DRAFT Desire emerges from excitement. A psychophysiological perpective on sexual motivation. Stephanie Both Walter Everaerd Ellen Laan Department of Psychology, University of Amsterdam, Roetersstraat 15, 1018 WB Amsterdam, The Netherlands (email: sboth@uva.nl) In the dominant model of human sexual response sexual desire, excitement, and orgasm are distinguished as consecutive phases (DSM-IV, 1994). The model is based on the psychophysiological research of Masters and Johnson (1966), and on the ideas of the psychiatrist and sex therapist Helen Kaplan (1995) who introduced the desire phase as the phase preceding sexual excitement. Kaplan was seeing in her clinic many female patients complaining about a lack of desire for sex. Absence of sexual desire, she reasoned, points to a phase in the normal sexual response cycle that activates the wanting to experience sexual excitement. “By thus examining the current sexual experiences of 2,109 patients and couples with chief complaints of deficient sexual desire I came to the conclusion that the pathological decrease of these patients’ libido is essentially an expression of the normal regulation of sexual motivation gone awry. More specifically, sexual motivation or desire, just like other needs or motives, such as hunger and thirst, is regulated by CNS control mechanisms.” (Kaplan, 1995, p. 3-4). Kaplan conceptualized sexual desire as an expression of a drive, comparable to hunger and thirst, influenced by sensors that signal changes in the internal environment of the body. In her view on sexual desire, psychoanalytic thinking can be heard; thinking that has long dominated ideas about sexual motivation. Even though there is little evidence for a homeostatic mechanism in human sexual motivation, the essence of the concept of sexual drive remains in the dominant model of sexual response and in the DSM diagnosis of hyposexual desire that is based on that model. In this contribution, first, the concepts libido, lust and drive that were introduced by Freud will be discussed. Then modern motivation theory and the close relationship between emotion and motivation mechanisms will be elaborated upon. This relationship will be illustrated by recent experimental studies that we conducted on motor preparation, sexual arousal and action. Sexual arousal and desire will be considered in the light of current knowledge about neurobiological 2 mechanisms of emotion and motivation. After that we will talk about the interaction of emotion and motivation circuits in the brain, and the role of dopamine in motivation. We will conclude that current knowledge about emotion and motivation mechanisms argues against Helen Kaplan’s assumption that desire and excitement are distinctive sexual response phases. Desire results from the conscious awareness of the sexually excited state of the body and the brain. This means that the experience of sexual desire can only come about through sexual excitement. The drive model versus incentive motivation models of sexual motivation The concepts of libido, lust, and drive Sexual motivation is a construct, used to explain the generation of sexual action. Sexual desire is the (subjective) experience of being attracted to or pushed towards objects or behaviors with potential rewarding effects. As we noted before, in Freud’s days sexual motivation was seen as a constant force (Everaerd, Laan, Both, & Spiering, 2001). For sexual desire Freud (1953) preferred the use of the word libido. "Everyday language possesses no counterpart to the word 'hunger', but science makes use of the word 'libido' for that purpose." (p. 135). In a footnote, added by Freud, it is explained that the German language word 'Lust' is ambiguous, because it can either mean the experience of need and of a gratification. In a note on page 212 the explanation has been elaborated upon. "The word 'Lust' takes into account the part played by preparatory sexual excitations which simultaneously produce an element of satisfaction and a contribution to sexual tension". 'Lust' has two meanings, and is used to describe the sensation of sexual tension ('Ich habe Lust = 'I should like to', 'I feel impulse to') as well as the feeling of satisfaction. Thus the word lust refers to sexual 3 arousal and the wanting to have more of that, as well as to sexual satisfaction. We will come across these two different meanings later on when concepts of wanting and liking that are important in recent motivation theories are discussed. Libido, according to Freud (1964), is fuelled by the sexual instincts. An instinct arises from a source within the body. "Its source is a state of excitation in the body, its aim is the removal of that excitation; on its path from its source to its aim the instinct becomes operative psychically. We picture it as a certain quota of energy which presses in a particular direction. It is from this pressing that it derives its name of 'Trieb' (literally 'drive)" (p .96). Freud made clear that libido does not arise from an external stimulus. "An instinct, then, is distinguished from a stimulus by the fact that it arises from sources of stimulation within the body, that it operates as a constant force and that the subject can not avoid it by flight, as is possible with an external stimulus" (p. 96). Freud conceived of the instinct as energy that pushes towards a certain direction. From that push-factor the German word ‘Trieb’, drive, is derived. Thus the sexual instinct comes from a source within the body, it operates as a constant force, and the subject can not escape from it as is possible in the case of an external stimulus. In this view libido is the result of an internal bodily tension, and there would be a need to neutralize this state. How the drive builds up remains unclear. In her discussion of the regulation of sexual motivation Kaplan (1995) used the concepts libido, lust and drive. She localized the sexual instinct in the hypothalamus, the organ in the brain where physiological deficits and the restoration of homeostasis are signalled. “ Once again we can learn from the similarities between eating and sex. More specifically, under normal circumstances, a state of starvation activates the ventromedial hypothalamic “appetite centers”. This neurophysiologic activity produces a subjective feeling of hunger” (Kaplan, 1995, p. 17). Because it is unknown how processes in the hypothalamus contribute to sexual motivation for the time being 4 she considered it to be a black box that, in interaction with sexual inciters, activates sexual desire and lust. There is, however, no evidence of any adverse effects of sexual abstinence. As Beach (1956) concluded: “No genuine tissue or biological needs are generated by sexual abstinence …. What is commonly confused with a primary drive associated with sexual deprivation is in actuality sexual appetite, and this has little or no relation to biological or physiological needs” (p. 4). In the case of sex there does not seem to be a biological need that demands satisfaction, as is the case in hunger and thirst. More recently, Herbert (2001) proposed that sexual behaviour may be thought of as a form of adaptation or response to a perceived deficit. He suggested that the hypothalamus uses the current levels of gonadal steroids to monitor the current levels of sexual interest and behaviour. He underlined, however, that sexual behaviour is a complex activity that relies upon the receipt and analysis of complex social stimuli. Animals and humans will only be brought into sexual readiness by changes in hormone levels when a sexually attractive stimulus is perceived. Incentive motivation According to the drive model we have sex because we feel sexual desire, this is an expression of Freud’s view that there is a constant force that seeks an outlet. Incentive motivation theories emphasize that sexual motivation is the result of the activation of a sensitive sexual response system by sexually competent stimuli that are present in the environment (Bindra, 1974; Singer & Toates, 1987). Once the sexual system, wherein sensitivity is influenced by hormones and neurotransmitters, interacts with the stimulus, the individual is pushed towards sexual activity. In this view sexual motivation does not emerge through a deficit signaled by the hypothalamus, but through the attractiveness of possible rewards in the environment. Desire is activated, through 5 expectations of reward, by attractive and rewarding stimuli in the environment. Motivation is strongly related to emotion mechanisms. Emotion and motivation mechanisms interact in such a way that it is sometimes hard to distinguish them; they are two sides of one coin. According to Bindra (1974) motivation emerges in the interaction of the organism and the environment. There is no motivation without a stimulus that predicts reward or danger (Schultz, 1998). Our brains are designed to adequately respond to changes in the environment, to avoid danger and to approach situations that may be rewarding. We learn through experience what is dangerous and what is rewarding. Emotions can be looked upon as action mechanisms that help the organism to adapt to aspects of the environment that promote or endanger survival. In this view emotions serve to satisfy concerns, and therefore result in motivational states or action tendencies (e.g. Frijda, 1986; Lang, 1993; LeDoux, 2001). The motivational state or action tendency is reflected in the physiological changes that accompany emotions and which prepare the body for action. Cognitive neuroscience is revealing how emotions, the consequent motivational states or action tendencies, and emotional feelings appear (Craig, 2002; Damasio, 2003; LeDoux, 2001). The actual or imagined presence of an emotionally competent stimulus activates the emotion-triggering sites in the brain. These emotion-triggering sites subsequently activate the emotion-execution sites that activate changes in the internal organs, and in the musculoskeletal system. Damasio (2003) and LeDoux (2001), and a long time before them William James (1884), stress that the conscious experience of emotion, what we call feelings, is the result of the perception of these changes. Feelings do not precede but follow emotion; feelings are based on the feedback of the emotional bodily and brain responses to the brain. Feelings are the end result of the whole ‘machinery of emotion’. 6 We propose that the mechanism through which sexual emotional states and feelings of sexual excitement and desire appear, will be similar as in other emotions that are coupled with relatively strong bodily reactions. Recently functional imaging studies showed that the subjective experience of different emotions like anger, disgust, anxiety, and sexual arousal is associated with activation of the insula and the orbitofrontal cortex (Craig, 2002; Morris, 2002; Sumich, Kumari, & Sharma, 2003). This indicates that the insula has a generalized role that is not specific to any particular emotion. Its role seems to be the representation of peripheral autonomic arousal that provides input to conscious awareness of emotional states. We suppose that processing of a sexual stimulus automatically results in preparation of the organism for sexual action. When we become aware of these bodily changes, through feedback of these bodily responses to the brain, we experience sexual excitement and desire. Thus, sexual desire does not appear out of the blue. Without a stimulus that activates arousal there will be no desire. In fact, there is no good reason to assume that desire and excitement are two fundamentally different things. Perhaps we can phenomenologically distinguish them such that feelings of excitement represent the subjective experience of genital changes, perhaps combined with a conscious evaluation that the situation is indeed ‘sexy’, and that feelings of desire represent the subjective experience of an action tendency, of a willingness to behave sexually. Processing of emotionally competent stimuli results in physiological changes that prepare the body for action. In case of threatening stimuli avoidance behavior will be activated, and in case of attractive (sexual) stimuli appetitive behavior will be triggered. Appetitive behavior includes locomotor responses to the goal, and occurs in parallel with autonomic and endocrine responses that prepare for efficient interaction with the goal (Robbins & Everitt, 1999). The generation of sexual appetitive behavior involves specific genital reactions. However, there will be also changes in the 7 somatic motor system. Signals are sent to the muscles to prepare for action. Eventually, these changes may result in sexual behavior. We will illustrate this process by discussing recent psychophysiological studies on motor preparation, sexual arousal and action. Sexual arousal and action tendency Research in women by Ellen Laan showed that there is an automatic relationship between sexual stimuli and genital response, and that this response may emerge without the person being aware of that (Laan & Everaerd, 1995). Recently we focused on somatic motor system changes that result from the processing of emotionally competent stimuli. More specifically, we searched for an appropriate measure for motor preparation. One way to do this is to monitor changes in the amplitude of reflexes. Motor preparation involves heightened activity in the spinal cord, and that activity will be expressed as a stronger reflex (Brunia & Boelhouwer, 1988). The reflex we use is the Achilles tendon reflex, for short, the T-reflex. Tendon reflexes are not sensitive to valence of an affective state, but they are augmented in states of preparation for action, and are modified by differences in arousal intensity (Bonnet, Bradley, Lang, & Requin, 1995; Brunia & Boelhouwer, 1988; Brunia & van Boxtel, 2000). Therefore investigation of T reflex modulation offers a window on the generation of action. Bonnet et al. (1995) hypothesized that stimuli that elicit emotional arousal will facilitate T reflex magnitude, relative to neutral, low arousal stimuli. They stated that the T reflex, which functions when the limb is activated for walking, standing, and other activities, is inherently nondirectional (one can run either towards or away from stimulation). Since the T reflex is nondirectional it would be involved both in actions that are appetitevely and defensively motivated. 8 They studied the modulation of T reflexes during the presentation of pictures from 'The International Affective Picture System' designed by Lang, Öhman, and Vaitl (1988). These pictures were designed to induce emotions varying in valence (positive to negative) and in intensity (low to high). As expected, T reflexes were significantly augmented when elicited during processing of highly arousing emotional pictures (either negative or positive) as compared with neutral pictures. Similar to Bonnet et al. we hypothesized emotional stimuli to automatically generate action tendencies. These action tendencies will result in increased spinal excitability, reflected in facilitated T reflex magnitude. We studied reflex modulation by appetitive (sexual) and aversive (anxiety and sexual threat) (Both, Everaerd, & Laan, 2003) and by sexual stimuli varying in intensity (Both, Everaerd, & Laan, in preparation). In these studies T reflex amplitude, genital response, subjective sexual arousal and subjective action tendencies were measured. In the first study subjects were shown 4 film clips of 5 minutes each: a sex stimulus depicting consensual sexual activity, an anxiety-provoking film, a sexually threatening film, and a neutral film that was not expected to be emotionally arousing. It was expected that the 3 emotional stimuli would result in changes in subjective action tendencies, the sexual film in a facilitated approach tendency and the sexually threatening and the anxiety-provoking film in a facilitated avoidance tendency. It was also expected that the 3 emotional stimuli would result in stronger Treflexes than the neutral film, and that reflexes during the neutral film would not be higher than during the preceding rest period. Both the positive and the negative emotional stimuli resulted in motor preparation, and the subjects reported that during the threatening stimuli they felt the wish to avoid, and during the consensual sexual stimulus the wish to approach. The increase in reflex amplitude in response to the sexual stimulus did not differ from the increase in response to the threatening stimuli. 9 In a second study sexual stimuli were used that differed in intensity. The low intensity stimulus depicted erotic kissing, the medium stimulus showed kissing and caressing, and the high intensity stimulus depicted intercourse. From a previous study of Ellen Laan (Laan, Everaerd, van der Velde, & Geer, 1995) we knew that these particular clips evoked distinct, and increasing levels of genital arousal in women. As expected, T-reflex amplitude increased with increasing levels of sexual stimulation, and these were significant differences even in a small sample of 10 women. These studies demonstrate that in interaction with emotionally competent stimuli a tendency is generated to avoid or approach. Negative or positive emotional stimuli generate an affective response, and part of this affective response is the generation of an action tendency, which is an expression of motivation. This action tendency increases as the intensity of the emotional state increases. To demonstrate that confrontation with a sexually competent stimulus leads to action tendencies and, eventually, sexual action, we studied sexual activity after laboratory induced sexual arousal (Both, Spiering, Everaerd, & Laan, under review). Male and female subjects were randomly assigned to a neutral or sexual condition. In the neutral condition subjects were exposed to a 15-minute neutral film, and in the sexual condition to a 15-minute erotic film. We expected that only in the sexual condition genital responses, subjective feelings of sexual arousal, and approach tendencies would be elicited. Subjects completed, 24 hours after the experimental session, a questionnaire about their sexual behavior during these 24 hours. We expected that subjects in the erotic film condition would engage in more sexual activity than the subjects in the neutral film condition. As expected, the subjects that were exposed to the erotic film had genital responses, increased T-reflexes, and reported sexual arousal and approach tendencies. Those exposed to the neutral film did not show these specific reactions. Moreover, the subjects who had seen the erotic film had engaged in more sexual activity than the subjects who did not see the erotic film. In sum, 10 these studies show that confrontation with sexual stimuli results in action tendencies, and these action tendencies increase the likelihood of actual sexual behavior. Neurobiological mechanisms In retrospect, Bindra’s view that emotion and motivation mechanisms are closely intertwined is in agreement with current ideas about how the brain may work. Sensory information is converted in the brain to set off motor responses in the autonomic and somatic nervous system. Bindra had no clear idea of the neurobiological mechanism that may explain the interaction of limbic and motor systems. Mogenson, Jones and Yim did a proposal in 1980 that still inspires motivation research (Mogenson et al., 1980; LeDoux, 2001). Recently Holstege (1998) did a similar proposal, the ‘emotional-motor system’. Holstege distinguishes the somatic motor system and the emotional motor system. The somatic motor system is controlled by the motor cortex and the brainstem. Through this system voluntary movements are controlled. The emotional motor system is controlled by structures that are part of or are connected with the emotional circuit in the brain, the limbic system. Through the emotional motor system specific emotional behaviors, like for example mating behavior, and more general changes, like increased muscle tension, are initiated. Mogenson, et al. (1980), and more recently LeDoux (2001), present the following sketch of the interaction between the limbic system, the emotion circuit, and the motor system, the motivation circuit. The interface between the amygdala, part of the limbic system, and the motor system is the nucleus accumbens. The nucleus accumbens receives direct input from the amygdala, and indirect input from the ventral tegmental area. This area is the source of the dopaminergic connections to the nucleus accumbens. This nucleus accumbens passes the information on to the globus pallidus, 11 which is connected to cortical and brainstem areas that control movement. This interface between the emotional and the motor circuit is necessary because primary (emotional) needs need to be transformed into actions, to satisfy those needs. Dopamine has an important role in the motivational circuit; it seems to be involved in both reward signalling and in the initiation of motor responses (Kalivas & Nakamura, 1999; Phillips et al, 2003). Dopamine has long been regarded as the transmitter responsible for the experience of satisfaction. However, studies in rats have shown that dopamine is not involved in the valence or appreciation of a stimulus, but in the tendency to approach a stimulus (Berridge, 1996). Berridge introduced the concepts of ‘wanting’ and ‘liking’. Liking represents the affective response to a stimulus. Both rats and humans exhibit specific facial expressions with the negative or positive appreciation of food, from these specific facial expressions the affective response can be derived. Wanting represents the tendency to approach a stimulus. This tendency may express itself in the frequency and intensity with which a rat presses a lever to obtain food. Berridge showed that manipulation of the dopamine system affects the instrumental behavior (wanting), and not the facial expressions (liking). The difference between wanting and liking is relevant for understanding disorders related to motivation. It explains why a person who is addicted to some substance can crave for the drug intensely, whereas subsequent intake of the drug is not very satisfying. Animal studies have shown facilitating effects of dopamine on sexual motivation (Melis & Argiolas, 1995), and the very few studies in humans also showed a facilitating effect of dopamine on sexual motivation and sexual arousal (Meston & Frohlich, 2000). We reasoned that measuring somatic motor system activity through means of T reflex modulation may offer a sensitive measure to investigate the effects of psychomotor stimulant drugs like dopamine on sexual arousal and sexual motivation in humans. We wanted to find out whether a dopamine agonist, that increases 12 dopamine levels in the brain, would affect sexual response, particularly action tendencies. We expected dopamine to affect the wanting component of sexual motivation, specifically the instigation of action, and therefore to result in stronger T reflex magnitudes in response to sexual stimulation. Secondly, based on the evidence for dopaminergic influences on penile response in men (e.g. Giuliano & Allard, 2001; Heaton, 2000), we expected levodopa to facilitate genital response. Conscious emotional feelings, and subjectively experienced tendencies for approach behavior may also be affected by levodopa. Although Berridge (1996) underlines that awareness of a motivational state may be dissociable from the underlying motivational processes that give rise to the conscious experience, it may be expected that substantial changes in the underlying processes will enter consciousness and will be reflected in subjective report. Both men and women participated to allow for investigation of gender differences in the effects of dopamine on sexual responses. Subjects (19 men and 28 women) were given a single dose of levodopa (100 mg), which increases dopamine levels in the brain (Both, Everaerd, Laan, & Gooren, in preparation). Participants visited the laboratory 2 times, receiving at one visit a placebo and at the other visit levodopa, following a double blind, crossover protocol. Fifty minutes after placebo/drug administration, when substantial dopamine levels were expected, subjects were asked to engage in a pleasant sexual fantasy, and then they were shown an erotic film. T reflexes, genital responses, subjective action tendencies and subjective sexual arousal in response to erotic stimulation were measured. We found that levodopa did not affect the subjective and the genital responses. There was a significant effect of levodopa on T-reflexes. In men, T-reflexes were stronger with levodopa, both in the sexual fantasy and in the erotic film condition. In women there were no effects of levodopa at all. Thus in accordance with evidence from studies in male rats, an increased level of 13 dopamine resulted in stronger instigation of action in response to sexual incentives in human males. The absence of an effect of levodopa on T reflex magnitude in women is in line with the conflicting reports about the effects of dopamine on sexual motivation in female rats (Meston & Frohlich, 2000) and warrants further study. The fact that levodopa increased male T reflex magnitude during sexual stimulation shows that, in line with the expectations, dopamine is involved in the energetic aspects of motivated behavior, and that T reflex modulation offers a sensitive measure for dopaminergic effects on the generation of sexual appetitive behavior in humans. About the sex difference in the effect of levodopa we can only speculate. As noted before, studies on dopaminergic effects on sexual motivation in female rats revealed conflicting results. These conflicting results are attributed to possible interactions of dopamine with the hormonal treatments that are used to induce estrus in female rats. There is evidence for steroid-dopamine interactions (e.g. Balthazart, Baillien, & Ball, 2002; Becker, 1999; Giuliano & Allard, 2001). The gender difference in the effect of levodopa in the present study might be due to differences in sex steroid levels in the brain. Perhaps the effect of dopamine depends on testosterone levels, which are higher in males. It would be informative to include hormonal status as a variable in future studies on dopaminergic effects on sexual responses in women. Conclusion The mechanism of sexual motivation can be summarized as follows. Processing of a sexually competent stimulus (actually present or imagined) automatically energizes emotional systems, resulting in bodily changes that prepare for sexual action. The elicited action tendency increases as the intensity of the emotional state increases. Dopamine is important for the transformation of 14 emotion into action. It seems to be involved in both reward signalling and in the initiation of behavioural action. The bodily changes that are elicited by a sexually competent stimulus include motor responses involved in general approach behaviour, and motor responses involved in sexspecific responses; e.g. relaxation of genital smooth muscles. The processing of a sexually competent stimulus is largely involuntary and unconscious. Feelings of sexual excitement and desire emerge when motor responses enter consciousness through the feedback of the bodily and brain responses to the brain. From this follows that the experience of sexual feelings is a consequence of an incentive energizing the sexual system. Feelings of sexual desire and excitement result from the awareness of the sexually excited state of the body and the brain. Hence, the experience of sexual desire can only come about through sexual excitement. Contrary Kaplan’s proposal sexual desire does not precede sexual excitement; excitement precedes sexual desire. However, the concepts of libido and drive can be replaced by more precise concepts derived from cognitive neuroscience. In addition, we know that reports of patients about sexual desire may be as much a reflection of current ideas or myths about sexual desire as to what actually happens in the motivational process. The consequences of our view on sexual desire are important for practice. From an incentive motivation model it should be concluded that hyposexual desire is not a manifestation of a malfunctioning instinct, but an indication that the emotion-motivation mechanism is not activated. In some cases hypoactive sexual desire may be caused by a lack of brain chemicals, but in most cases the cause will be the absence of attractive stimuli. In fact Kaplan was aware of that, since an important part of her treatment for hyposexual desire consisted of what she called: “Libido enhancing sexual homework assignments: fantasy and friction” (Kaplan, 1995, p. 6). That homework could be sexual fantasy, explicit erotic material, masturbation, or other methods of 15 erotic stimulation. Secondly, an incentive motivation view emphasizes the importance of the evaluation of the stimulus, which is determined by individual histories of sexual rewards. When a patient has little or no experience with sexual rewards or a mainly negative sexual or relational history, pharmacological enhancement of the sensitivity of the sexual system (be it with androgens, dopamine, or other pro-sexual drugs) will not facilitate sexual desire. 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