To the best of our knowledge, the present study is the first to empirically evaluate how lifelong PE patients respond to the anticipation and hedonic experience of sexual rewards in comparison to non-sexual rewards. Regarding reward anticipation, this study revealed that compared to HCs, lifelong PE patients exhibited significantly faster RTs to erotic cues than to monetary cues. Regarding hedonic experience ratings after obtaining the actual reward, only lifelong PE patients rated erotic rewards as more pleasant than monetary rewards. These results imply that lifelong PE patients process erotic rewards differently from healthy controls. As such, the findings of this study may provide an insightful clue regarding how PE patients respond to the rewarding properties of sexual behavior and consequently shed light on the etiology of PE.
As pointed out above, reward-predicting cues are associated with incentive motivational processes 23–26. Such incentive motivational properties of reward-related cues can serve to promote an approach toward and consumption of rewards and thus may bias behavioral choices toward potentially rewarding events. In this sense, our observation that lifelong PE patients exhibited significantly faster RTs to erotic cues than to monetary cues implies an increase in incentive motivation to pursue erotic rewards compared to monetary rewards among them. Such hypersensitivity to erotic reward-predicting cues can in turn lead to excessive attribution of incentive salience to erotic reward-related representations, causing pathological ‘wanting’ to obtain erotic rewards.Sexual behavior is generally considered pleasurable and rewarding. It is not surprising hence that brain areas implicated in rewards are elicited when individuals anticipate such rewards. A wealth of evidence supports the notion that the connection of the ventral pallidum (VP) with the ventral striatum (VS), including the nucleus accumbens (NAcc), forms a subcortical neurocircuitry mediating incentive motivation elicited by reward-predicting cues 24, 26. We suggest that the enhancing effect of PE on incentive motivation may arise from enhanced responsiveness of the VS-related motivational neurocircuitry toward erotic cues in lifelong PE patients. Considering that this subcortical incentive-motivational neurocircuitry is an important component of the mesolimbic dopamine system in humans 30, we further postulate that these findings may reflect that dopaminergic (DA) hyperactivity is involved in PE. In this respect, our findings add to a growing literature supporting the argument that alterations in dopaminergic control of ejaculation may be an aetiological factor contributing to ejaculatory dysfunction including PE 31. However, the majority of previous studies in animals and humans focus on the possible role of dopaminergic receptors or the dopamine transporter gene (DAT1) polymorphism and PE 31, 32. Here, our observation during reward anticipation in lifelong PE patients seems to provide indirect evidence in support of the argument that the dysfunctional nigrostriatal dopamine pathway plays a special role in ejaculatory dysfunction including PE 31, although this needs to be confirmed in studies that test this hypothesis directly. Meanwhile, excessive attribution of incentive salience to erotic reward-related representations may confer hypersensitivity to hedonic value of erotic rewards in lifelong PE patients. Our findings indeed support this argument by showing that PE can also enhance the hedonic impact of obtained erotic rewards. For the hedonic experience of actual rewards, we found that erotic rewards were rated as more pleasant than monetary rewards only in lifelong PE patients, thereby suggesting that lifelong PE patients exhibited increased hedonic drives to erotic rewards compared to monetary rewards. From this, it seems rather likely that lifelong PE patients may have allostatic changes in the hedonic set-point for erotic rewards and thus, attribute higher reward values to such rewards. Similar to our observation of the enhanced incentive motivational processes elicited by erotic cues in lifelong PE patients, we would assume that the enhanced hedonic impact of obtained erotic rewards by PE patients may possibly reflect heightened responsiveness of the hedonic neurocircuitry that is implicated in subjective hedonic processing in humans. The prefrontal cortex mainly including the orbitofrontal cortex (OFC) is found to be central to the hedonic neurocircuitry, which is also a key component of the mesolimbic dopamine system in humans 33. In this sense, it seems to be rational to speculate that PE can also enhance the hedonic impact of obtained erotic rewards, possibly via effects on the hedonic circuit of the mesolimbic dopamine system. Taken together, lifelong PE patients exhibited an allostatic shift in both the incentive motivational process and the hedonic/pleasure process of erotic reward processing. Given that hypersensitivity to reward has been argued to be one of two independent dimensions of impulsivity 34, these findings likely reflect a changing balance in cognitive control capacities versus rewarding properties of sexual behavior in lifelong PE patients. Hence, excessive rewarding properties of sexual behavior may override cognitive control capacities in PE, which has recently been claimed to be a core mechanism underlying the aetiologies of PE 35. In this sense, our findings may reveal new perspectives on the treatment options for PE. Future therapies for PE may include electrical stimulation or drugs that can interfere with incentive motivation and the hedonic experience of rewarding properties of sexual behaviors.
Finally, it is noted that behavioral measures of responses to standardized psychological tasks may provide a distinct, yet complementary approach to comprehensively evaluating the psychological functions of PE patients, when considering that self-report and behavioral measures have recently been claimed to tap very different response processes36. For this reason, this complementary approach may help to deepen the insight into the etiology of PE. Despite encouragement, it has not been until recently that researchers have begun to contribute to this understudied area of research. For example, a recent study provided an important clue into characterizing social cognitions in PE patients by showing a deficit in affective Theory of Mind (ToM) abilities of lifelong PE patients using an emotional intention recognition task 37. This highlights a need to further advance our knowledge of the underlying psychopathologies of PE through this complementary approach.
Limitations
In spite of our interesting findings, the present study includes limitations that warrant mention. First, the present study only included patients suffering from lifelong PE. Given that PE is a heterogeneous and multifactorial condition and the difference between PE subtypes has been increasingly highlighted 19, 38, 39, this may affect the “generalizability” of our results to PE patients in general. Future research should aim at characterizing how different subforms of this condition respond to rewarding properties of sexual behavior. Second, given that the present study focused on the Incentive Delay Task which is a frequent measurement of reward processing, it is an open question to what extent the present results can be generalized into other types of paradigms measuring reward processing. As a consequence, it is necessary to incorporate different paradigms to better characterize how PE impacts the regulation of the rewarding aspect of sexual behavior in future studies. Despite these limitations, we believe that our findings open up the possibility to gain further insights into functional characteristics and pathological signatures underlying sexual reward processing in PE patients.