Our understanding of the female sexual response emerges from an ongoing dialogue between mind and body. These conversations between mind and body play essential roles in mediating and disrupting sexual function. The classical assumptions that guided sexual science for many years is the idea that changes in genital physiology should directly reflect a woman’s subjective sexual desire and arousal. The foundations of these assumptions have slowly eroded as female sexuality researchers have used stronger study designs and more precise technologies to measure proxies of mind and body.

The scientific and clinical fallout has been enormous. These findings have lead to multiple revisions diagnostic criteria for sexual dysfunction, clinical guidelines for the management of sexual dysfunction, and even the very definitions of these constructs, desire and arousal. For example, this lack of knowledge inspired controversial changes in the DSM-5 criteria for sexual dysfunction related to desire, arousal, and pain. In response, serious ideological chasms have divided the field of female sex research.  This is not a theoretical exercise. These decisions determine the diagnostic coding of sexual dysfunctions used by insurance companies to cover treatment (or not). These decisions influence clinical phenotyping that is used to divide women into groups so that we can better understand the nature of these processes. These decisions impact how the FDA measures treatment efficacy as new pharmacological compounds are developed to treat female sexual dysfunction. These decisions influence how experts explain sexuality to women, and by extension, how women understand their own sexuality.

Our limited understanding of human sexual function has broad scientific consequences. The truth is that we lack sufficient knowledge of physiological changes that lead to and sustain desire, arousal, orgasm, and pain. Forty years of research has overwhelmingly focused on the early stages of sexual response: sexual desire (the subjective component of sexual response) and sexual arousal (the genital component of sexual response). The formal study of this subjective/genital relationship is female sexual psychophysiology. The goal of sexual psychophysiology research is to identify the emergent interactions between genital and subjective arousal, usually in response to visual, auditory, or olfactory stimuli that researchers have deemed sufficiently “erotic.” One of the biggest strengths of researchers in this subfield is that they have continually questioned their own theoretical and clinical assumptions along the way. Their interest lies in discovering what IS, not what SHOULD BE true about female sexuality. As a result, there as been an active resistance to the oversimplification of female sexuality. And to be fair, a large faction of clinicians and researchers argue that these studies have already reduced female sexuality to its biomechanical, socially prescribed parts.

 

Dimensional Sexuality

Sexuality is multi-dimensional. It includes:

  1. Sensations (the perception of pleasant sensory input);
  2. Meta-awareness of Sensations (embodied sensory pleasure);
  3. Psychology (cognitive/emotional processing of and preferences for erotic information);
  4. Memory (past experiences that have shaped sexual reward); and
  5. Motivated behaviors (decisions to act based on these sensory/cognitive states).

Given this complexity, we are faced with the questions: What is a biologically sound operational definition of sexual desire and arousal? How can these definitions be quantified? And how can we tell when these processes are deficient?

 

Historical Highlights of Sexual Science

Let’s begin with a concise overview of the history of the problem:

1.Frank Beach Defined Sexual Response in Mammals

Classic animal research described MALE SEXUAL BEHAVIOR using a simplistic pre/post framework that included pre-copulatory and consummatory sexual behavior.  Frank Beach’s observations of female mammals lead to an expansion of these concepts that differentiated phases of FEMALE SEXUAL BEHAVIOR:

(A) Attractivity, defined as the visual or olfactory cues that elicit sexual interest prior to physical contact;

(B) Proceptivity, defined as the physical approach behavior (i.e., increased motor activity) indicative of sexual interest such as hopping, darting, or paced mating; and

(C) Receptivity, defined as the behaviors associated with copulation (e.g., lordosis).

When these concepts are extrapolated to humans, sexual desire includes elements of attractivity and receptivity–identifying sexual features and approaching those features.  In other words, desire includes the internal sexual motivation that may (or may not) be externally expressed by approaching a potential mate. Sexual arousal may begin with attractivity, but it definitely plays a role in perceptivity and receptivity.

 

2. In the late 1960s and early 1970s, Masters and Johnson developed a theoretical model of Human Sexual Response that to this day remains the basis for medical education. Interestingly, this model began with sexual “excitement” (more akin to sexual arousal) and they did not explicitly acknowledge a role for sexual desire. Their approach has been criticized for its biomechanical focus (i.e., are all of the moving sexual parts functioning properly?). The Masters and Johnson model of female and male sexual response includes:

(A) Excitement, defined as genital arousal and awareness of genital arousal;

(B) Plateau, defined as a high level of sustained arousal;

(C) Orgasm, defined as an intense physiological and psychological trance-like state; and

(D) Refractory Period, which is a variable period of sexual satiety.

 

3. Helen Singer Kaplan added Desire to Masters & Johnson’s sexual response model in 1974, which formally introduced the idea thatinternal motivation (colored by perception, memory, and judgment) precedes physiological sexual arousal. However, she also suggested that sexual desire and arousal overlap over time, and this concept was emphasized in Rosemary Basson’s 2003 Circular Model of female sexual function. Basson referred to a lack of desire as “inhibited or hypoactive sexual desire.”

4.In the 1990s, John Bancroft suggested that sexual desire is a positive emotional state.

5.1990s-2000s: several psychophysiology studies examining correlations between subjective arousal to erotic films and concurrent genital arousal (measured via vaginal blood flow, an admittedly over-simplistic measure) consistently found variable or null correlations between vaginal blood flow and subjective perception of arousal. This finding has been replicated across several laboratories, with several measures of genital arousal. Essentially, women’s subjective feelings of desire/arousal are not linearly correlated with degree of genital response.

6.1999: Kim Wallen (a primatologist at Emory in Atlanta) published a paper describing that, although female macaques’ frequency of sexual behavior does not vary across the estrus cycle, the rate of female-initiated sexual activity peaks right before ovulation. This was important because it emphasized female initiation of sexual activity as a hormone-mediated index of sexual desire.

7.During this time, researchers at the Kinsey Institute posited a “Sexual Excitation/Inhibition” model of sexual functioning (again, not the most innovative idea). However, this concept did draw attention to the fact that certain classes of psychological stimuli can enhance or inhibit sexual arousal, and in women, a greater variety of concerns inhibit sexual desire/arousal (fear of pregnancy, lack of partner trust, body image issues, etc). This is the first official recognition of female selectivity, which is hypothesized by Trivers (1974): evolutionarily, greater parental investment in females will encourage greater selectivity of mates/mating contexts and would explain the significant impact of inhibitory factors on female sexuality.

8.In 2000, Rosemary Basson proposed a circular model of female sexual response, wherein desire is difficult to distinguish from sexual arousal because they build upon one another (she just formalized what Kaplan hypothesized, but Basson gets credit for this concept nowadays). What Basson highlights that is quite important is that sexual desire/arousal requires synergy between cognitive, emotional, and sensory processes, and a deficit in any one of these processes may disrupt and/or halt the entire process.

9.Cindy Meston and David Buss publish the book “Why Humans Have Sex,” which describes the enormous variability in motivations for sexual behavior.  Although I’m not crazy about Buss, I do respect some of his earlier work describing the many reasons why women have sex, which is very relevant—he notes that women may have sex to improve a relationship, to instrumentally attain a goal, to relieve stress, etc. His arguments remind me of female bonobos using sex to reduce social conflict when two males are fighting–they will essentially separate the males and mate with them to calm them down. So technically, instrumental use of sexuality is a manifestation of desire, as well…

10.In 2007, an important paper showed that women are subjectively and genitally aroused by erotic depictions of men, women, and primates, whereas men show sexual orientation-specific arousal (e.g., hetero men get aroused to hetero or female-on-female stimuli, gay men get aroused mostly by male-on-male stimuli). This popularized the concept of female sexual fluidity.

11.Between 2008 and 2012, testosterone became widely prescribed as an off-label treatment for low sexual desire in the United States. I personally believe testosterone’s aromatization to estrogen is likely the key to its clinical efficacy (synthetic estrogens may not be as effective), but the field was obsessed with testosterone as an important factor in female sexual desire.

12.In general, it becomes clear that desire may take on two meanings: incentive saliencewhen a new sexual stimulus is encountered (wanting), and motivation that reflects prior learning (liking).  The latter is more clinically relevant when the sexual stimulus is one’s partner after 5 years of cohabitation!

13.In 2014, my paper in mice revealed that tonic inflammatory pain induced in the mouse vulva, hindpaw, tail, and cheek equally reduced (but did not eradicate) female-paced sexual behavior. In contrast, males with pain in comparable locations were able to work through the pain and exhibited no change in sexual performance (!).  Interestingly, apomorphine, melanotan-II (a melanocortin receptor ¾ agonist), and gabapentin restored female sexual behavior. These findings suggest that amping up sexual motivation with pharmacological agents can overcome pain-induced inhibition of sexual behavior.

14.In 2015, the most recent revision of the DSM-5 officially combined sexual arousal and desire dysfunction—this formalizes their overlap and complicates ongoing efforts to study these constructs as distinct phenomena.

 

Men know when they are aroused. They have highly reliable visual indicators that tell them about their arousal. Women’s genitals are hidden from view. Religio-cultural beliefs do not encourage girls or young women to acknowledge or attend to their genitals, and young women learn that their monthly “curse” must be sanitized, hidden, and even suffered through if they experience painful menstrual cramps. Perhaps it comes as no surprise that there is little concordance between subjective and physiological sexual arousal.*  What does that mean? It means that female sexual arousal does not show predictable linear increases with progressively more intense sexual stimuli, as it does in men.  It means that women report varying levels of awareness of physiological sexual arousal, and this awareness appears to be unrelated to sexual functioning and sexual behavior (1).  This finding has been replicated using multiple technologies, study designs, analysis methods, across international laboratories. It means that women may approach sexual information in a very different way. As Ellen Laan so eloquently stated: “Thus a stimulus is not intrinsically sexual, it becomes sexual by its transformation…” (2)

So let’s break this process down.

Contemporary models of female sexual response describe an initial subjective shift from neutrality to sexual desire as a woman recognizes sexual stimuli in her environment (3). If a woman is aware of this perceptual shift, she may ask herself, “Is it appropriate to get aroused right now?” If a woman then decides it is safe and appropriate to focus on her sexual cues (note that safe and appropriate are absolutely relative!), a incremental increase in both arousal and desire will emerge (4). If a woman is unaware of this shift, her thoughts, emotions, and behaviors may be implicitly biased toward or against sexual cues, depending on her sexual history (5). Once desire and arousal begin to build to a perceivable level, they depend on attention to the sexual cue (“Sex…or laundry? Ugh I forgot to cancel my Amazon Prime membership…”) (6), positive appraisal of the sexual cue (“I wonder what those smiling lips could do…?”), the desire to approach this sexual cue (“Wheeeeere is my rabbit?”), degree of physiological arousal (7), and of course experiential engagement (8). Sexual desire encompasses the psychological and the behavioral aspects of this process, and sexual arousal consists of the body’s concurrent response and a woman’s subjective awareness of her body’s response to the sexual cue.

Yes, we are splitting hairs with this definition of sexual arousal. A woman may not be aware of increased vaginal lubrication, but she may perceive tingling or warm sensations. Consider Laan and Everaerd (2), who found that women’s cognitive appraisals of erotic stimuli predicted changes in subjective sexual arousal. In contrast, cognitive appraisal explain less variability in the degree of genital arousal. The implication is that a stimulus explicitly evaluated as “sexual” may evoke a genital response that doesn’t really influence a woman’s perception of her own sexual arousal.  Given that clinical relevance and efficacy is determined by patient-reported outcomes, a woman’s perception of her sexual arousal is more important than the arousal itself (9).

This is assuming that our measure of genital arousal is valid. Sexual psychophysiology research has capitalized on the use of effective erotic stimuli to maximize physiological arousal in laboratory analog settings. Erotic stimuli are judged to be effective if they produce corresponding increases in both physiological sexual arousal and self-reports of subjective arousal.  However, if physiological arousal does not imply the presence of subjective arousal, we are unable to progress to the next levels of scientific questioning.

 

* Footnote.

A large subset of women whose genital arousal tracks closely with their subjective perception, but we have yet to identify physiological differences to explain this. My interpretation of the data is that a strong learned component mediates the mind/body synchrony in women with high concordance (“Practice makes perfect!”).

 

 

 

 

 

 

 

 

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