects on the central motive state neither in rodents nor in humans. Since data concerning the effects of altered general arousal on release of many of the compounds listed in Table 2 are lacking, this is a tentative conclusion. It may also be observed that the compounds known to be released during sex are also released by enhanced general arousal. This is not surprising, since sex enhances general arousal.

We have presented abundant evidence showing that whenever sexual responses are activated, general arousal is also increased. We have also shown that some compounds released during the exposure to sexual incentives simultaneously enhance sexual and general arousal. This coincidence is not surprising. In rats and humans, copulatory behavior involves substantial physical activity, in the form of coordinated activity in skeletal muscles. The level of general arousal is an important determinant of that activity. At the same time, copulation requires a series of specific genital responses. The main genital response in males is erection, in the human an entirely vascular response. In the rat, vascular erection is reinforced by contraction of the striated penile muscles. Furthermore, in the rat, activity in these muscles is necessary for achieving vaginal penetration, and they will also contribute to the expulsion of semen at ejaculation in rats and men. During the first phase of ejaculation, seminal emission, smooth muscles in the epididymis and vas deferens will propel spermatozoa into the urethra while other smooth muscle cells will expel the contents of the seminal vesicle and the prostate. These contents will form the bulk of the ejaculate. In females, the main genital responses are clitoral engorgement and vaginal lubrication. Interestingly, there is some evidence suggesting that these sexual responses may be activated outside of sexual contexts by extreme levels of general arousal (Sachs, 2007, Sachs, 2008). What we could call “effective sexual motivation”, or momentaneous activity level in the sexual central motive state, is always a combination of sexual and general arousal, as we try to illustrate in Fig. 1. We have found no evidence for any difference between humans and rodents in this respect.

8. Are the differences between rats and humans more than trivial?

Another purpose with the description of the hormonal and transmitter responses to sexual stimuli or sexual activities or changes in the level of general arousal was to compare rodents and humans. Similarities would strengthen the popular notion that rodents can be used to predict effects of drugs on human sexual functions (Ågmo, 2014, Ågmo et al., 2004, Le Moëne and Ågmo, 2019). Important dissimilarities would question that notion. The summaries presented in Table 1, Table 2 clearly suggest a strong similarity between rodents and humans. The neurochemical control of the sexual central motive state seems to have been highly conserved among mammals, and it should, consequently, be possible to make reliable predictions from one mammalian species to another.