1 The Role of Conditioning in Sexual Arousal Heather Hoffmann Conditioning models hold intuitive appeal for explaining the etiology of atypical sexual arousal. The majority of treatments for sexual disorders are based on such models (Plaud & Martini, 1999) and numerous case studies attest to the effectiveness of behavior or response modification techniques in dealing with paraphilias (Gaither, Rosenkranz & Plaud, 1998). It is also a common theoretical assumption that learning plays an important role in the development of normative sexual arousal patterns (e.g., Ågmo, 1999; Hardy, 1964; McConaghy, 1987; Pfaus, Kippin, & Centeno, 2001; Roche& Barnes, 1998; Woodson, 2002). Yet there are limited laboratory data, at least in humans, showing the effects of learning on sexual arousal, and precisely how conditioning processes affect what we find erotic remains unclear. Since I am interested in the how stimuli acquire sexually arousing properties the present chapter will focus on classical conditioning. However, a brief review of the two standard types of laboratory conditioning paradigms and their interaction may be useful. Classical (a.k.a. Pavlovian or respondent) conditioning involves learning about the relationship between an initially “ineffective” cue (the CS) and a behaviorally significant stimulus (the US) and typically results in a conditioned emotional or motivational state (the CR). Operant (a.k.a. Skinnerian or instrumental) conditioning typically creates changes in the frequency of (goal-directed) behavior (R) resulting from its association with reinforcing or punishing consequences (SR). Pavlovian and instrumental conditioning can be distinguished at a conceptual and procedural level, but in practice it has been difficult to separate their effects (Schwartz, 1989). For example, it was once thought that the different 2 types of conditioning were applicable to different classes of behavior (i.e., classical to autonomic responses and operant to skeletal ones). However, operant procedures have been shown to affect reflexive behavior and voluntary responding can be classically conditioned. Procedures exist for separating the roles of classical and operant contingencies in the control of behavior but their interactions are complex and both processes appear to simultaneously affect any given learning situation. For example, in sexual learning situations, stimuli that have acquired arousing properties through Pavlovian procedures can also contribute to the approach of those stimuli. Such an explanation has been used to describe the development of paraphilias (Junginger, 1997; McGuire, Carlisle, & Young, 1965). An accidental pairing of a neutral object (CS) with arousal or orgasm (US) gives the stimulus erotic value. Sexual arousal to the object (CR) elicits approach and/or masturbation (R) that is positively reinforced by an increase in sexual arousal and orgasm (SR). Both conditioning processes most likely contribute to acquired arousal but the classical association appears to be at the core of such learning. In addition, the majority of studies in both animals and humans have examined the role of Pavlovian procedures in sexual arousal. The laboratory evidence Nonhumans Pfaus, Kippen, and Centeno (2001) provide the most recent review of the influence of learning on sexual and reproductive behaviors in a variety of species, including humans. They concluded that classical and operant conditioning produce both temporary and lasting changes in appetitive, precopulatory, and consummatory sexual behavior. Although Sachs and Garinello (1978) found conditioned decreases in the time to display penile erection in 3 rats, sexual arousal in nonhuman research is usually measured indirectly through changes in latencies to engage in other sexual behaviors. For example, Domjan and colleagues found conditioned approach, conditioned courtship, and conditioned copulatory behaviors in male quail in the presence of CSs (e.g., colored lights, orange feathers, bird models, and contextual cues) that were previously paired with either visual exposure to a female or the opportunity to copulate with a female (for review see Domjan & Holloway, 1998). In male rats, Zamble, Hadad, Mitchell and Cutmore (1985) found conditioned decreases in ejaculatory latency in the presence of a CS (plastic tub) that had previously been paired with exposure to a female without consummation. Kippin, Talianakas, and Pfaus (1997) found conditioned ejaculatory preference to females scented with an odor which was previously associated with the ability to copulate. Studies on conditioning of female sexual arousal are less common. Gutiérrez and Domjan (1997), found increases in squatting behavior (an index of sexual receptivity) in female quail, following the paired presentation of a particular compartment (CS) and copulatory opportunity. Female rats engage in a wide range of behaviors that control their sexual interactions with males, but it has yet to be demonstrated which of, and to what extent, these behaviors are influenced by conditioning (Pfaus et al., 2001). Humans O’Donohue and Plaud (1994) have provided the most recent review of the conditioning of human sexual arousal. They concluded that while there is some evidence for classically conditioned sexual arousal in men as measured by changes in penile circumference or volume (e.g., Kantorowitz, 1978; Langevin & Martin, 1975; Rachman, 1966; Rachman & Hodgson, 1968), interpretation of the results are complicated by 4 methodological problems. They reported no studies showing that conditioning can affect sexual arousal in women. Since the O’Donohue and Plaud review was published, two well-controlled studies using non-clinical samples have shown convincing evidence for respondent conditioning of male sexual arousal. Lalumière and Quinsey (1998) found enhanced genital responding to slides of partially nude females after they had been paired with sexually explicit videotapes of heterosexual interactions, and Plaud and Martini (1999) found increases in penile circumference to a penny jar after it was paired with slides of nude or partially nude females. Letourneau and O’Donohue (1997) examined the role of classical conditioning in women’s sexual responses but they failed to show conditioned genital or subjective responses to a CS (an amber light) that had been repeatedly paired with an erotic film. In contrast, Hoffmann, Janssen, & Turner (2003) found conditioned genital arousal in women. Procedural differences may account for the discrepancy. Like Letourneau and O’ Donohue, we used a visual stimulus as the CS and erotic film clips as USs, yet our stimulus and interval parameters were more succinct (paralleling those used in studies finding conditioned genital arousal in men) and our USs were more effective in inducing genital arousal. Our study was aimed at more than showing that women’s sexual arousal could be influenced by conditioning. We used the same experimental paradigm to examine the conditioning of genital arousal in both women and men. Photographs presented on videotape served as CSs and erotic film clips that had been rated as arousing by both men and women (Janssen, Carpenter, & Graham, 2003) served as the USs. Domjan and Hollis (1988) proposed that males might show conditioned sexual arousal more readily, and to a wider range of cues, than females. It has also been suggested that women’s sexual arousal 5 may not be as readily conditionable as men’s (Bancroft, 1989; Kinsey, Pomeroy, Martin, & Gebhard, 1953). However, Baumeister’s (2000) proposal that women are more erotically plastic suggests that they could be more sensitive to conditioning than men. Potential differences in propensity for sexual conditioning may involve gender differences in the effectiveness of various CSs and USs in the conditioning of arousal. In addition to examining gender differences in conditionabilty, we also explored the notion of biological preparedness (e.g., Dellarosa Cummins & Cummins, 1999; Mineka & Öhman, 2002; Seligman, 1970) in sexual conditioning, proposing that a sexually relevant CS (photograph of an abdomen of the opposite sex) would be more effective than a sexually irrelevant CS (photograph of a gun). Finally, assuming that subjects would be less likely to alter their expression of arousal if they did not realize they were being conditioned, we also varied the subjects’ awareness of CS presentation and in doing so their awareness of the CS-US contingency. CSs were presented either “subliminally” (i.e., for 30 m/sec followed immediately and hence backward masked by the film US) or “consciously” ( i.e., for 10 sec). When stimuli were presented outside the subjects’ awareness, both women and men showed conditioned genital arousal to the abdomen CS but not to the gun CS. These results are similar to those found by Öhman, Esteves, and Soares, (1995) using a fear conditioning paradigm, i.e., they found conditioned increases in skin conductance response to fear- relevant but not fear irrelevant stimuli that were presented outside the subject awareness and paired with a mild shock to the fingers. Even though our manipulation and measurement of awareness were rather crude, our results suggest a prepared link between sexually relevant stimuli and genital responses and support an independent role for 6 automatic processing in sexual responding consistent with some models of sexual arousal (Janssen, Everaerd, Spiering, & Janssen, 2000). When consciously perceived CSs were used however, men again showed conditioned increases in penile tumescence to the abdomen but not the gun CS, whereas women showed the opposite effect, i.e., conditioning to the gun but not the abdomen stimulus. The latter result was unexpected. Perhaps the gun-arousal associations in women may have been facilitated by increased attention (Beylin & Shors, 1998; Shors & Matzel, 1997) or excitation transfer (Hoon, Wincze, & Hoon, 1977; Meston & Gorzalka, 1995; 1996; Meston & Heiman, 1998) as women (but not men) showed increased skin conductance responses to the gun (but not the abdomen) CS. Small sample size in the target group prevented appropriate assessment of this hypothesis, but we intend to examine this issue in the future. Our study hinted at gender differences in the conditions under which sexual learning occurs, at least when consciously perceived CSs were employed. If fact, with both subliminally and consciously presented CSs, conditioning appeared stronger in women than men. However, the lack of a common physiological measure of arousal prevents a direct gender comparison. Moreover, gender differences in arousal patterns during conditioning could have accounted for the observed results. Men showed arousal responses to the CS prior to and independent of conditioning, whereas women did not. Hence the observed differences between women and men may have been due to differences in our ability to detect learning rather than due to a genuine gender difference in the strength of the CR. 7 In addition to replicating and expanding on the abovementioned findings, we have begun to examine individual differences in conditionability, as well as to use CSs from other sensory modalities. Individual differences. There are most likely various individual differences in classical conditionablity (e.g., Martin, 1997). Kvale, Psychol and Hugdahl (1994) found that autonomic (cardiovascular) reactivity is positively correlated with the susceptibility to learning a tone-noise association and to acquiring anticipatory nausea and/or vomiting in people receiving chemotherapy. Kantorowitz (1978) showed a significant correlation between extraversion and conditioning of pre-orgasmic sexual arousal and a significant correlation between introversion and post-orgasmic sexual arousal. In our study we found that conditionablity did not appear to be related to the amount of experience subjects had with erotic film, however there was not much variation among our participants on this measure. We also collected survey data from some of our subjects and correlated it with the strength of the CR. Specifically, we measured introversion/extraversion and we administered the Sexual Experience Scales (SES) subscale for Psychosexual Stimulation (Frenken, 1981) and the Sexual Inhibition Scales/Sexual Excitation Scales (SIS/SES) (Janssen, Vorst, Finn, & Bancroft, 2002). The former measures the extent that someone seeks sexual stimuli of an auditory-visual or imaginary kind and the latter measures sexual excitation (SE) or the propensity for sexual arousal and two forms of sexual inhibition (SIS-1 and SIS-2). SIS-1 is inhibition related to performance failure and SIS-2 is inhibition related to negative consequences. There were no clear relationships for men but for women the strength of the CR was inversely related to their scores on both inhibition scales but the correlations were not significant (p = .12, p = .13, respectively). This suggests that women 8 who are low in sexual inhibition may be more likely to show conditioned sexual arousal. However, what sexual inhibition means for women is unclear as the SIS/SES-female version that was used was adapted from research with men. Olfactory CSs. Olfactory cues play a large role in sexual arousal in animals, and odors have been used as effective CSs in the conditioning of sexual arousal in a variety of nonhuman species (Domjan & Holloway, 1998; Pfaus et al., 2001). While noxious odor stimuli have been used as USs to decrease sexual arousal in clinical settings (e.g., Colson, 1972; Earls & Castonguay, 1989; Junginger, 1997), olfactory stimuli have not been used as CSs in the conditioning of human sexual arousal. Studies indicate that smell plays a significant role in human sexual attraction. Herz and Cahill (1997) found that odor is an important guide for mate selection in women and men, and that women valued odor more so than men. Herz and Inzlicht (2002) showed that, for women, body odor was more important than looks (the reverse was true for men) and that, for women, smell was more valuable than all but one social factor (i.e., pleasantness). Because people report that smell is important in attraction and since the majority of fetishes are related to olfactory or tactile stimuli (Money, 1988), humans, and in particular women, may be likely to associate sexual arousal with odor cues. We are currently attempting classical conditioning of genital arousal using an olfactory CS. Discrete presentations of an odor stimulus (delivered via an olfactometer) were paired with erotic film clips as the US. A pilot study using only women found evidence for conditioned arousal to a strawberry odor in three of six subjects. It would be interesting to compare the relative effectiveness of an olfactory versus a visual CS in women and men. 9 The specifics of what is learned Classical conditioning is typically interpreted as learning of a predictive relationship in which the CS comes to signal the onset of the US, yet other types of learning can result from exposure to Pavlovian procedures. For example, even though conditioned taste aversion (CTA) learning is similar to other types of classically conditioned avoidances, a flavor cue that has been paired with a nausea-inducing agent not only comes to signal impending negative consequences but also itself becomes distasteful. Taste cues that predict the onset of shock or other cutaneous phenomenon result in avoidance but not acquired distaste (Pelchat, Grill, Rozin, & Jacobs, 1983; Pelchat & Rozin, 1982). For example, if a person becomes ill after eating something, they may become disgusted by the taste or smell of that food whereas if they experience an allergic reaction (e.g., breaking out in hives) after consuming that food, it typically does not become unpalatable. CTA learning appears to involve shifts in the hedonic value of the CS. Perhaps this also occurs in some instances in the conditioning of sexual arousal. Rozin, Wrzesniewski, and Byrnes (1998) proposed that the acquisition of fetishes may involve aspects of what is known in the human conditioning literature as evaluative conditioning (EC). Levey and Martin (1975) coined the term and described EC as an associative transfer of valence as a result of exposure to Pavlovian procedures. A common paradigm used in EC is pairing a picture of a “neutrally-rated” face (CS) with attractive or unattractive faces (USs) which results in a positive or negative shift in the evaluation or “liking” of the CS as assessed by verbal ratings. Most EC studies involve second order USs that are not biologically relevant (e.g., a picture of an attractive face, an unpleasant taste), however EC has been observed with a primary (shock) US (e.g., Hermans, Vansteenwegen, Crombez, 10 Baeyens, & Eelen, 2002). Most human conditioned arousal studies assess learning by changes in genital responding rather than by changes in self report. An exception is Letourneau and O’Donohue (1997) who assessed but did not find a change in subjective arousal ratings of the CS. However, this is not necessarily informative since their procedures did not produce conditioned genital arousal. Further, when using primary USs, a more indirect measure of EC (e.g., an affective priming task) is used to avoid demand characteristics (for more details see De Houwer, Thomas & Baeyens, 2001). The erotic photographs and films clips used as USs in conditioned arousal can be considered second order USs but they produce a stronger behavioral response than those typically used in EC. Hence it may be more appropriate to assess shifts in CS valence during sexual conditioning using an indirect measure. EC shares a number of properties with more conventional classical conditioning, but it is more resistant to extinction, not as sensitive to changes in CS-US contingency or to modulation (e.g., occasion setting) and can occur without awareness of the contingency (De Houwer et al., 2001). Some research, mainly in nonhumans, suggests that the conditioning of sexual arousal may show some characteristics of EC. In rats, Pfaus, Theberge, and Kippen (2003) found that an initially aversive odor can become appetitive after copulation with females scented with this odor, which suggests a hedonic shift in CS valence. Villarreal and Domjan (1998) found that male gerbils showed conditioned approach to an odor CS even though it was inconsistently paired with copulation, suggesting that learning in this situation may not have been particularly sensitive to contingency. In humans, the acquisition of a fetish appears to involve affective change. In laboratory studies, Langvin and Martin (1975) found some evidence that the strength of conditioned arousal in men did
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