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Review
. 2023 Nov 17:17:1285810.
doi: 10.3389/fnins.2023.1285810. eCollection 2023.

The elusive concept of sexual motivation: can it be anchored in the nervous system?

Elisa Ventura-Aquino #  1 , Anders Ågmo #  2
Affiliations
Review

The elusive concept of sexual motivation: can it be anchored in the nervous system?

Elisa Ventura-Aquino et al. Front Neurosci. .

Abstract

Sexual motivation is an abstract concept referring to the mechanisms determining the responsivity to sexually relevant stimuli. This responsivity determines the likelihood of producing a sexual response and the intensity of that response. Both responsivity to stimuli and the likelihood of making a response as well as the intensity of response are characteristics of an individual. Therefore, we need to assume that the concept of sexual motivation materializes in physiological mechanisms within the individual. The aim of the present communication is to analyze the requisites for the endeavor to materialize sexual motivation. The first requisite is to provide an operational definition, making the concept quantifiable. We show that parameters of copulatory behavior are inappropriate. We argue that the intensity of sexual approach behaviors provides the best estimate of sexual motivation in non-human animals, whereas the magnitude of genital responses is an exquisite indicator of human sexual motivation. Having assured how to quantify sexual motivation, we can then proceed to the search for physiological or neurobiological underpinnings. In fact, sexual motivation only manifests itself in animals exposed to appropriate amounts of gonadal hormones. In female rats, the estrogen receptor α in the ventrolateral part of the ventromedial nucleus of the hypothalamus is necessary for the expression of sexual approach behaviors. In male rats, androgen receptors within the medial preoptic area are crucial. Thus, in rats sexual motivation can be localized to specific brain structures, and even to specific cells within these structures. In humans, it is not even known if sexual motivation is materialized in the brain or in peripheral structures. Substantial efforts have been made to determine the relationship between the activity of neurotransmitters and the intensity of sexual motivation, particularly in rodents. The results of this effort have been meager. Likewise, efforts of finding drugs to stimulate sexual motivation, particularly in women complaining of low sexual desire, have produced dismal results. In sum, it appears that the abstract concept of sexual motivation can be reliably quantified, and the neurobiological bases can be described in non-human animals. In humans, objective quantification is feasible, but the neurobiological substrate remains enigmatic.

Keywords: brain; erection; operational definition; sexual approach; sexual motivation; vaginal lubrication.

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Conflict of interest statement

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

Figures

Figure 1
Figure 1
Schematic representation of the sequence of events during a sexual encounter according to the sexual incentive motivation model. For a detailed analysis of this model, see Ågmo and Laan (2023). The figure is reprinted from that paper under license CC BY.
Figure 2
Figure 2
Drawings of the procedures used to measure sexual motivation in the pioneering studies of the Meyerson group in Uppsala. For a detailed description, see Meyerson and Lindström (1973). Reprinted from Meyerson et al. (1973) with permission from Elsevier.
Figure 3
Figure 3
(A) Time (seconds) that male rats spent in the incentive zones in an experiment where either one incentive cage was empty and the other contained another male (Male) or one cage was empty and the other one contained a sexually receptive female (Receptive female). (B) Similar data from an experiment where the choices were either between an empty cage and an ovariectomized, nonreceptive female (Ovex female) or between an empty cage and a receptive female (Receptive female). XXXDifferent from the empty cage, p < 0.001; ++Different from the time spent in the male incentive zone in the test with empty cage—another male, p < 0.01; +Different from the time spent in the ovariectomized female incentive zone in the test with empty cage—ovariectomized female, p < 0.05. Modified from Ågmo et al. (2004), with permission from Elsevier.
Figure 4
Figure 4
Preference score (A) and time (in seconds) spent in the vicinity of a social incentive (another male rat) and in the vicinity of a sexual incentive (sexually receptive female) (B) in a group of intact male rats (Intact), a group of males that had been castrated for at least 30 days (castrated) and a group of castrated males implanted with a testosterone-containing Silastic® capsule 20 days before the test. There were 12 males per group. Statistics: Main effect of treatment on the preference score, F(2,33) = 10.691, p < 0.001. Main effect of treatment on the time spent with the incentives, F(2,33) = 3.878, p = 0.031. Main effect of incentive, F(1,33) = 44.419, p < 0.001; interaction incentive × treatment, F(2,33) = 12.400, p < 0.001. ***Different from the female, p < 0.001, ++different from the castrated group, p < 0.01, +++p < 0.001. The preference score (C) and the time spent in the vicinity of either a castrated or an intact male (D) obtained in ovariectomized females treated with varying doses of estradiol benzoate + progesterone. N = 16. Statistics: Main effect of estradiol dose on the preference score, F(3,45) = 3.511, p = 0.023. Main effect of dose on time spent with the incentives, F(3,45) = 2.800, NS; Main effect of incentive, F(1,15) = 12.390, p < 0.01; interaction dose x incentive, F(3,45) = 3.274, p < 0.05. Hormone treatment did not affect the time spent with the castrated male, whereas the time spent with the intact male was dose-dependently increased. *Different from the vehicle, p < 0.05; **p < 0.01; +Different from castrated male, p < 0.05; ++p < 0.01, +++p < 0.001. Data are mean ± S.E.M. The male data come from Attila et al. (2010) and the female data from Spiteri and Ågmo (2006). Procedural details are found in these papers.
Figure 5
Figure 5
(A) Time (seconds) that male rats spent in the incentive zones either without preceding sexual activity (Unmated) or after copulating for 4 h (Exhausted). Data are mean ± S.E.M. *Different from intact male, p < 0.05; +Different from unmated, p < 0.05, ++p < 0.01, and +++p < 0.001. (B) Time (seconds) that female rats spent in the incentive zones either without preceding sexual activity (Unmated) or after having received three ejaculations in a standard mating test (Mated). Data area mean ± S.E.M. **Different from the castrated male, p < 0.01; ++Different from the time spent in the intact male incentive zone when unmated, p < 0.01. Modified from Ågmo et al. (2004), with permission from Elsevier.
Figure 6
Figure 6
Hypothetical relationships between the activity of the sexual central motive state and the genital response. (A) There is a linear relationship. (B) The relationship is curvilinear.
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