Commentary: “Hearing, touching, and multisensory integration during mate choice” – Sex, Drugs and Leather Jackets

A Commentary on

Hearing, touching, and multisensory integration during mate choice

by Lenschow, C., Mendes, A. R. P., and Lima, S. Q. (2022). Front. Neural Circuits 16:943888. doi: 10.3389/fncir.2022.943888

Introduction

Lenschow et al. (2022) reviewed the recent findings related to the literature on hearing and touching in partner/mate choice/preference in animal models, as well as the multisensory integration circuits in this phenomenon. Their review covered evidence from rats, mice, and humans, while distinguishing groups by sex and evaluating the contribution of vocalizations and somatization during premating, mating, and post-mating choice, to further analyze the synergistic action of multisensory cues in this phenomenon.

The authors carried out great work describing, organizing, and discussing the available research, providing a wide breadth of the literature. They also acknowledge being unable to include all relevant studies due to space constraints. Therefore, in light of this limitation, the following commentary will provide essential missing pieces of evidence regarding the manipulation of somatosensory cues in partner/mate preference/choice, and will discuss the role of opioids in this phenomenon.

Animal evidence on somatosensory cues in partner/mate preference/choice

Domjan et al. were perhaps the first to demonstrate experimentally that animals can develop sexual fetishes. They trained Japanese quail males to associate an inanimate taxidermy quail female before copulation with a sexually receptive partner (SRP). In the “fading” group, the taxidermic female was gradually covered with terrycloth, to be fully covered leaving no quail features at the last trial of training. In the “non-fading” group, the taxidermic female was always presented fully covered. At the test session, males were presented only with the fully covered taxidermic female. Males in the fading group spent more time around the taxidermic female and displayed more copulatory behaviors toward it (e.g., grabs, mounts, and cloacal contacts) than those in the non-fading group (Domjan et al., 1992). They also showed persistence of copulation with a taxidermic female even after 20 trials of extinction, but this was not reflected when using light as a conditioned stimulus, nor when food was used as an unconditional stimulus instead of an SRP female quail (Köksal et al., 2004). Interestingly, considering that an important part of partner/mate preference/choice is undeniably related to reproduction, when given the opportunity to copulate with a real SRP, quail males who copulated with the taxidermic female fertilized a greater proportion of eggs than control males (Cetinkaya and Domjan, 2006).

Quintana et al., moreover, demonstrated that a somatosensory cue can be used as a conditioned stimulus to drive partner/mate preference/choice in male and female rats. Quintana et al. (2019b) found that animals were able to copulate with SRP wearing a rodent jacket for 14 training trials and they were later tested in an open field for their preference, using two random SRP, one with the jacket on and the other with the jacket off. Males who copulated with females wearing jackets showed a preference toward jacketed partners, whereas females only showed a mate/partner preference/choice when the jacket was associated with SRP during the training, and its absence indicated sexually non-receptive partners. Previous research has consistently demonstrated that these rewarding associations are mainly the product of opioid transmission in several brain areas (Pfaus et al., 2012). Thus, a follow-up study (Quintana et al., 2019c) used a similar training strategy, but male rats were either injected with naloxone, an opioid antagonist, or a saline solution before each trial. During the same preference test, while injecting saline into both groups, they found that males injected with saline during training displayed a preference toward jacketed females, whereas males injected with naloxone displayed a preference for unjacketed females. Among the many brain areas where opioids are known to facilitate a conditioned partner/mate preference/choice, two major brain hubs are the medial preoptic (mPOA) and ventral tegmental areas (VTAs; Pfaus, 2009; Georgiadis et al., 2012). Quintana et al. (2019a) found that when they microinjected naloxone into the mPOA of males trained to associate the jacket with SRP, their partner/mate preference/choice shifted toward unjacketed females, whereas microinjections of naloxone into the VTA only abolished that preference. Subsequent detection of c-Fos protein induced by the jacket showed that, relative to the control group, microinjections of naloxone into the mPOA suppressed c-Fos in both the mPOA and VTA, whereas microinjections of naloxone into the VTA suppressed c-Fos only in the VTA. These findings demonstrate that for a partner/mate preference/choice, a somatosensory cue works as a conditioned stimulus just like when using cues from other sensory modalities (e.g., olfactory; Pfaus et al., 2012), likely through similar neural pathways.

It has also been shown that a somatosensory cue can modulate sexual arousal and behaviors in those who wear a fetish cue. Pfaus et al. (2013) gave males, either wearing or not wearing a jacket, several copulatory experiences with SRP. During the test, half of the males wore the jacket, whereas the others did not. Those who did not wear a jacket during training or the test copulated normally, as did those who wore a jacket during training and the test, and those who did not wear the jacket during training but were tested with it. However, males who wore the jacket during training but not during the test made significantly fewer anticipatory level changes, had fewer longer mount, intromission, ejaculatory latencies, and ejaculated significantly less. Similar results were found when males were trained to associate wearing the jacket with sexually non-receptive females, and then tested while wearing the jacket.

Discussion

While it is undeniable that animals copulate to reproduce, there have been numerous reports of animals of different species copulating with different objects, fetishes, or not-sexual targets (Young, 1949; Beach, 1950; Barraud, 1953; Ficken and Dilger, 1960). Indeed, partner/mate preference/choice is known to be fostered through opioid transmission responsible for sexual pleasure and reward, which in turn sensitizes dopamine, oxytocin, and vasopressin systems responsible for attention, arousal, and bonding, along with the learned experience that ultimately determines not only who but also what is sexually attractive and arousing (Quintana et al., 2022). The same mechanisms are also used to predict why humans deviate from the reproductive aspects of this phenomenon (Pfaus et al., 2020).

Author contributions

The author confirms being the sole contributor of this work and has approved it for publication.

Conflict of interest

The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher's note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

References

Barraud, E. M. (1953). Sexual behavior occurring as overflow activity in juvenile house sparrow. Br. Birds 46, 382.

Beach, F. A. (1950). Sexual behavior in animals and man. Harvey Lect. 43, 259–279.

Cetinkaya, H., and Domjan, M. (2006). Sexual fetishism in a quail (Coturnix japonica) model system: test of reproductive success. J. Comparat. Psychol. 120, 427–432. doi: 10.1037/0735-7036.120.4.427

Domjan, M., Huber-McDonald, M., and Holloway, K. S. (1992). Conditioning copulatory behavior to an artificial object: efficacy of stimulus fading. Anim. Learn. Behav. 20, 350–362. doi: 10.3758/BF03197958

Ficken, M. S., and Dilger, W. C. (1960). Comments on redirection with examples of avian copulations with substitute objects. Anim. Behav. 8, 219–222. doi: 10.1016/0003-3472(60)90030-0

Georgiadis, J. R., Kringelbach, M. L., and Pfaus, J. G. (2012). Sex for fun: a synthesis of human and animal neurobiology. Nat. Rev. Urol. 9, 486–498. doi: 10.1038/nrurol.2012.151

Köksal, F., Domjan, M., Kurt, A., Sertel, O., Orüng, S., Bowers, R., et al. (2004). An animal model of fetishism. Behav. Res. Ther. 42, 1421–1434. doi: 10.1016/j.brat.2003.10.001

Lenschow, C., Mendes, A. R. P., and Lima, S. Q. (2022). Hearing, touching, and multisensory integration during mate choice. Front. Neural Circuits 16, 943888. doi: 10.3389/fncir.2022.943888

Pfaus, J. G. (2009). Pathways of sexual desire. J. Sex Med. 6, 1506–1533. doi: 10.1111/j.1743-6109.2009.01309.x

Pfaus, J. G., Erickson, K. A., and Talianakis, S. (2013). Somatosensory conditioning of sexual arousal and copulatory behavior in the male rat: a model of fetish development. Physiol. Behav. 122, 1–7. doi: 10.1016/j.physbeh.2013.08.005

Pfaus, J. G., Kippin, T. E., Coria-Avila, G. A., Gelez, H., Afonso, V. M., Ismail, N., et al. (2012). Who, what, where, when (and maybe even why)? How the experience of sexual reward connects sexual desire, preference, and performance. Arch. Sex Behav. 41, 31–62. doi: 10.1007/s10508-012-9935-5

Pfaus, J. G., Quintana, G. R., Mac Cionnaith, C. E., Gerson, C. A., Dubé, S., and Coria-Avila, G. A. (2020). Conditioning of sexual interests and paraphilias in humans is difficult to see, virtually impossible to test, and probably exactly how it happens: a comment on Hsu and Bailey (2020). Archiv. Sex. Behav. 49, 1403–1407. doi: 10.1007/s10508-020-01739-2

Quintana, G. R., Birrel, M., Marceau, S., Kalantari, N., Bowden, J., Bachoura, Y., et al. (2019a). Differential disruption of conditioned ejaculatory preference in the male rat based on different sensory modalities by micro-infusions of naloxone to the medial preoptic area or ventral tegmental area. Psychopharmacology 236, 3613–3623. doi: 10.1007/s00213-019-05334-9

Quintana, G. R., Desbiens, S., Marceau, S., Kalantari, N., Bowden, J., and Pfaus, J. G. (2019b). Conditioned partner preference in male and female rats for a somatosensory cue. Behav. Neurosci. 133, 188–197. doi: 10.1037/bne0000300

Quintana, G. R., González, B., Borduas, E., Lemay, V., Yarur, F., and Pfaus, J. G. (2019c). Naloxone disrupts the development of a conditioned ejaculatory preference based on a somatosensory cue in male rats. Behav. Neurosci. 133, 198–202. doi: 10.1037/bne0000302

Quintana, G. R., Mac Cionnaith, C. E., and Pfaus, J. G. (2022). Behavioral, neural, and molecular mechanisms of conditioned mate preference: the role of opioids and first experiences of sexual reward. Int. J. Mol. Sci. 23, 168928. doi: 10.3390/ijms23168928

Young, H. (1949). Atypical copulatory behavior ofa robin. Auk 66, 94. doi: 10.2307/4080696