The following page deals with some micropsychological aspects of human sexuality. It is a pre-print of a paper published in: Med Hypotheses 76 (2010) 384-387 D.O.I. 10.1016/j.mehy.2010.10.048

The Roots of Sexual Arousal and Sexual Orientation

Yehuda Salu, Ph.D.

Department of Physics and Astronomy, Howard University, 2235 6^th Street NW, Washington, DC 20059.  202-806-6025, fax: 202-806-5830, ysalu@howard.edu

Abstract

Unlike members of other species that are genetically wired to be attracted to their sexual partners, humans learn the cues that guide them in choosing their sexual partners and that trigger sexual arousal. Genetically wired mechanisms must be directing the acquisition of those cues and organizing them in information structures that underlie human sexual behavior. Individual sexuality is a combination of the genetic mechanisms and information learned through personal experiences. This article focuses on the roots of human sexuality –on genetically embedded mechanisms, common to all humans, around which the wide variety of sexual behaviors is built. It proposes a model that defines the basic mechanisms and their role in developing individual sexuality. It is suggested that three brain areas host the root of human sexuality: the auditory area, which provides stimuli that serve as cues for the identification of a mate; an emotional area, which provides cues for emotional arousal; and a corporal area, which controls the physiological expressions of arousal. The amygdala is a main candidate for the emotional area, and the hypothalamus for the corporal area, but other areas may also provide those inputs. Experimental observations that support this model are discussed, and an outline of additional experiments for validating the model is proposed. If validated, the model would provide knowledge that fills a gap in the understanding of human sexuality –knowledge that would benefit individuals, the medical profession, and society as a whole.

Introduction

Throughout their lives, individuals develop their behavioral and emotional patterns from roots that are genetically embedded in their brains. This article proposes a theory about the roots of sexual orientation and arousal, and outlines how innate learning mechanisms and individual experiences expand those roots to create the wide spectrum of human sexual emotions and behaviors.

At puberty, many people discover that their sexuality has emerged, without them even noticing how it was evolving. Asexual experiences during childhood have been processes by the brain and formed the adult sexual phenotype. This article focuses on pre-pubertal developmental mechanisms. The same general mechanisms continue also after puberty, but by then, additional factors, which depend on the mature sexual system, affect the outcome.

The sexual system of the newborn consists of “hardware” and “software”. The hardware is the immature sex organs, and the software is the immature brain programs that activate that hardware. Both parts evolve with time and experience, and at puberty the entire system becomes functional. Although it is not known how the software is encoded, it is apparently realized as synaptic weights between neurons that form neural networks. Neural networks process external stimuli and activate the physiological and mental components of the sexual system.

Classical conditioning is one of the innate mechanisms that the brain uses for acquiring and recording information in its neural networks. Three factors participate in classical conditioning (e.g. Pavlov's experiment): the unconditioned stimulus US(taste of food), the unconditioned response UR (salivation), and the conditioned stimulus CS (bell's ring). The unconditioned stimulus US and its response UR are already a part of the brain's information system.  Then, the unconditioned stimulusUS triggers the unconditioned response UR in the presence of the conditioned stimulus CS. After the learning is complete, the CS too becomes a trigger of the UR. The UR is now called the conditioned response CR of the CS.

A CS that has become associated with an UR through conditioning may serve as theUS in a subsequent conditioning. For example, a whistle that has become associated by conditioning with the feeling of reward, can serve as the US in subsequent training of a dog, and associate other behaviors and stimuli with feeling rewarded. That is how root associations can be expanded to general behavior repertoires.

Classical conditioning is ubiquitous, and it ought to be genetic. It has been demonstrated that human adults can learn new sexual arousal cues by conditioning (1). Conditioning probably underlies the development of the software of the sexual system. Therefore, the innate sexual US's and UR's are the root of human sexuality; they determine the sexuality of the individual. Unlike in Pavlov’s experiments, the innate sexual US's and UR's are not so self-evident. The sexual system is not functional at infancy. Its software and hardware develop during many years of personal experiences, till they mature at puberty. In adults, both root and conditioned stimuli commingle in triggering sexual behaviors. The purpose of this paper is to identify the root US's around which human sexuality develops.

The software of the sexual activities that the brain uses consists of input and output routines. They control the sexual activities and coordinate them with the external circumstances. The input routines, which are the focus of this article, determine the sexual orientation and what arouses a person.

Many attempts have been made to identify the US's that serve as the input cues to the root sexual orientation routines.

Chemical compounds whose production in men is different than in women were found, and if ingested they affect sexual behavior (2,3). However, it has not been demonstrated that humans naturally use those compounds, or in general, that humans depend on pheromones or olfactory signals to identify a mate or to get aroused (4).

Breast feeding apparently does not provide the root stimuli around which sexual orientation is built; the distribution of sexual orientations among adults who were breast-fed does not seem different from that of formula-fed people.

Differences in the appearance of men and women, such as chest shape and facial hair, are affected by clothing and other social norms that may vary with time and location, so they cannot provide a universal root US's for sexual orientation.

Studies of the correlations between the sexual orientations of parents and the sexual identities of their children suggest that, in general, the sexual orientation of the parents is not a major factor that affects the sexual identities of their children (5,6). However, more studies of larger populations and of a wider variety of parental compositions are needed in order to sort out cause-effect relationships.

There are pre- and post-natal differences between the hormonal profiles of females and males. These differences are responsible for the development of the sex organs and for general gender-characteristic behaviors, but they do not seem to determine sexual orientation (7-10).

Several morphological and functional brain differences between the sexes have been observed (11), but their roles in sexual activities need clarification.

In homosexual men (HoM), the size of the suprachiasmatic nucleus is twice the size that it is in HeM, and this difference may be attributed to pre-natal hormonal differences.(12,13).

HoM, like HeW, have a smaller area in the frontal part of the hypothalamus (the INAH-3) than do HeM (14).

The anterior commissure of HoM is larger than that of HeM. This structure, which is larger in women than in men, connects the left and right temporal cortexes and is thus involved in sex differences related to cognitive abilities and language (15).

The hypothalamus of HoM, is not as responsive to a classic antidepressant (fluoxetine) as that of HeM, which points to a difference in the activity of the serotonergic system (16).

The progesterone derivative 4,16-androstadien-3-one (AND), whose concentration in men’s sweat is approximately 10 time greater than in women’s, and the estrogen-like steroid estra-1,3,5(10),16-tetraen-3-ol (EST), which was detected in women’s urine, elicited different responses, concurrent with sexual orientation, in the hypothalamus of HeW and HoM, but not it HeM. (2) and in HoW’s and HeW (3).

Brain areas that are activated during sexual stimulation have been mapped, using non-invasive methods. Numerous studied (17) use fMRI and PET scans. Others use electrical evoked potential, and some used MEG (18). A general experimental paradigm is comparing and contrasting activations that were triggered by sexual stimuli with activations of asexual stimuli or with a quiet baseline. Videos and still pictures are common visual stimuli in such experiments. The Achilles heel of visual stimulation is the multitude of factors that are involved in the experiments and the subjectivity of some of the criteria. Brain areas that handle cognitive, emotional, motivational and physiological information participate in the process in both men and women, including the thalamus, amygdala, inferior frontal lobe, orbital prefrontal cortex, medial prefrontal cortex, cingulate cortex, insula, corpus callossum, inferior temporal lobe, fusiform gyrus, occipitotemporal lobe, striatum, caudate, and globus pallidus (17). The level of activation of some of the areas depends on hormone levels, which vary with time and subject (19). The stimuli vary from one experiment to another, and the appraisal of the specific features that cause the arousal may be subjective (20). Overall, it is difficult to establish cause-effect sequences from these experiments. Nevertheless, it has been established that the ways that the brain processes sexual information varies according to the sex and the sexual orientation of the person. Some areas, such as the hypothalamus and the amygdala, appear to be more central to the processes than others (17). Areas associated with reward, such as the ventral striatum and centromedian thalamus, also responded in accordance with the sexual orientation of the person (21).

The Model

The root of sexual orientation

In many species, pheromones drive sexual attraction. In one mode of operation, a female releases a pheromone, and a male detects it. That triggers a sequence of activities in the male that leads him to the female. All this is possible because the releasing organs of the female and the detecting organs of the male are genetically designed to work together. In analogy, in order to uncover the roots of human sexual orientation, it is needed to identify a genetic human system that emits signals that depend on the sex of the emitter, and a receiving system that responds to those signals according to the sex of the receiver.

The auditory system fits these specifications. The voice of men is distinct from the voice of women, and this distinction is easily detected by the auditory system. Voice is one of the most reliable cues that humans use in order to recognize the sex of the speaker. Voice is a genetic, robust, universal cue that is not susceptible to surrounding factors. Therefore, it is suggested that voice is the enigmatic root US, around which sexual orientation is built by conditioning.

In a boy that will become a heterosexual men (HeM), the innate receiving sexual routine is genetically tuned to respond to women's voice. When the boy hears a woman’s voice, features of that woman are conditioned and become cues of the boy’s immature sexual-attraction-center. After puberty, these cues will trigger in this HeM sexual attraction to women. Similarly, in HeW, the voice detectors are tuned to men’s voice, in HoM they are tuned to men’s voice, in HoW they are tuned to women’s voice, and in BiW and BiM they are tuned to the voices of both men and women.

Evolvement of arousal cues

Identifying a potential mate of the desired sex is one goal of the sexual software. Another goal is triggering arousal towards that mate. The arousal software generates emotions that help trigger the physiological expressions of sexual arousal. It is plausible that the root arousal software, around which the mature software is built, deals with genetic emotions.

Fear is a genetic innate emotion that participates as the US and the UR in conditioning. It is the activated state of its default opposite, feeling safe. These two opposites can happen simultaneously, and when they do, an overall feeling of arousal may result. For example, fear and feeling-safe get mixed in a roller-coaster ride. The result is a kind of arousal. When watching a favorite team playing a close match, the fear of losing and the feeling of personal safety create a state of arousal. Such arousal feelings are different from pure fear and from pure safety. It has been suggested (22) that a combination of two feelings: fear of another person and, at the same time, feeling safe is a root of sexual arousal. This combination is called SWAP, for Safe With Another Person. In children, whose sexual system is still immature, feeling SWAP activates conditioning processes that acquire sexual arousal cues in asexual situations. For example, a child that is scared of a stranger clings to her mother’s leg. Features of the situation, such as touching a leg, become cues of SWAP. After puberty, in synergy with sexual orientation cues and in the appropriate ambiance and state of mind, touching the leg of her partner would trigger her sexual arousal.

Although feeling SWAP appears to be a root US of sexual arousal, it may, but it does not have to actually cause all adult arousals. This is a general property of all cues that serve as root US’s in conditioning. For example, a dog that due to conditioning feels rewarded by various stimuli, will still feel rewarded by food, the root US that was used in the training. Also, after puberty, physical erotic pleasures become operational, and they can serve as US's for learning arousal cues. Those cues do not have to depend on feeling SWAP. For example, a fragrance that one of the partners wears may become an arousal cue, due to its association with experienced sexual pleasures.

Prevalence of SWAP                                       

The role of feeling SWAP in acquiring and in triggering arousal is elucidated by analyzing common observed behaviors and testimonials.

Starting at about three years of age, it is common for children to be apprehensive of becoming friends, or even associating with children of the opposite sex. At the same time, they feel safe with friends of their own sex. In fewer cases, children prefer associating with the opposite sex and avoid their own. It is possible that those SWAP feelings trigger conditioning of cues of sexual arousal and orientation in asexual interactions. Those cues could become part of the adult’s sexual repertoire. The same emotional tension between the need to feel safe with a partner and the concern of being rejected is a common ingredient of sexual arousal also in the adult. The acquisition of those cues is usually influenced also by explicit and implicit social interventions.

In general, there are two strategies for creating safety feelings in situations of feeling threatened by another person. One is taking control over that person. The other is surrendering. Both strategies create a feeling of safety in the presence of fear, which is SWAP. The theme of controlling a partner or being controlled, which generates the feeling of SWAP, which creates arousal, is common in a wide spectrum of sexual interactions. In “milk-and-honey” interactions, body-language messages, such as sexual positions, is one way of enacting that theme. In “off-the-main-stream” interactions, it is expressed in games of dominance, submission and sadomasochism. Those arousing games are played with the consent of the players and do not interfere with their wellbeing. In paraphilia, those emotions take over the perpetrators and interfere with their wellbeing and with the rights and wellbeing of others (23,24). In dysfunctional situations, other emotions, such as guilt and shame, which have traits of fear in them, interfere with the creation of SWAP and muffle the arousal.

The Loci

The roots of sexual arousal and orientation reside in inter-related brain areas that handle three kinds of information: sensory, emotional, and corporal. According to the proposed model, the auditory system is a main provider of sensory stimuli that identify the sex of a potential partner. The amygdala and the hypothalamus are two of the centers that are involved in generating the characteristic feelings and in triggering the bodily responses of sexual activity (25, 26). The details of the innate connectivity between those three areas determine the root US’s and UR’s around which individual sexuality is developed. The first developmental stage occurs from childhood to puberty, and it relies on asexual individual experiences. During this period, asexual cues that are typical to the child’s surroundings are collected and assembled in information structures that will serve as sexual cues for the adult. Different innate connectivity patterns between those brain areas cause different mature sexual orientations. After puberty, centers that are directly related to sexual activity and pleasure join in and provide additional US’s and UR’s around which individual sexuality continues to develop.

Feasibility of the Model

Several observations support the feasibility of the model. The basilar membrane creates a tonotopical representation of the incoming sound. High pitch components cause stronger vibrations at the narrow end of the membrane. As the frequency of the sound decreases, the stronger vibrations shift towards the wide end of the membrane. Hair cells translate the vibrations of the membrane into electrical signals that propagate to the brain. The auditory tract and parts of the auditory cortex are also organized tonotopically (27). Thus, various brain areas receive information about the spectrum of the sound, and this information could be used for identifying the sex of a speaker.

The inner ear shows sexual dimorphism. The cochleae of human females are 8-13% shorter than those of males (28). Otoacoustic emission (OAE) is sound generated by the cochlea in response to external sound. It enhances features if the incoming sound. It was found that there are sex differences in OAE even in newborns, and that in adult women there is a correlation between such differences and sexual orientation (28).

Auditory evoked potentials, which are presumed to correspond to populations of neurons from the auditory nerve through auditory cortex, showed differences in mean latency or amplitude that correlate with sex and with sexual orientation of women (29).

According to the model, an amygdala, a hypothalamus, or any area of a similar role that is innervated heavier by high-pitch neurons would respond stronger to women. Areas that are innervated heavier by low pitch neurons would respond stronger to men. Such connectivity dimorphism may be created by pre- and post-natal genetic and hormonal factors that regulate neurogenesis, cell migration, cell differentiation, cell death, axon guidance and synapsogenesis. Sex differences in cell positions in the developing pre-optic area and the hypothalamus suggest that cell migration may be one target for early molecular actions that impact brain development and sexual differentiation (30-32). Other morphological changes in the hypothalamus and the preoptic areas have been correlated with sex and sexual orientations (14) The amygdala is involved in processing emotions, in particular fear, and in retaining long-term memory of emotionally-arousing events. Sex related differences in the hemispheric lateralization of processing emotional arousal by the amygdala were observed (33). Sex related differences were found in the relative size of the amygdala and hippocampus (34).The amygdala is larger relative to total cerebral size in men compared with women, and in boys compared with girls (35).

Testing the model

The model suggests that the auditory system provides the US’s stimuli around which individual sexuality evolves. However, people born with dysfunctional inner ear and auditory neural networks still develop their sexuality before puberty. This is an indication that the model describes a sufficient, but not necessary condition for the development of individual sexuality. Combinations of other factors, such as social, visual, olfactory and tactile, may act in parallel to the auditory stimuli. The relative role of auditory versus other cues may be assessed by comparing populations of intact and hearing impaired people.

Although human voice is an innately embedded feature that is used for identifying the sex of a speaker, it is not known which parts of the auditory system separate this cue from the rest of the sounds. In the last trimester of pregnancy, human fetuses already respond to the voice of their mother differently than to the voice of men (36). So, any part of the auditory system, from the inner ear to the auditory cortex, may be a candidate for the role of providing the cues to the sexual system.

A similar situation exists also in the two other parts of the model; the amygdala and the hypothalamus. These structures are involved in the integration of emotional and corporal information that is directly related to sexual activity. However, they themselves have bi-directional connections with higher and lower brain areas. So, even though they are primary candidates, other brain structures may also be involved in hosting the roots of sexuality.

Although the connectivity between auditory, emotional and corporal brain centers determines the root of human sexuality, reward centers may also have effect on the evolving sexuality. Reward centers affect the rate at which information is recorded. If a reward center favors one voice pitch over another, this could affect the formation of connections between the auditory and the two other centers of the model.

Off-the-shelf brain imaging, EEG, MEG and histological methodologies and techniques, such as those used in the references quoted here, could be used for validating the model. The correlation between the frequency of sound and activated cortical and sub cortical brain areas could be further explored using those and other methods. In particular, responses of brain areas to men’s and women’s voice could be mapped and sequenced. This includes responses to voice in both asexual and sexual contexts. The role of different emotions in triggering brain sexual response centers could also be further investigated.  If the model is validated, it would shed light on one of the oldest, fundamental, unresolved questions: why humans do it as they do it?

References

(1)  Klucken T, Schweckendiek J, Merz CJ, Tabbert K, Walter B, Kagerer S, Vaitl D, Stark R. Neural activations of the acquisition of conditioned sexual arousal: effects of contingency awareness and sex. J Sex Med. 2009; 6(11):3071-85.

(2) Savic I, Berglund H, Lindström P. Brain response to putative pheromones in homosexual men. Proc Natl Acad Sci USA. 2005;102:7356–7361.

(3) Berglund H, Lindström P, Savic I. Brain response to putative pheromones in lesbian women. Proc Natl Acad Sci USA. 2006;103:8269–8274.

(4) Meredith M. Human Vomeronasal Organ Function: A Critical Review of Best and Worst Cases. Chem. Senses 2001; 26: 433-445.
(5) Golombok S., Tasker F. Children in lesbian and gay families: theories andevidence. Ann. Rev. of Sex Res., 1994; 5, 73–100

(6) Tasker F. Children in Lesbian-Led Families: A Review. Clinical Child Psychology and Psychiatry 1999; 4, 153-166

(7) Meyer-Bahlburg HF. Sex hormones and female homosexuality: A critical examination.   Arch. Sex. Behav. 1979, vol 8, 2101-119

(8)  Banks A, Gartrell NK. Hormones and sexual orientation: a questionable link, J. Homosex 1995; 30, 247-268.

9) Meyer-Bahlburg HF, Dolezal C, Baker SW, Carlson AD, Obeid JS, New MI.   Prenatal androgenization affects gender-related behavior but not gender identity in 5-12-year-old girls with congenital adrenal hyperplasia. Arch Sex Behav. 2004; 33, 97-104.

(10) Gooren L. The biology of human psychosexual differentiation. Horm. Behav 2006; 50, 589-601.

(11) Swaab DF. Sexual orientation and its basis in brain structure and function. Proc Natl Acad Sci U S A. 2008 July 29; 105(30): 10273–10274.

(12) Swaab DF, Hofman MA. An enlarged suprachiasmatic nucleus in homosexual men. Brain Res. 1990;537:141–148.

(13) Swaab DF, Slob AK, Houtsmuller EJ, Brand T, Zhou J-N. Increased number of vasopressin neurons in the suprachiasmatic nucleus (SCN) of “bisexual” adult male rats following perinatal treatment with the aromatase blocker ATD. Dev Brain Res. 1995;85:273–279.

(14) LeVay S. A difference in hypothalamic structure between heterosexual and homosexual men. Science. 1991;253:1034–1037.

(15) Allen LS, Gorski RA. Sexual orientation and the size of the anterior commissure in the human brain. Proc Natl Acad Sci USA. 1992;89:7199–7202.

(16) Kinnunen LH, Moltz H, Metz J, Cooper M. Differential brain activation in exclusively homosexual and heterosexual men produced by the selective serotonin reuptake inhibitor, fluoxetine. Brain Res. 2004;1024:251–254.

(17) Rupp H, Wallen, K.  Sex Differences in Response to Visual Sexual Stimuli: A Review. Arch Sex Behav. 2008; 37(2): 206–218.

(18) Costa M, Braun C, Birbaumer N. Gender differences in response to pictures of nudes: A magnetoencephalographic study. Biological Psychology. 2003;63:129–147

(19) Gizewski ER, Krause E, Karama S, Baars A, Senf W, Forsting M. There are differences in cerebral activation between women in distinct menstrual phases during the viewing of erotic stimuli: A fMRI study. Experimental Brain Research.2006;174:101–108.

(20) Janssen E, Carpenter D, Graham CA. Selecting films for sex research: gender differences in erotic film preferences. Archives of Sexual Behavior. 2003;32:243–251

(21) Ponseti J, Bosinski HA, Wolff S, Peller M, Jansen O, Mehdorn HM, et al. A functional endophenotype for sexual orientation in humans. NeuroImage.2006;33:825–833

(22) Salu Y. Micropsychology, ISBN 1434 847 810, Create Space, 2008;  pp 31-78.

(23) APA. Diagnostic and Statistical Manual of Mental Disorders DSM-IV-TR Fourth Edition (Text Revision)  ISBN-10: 0890420254. American Psychiatric Publishing, Inc.; 4th edition (June 2000).  http://allpsych.com/disorders/dsm.html

(24) World Health Organization.  International Statistical Classification of Diseases and Health Related Problems (The) ICD-10, Volume 1: Tabular List (Second Edition, Tenth Revision). ISBN-10: 9241546492. World Health Organization; 2nd edition (December 2004)   http://www.who.int/classifications/icd/ICD-10_2nd_ed_volume2.pdf

(25) Giuliano F, Rampin O. Neural control of erection. Physiol Behav. 2004; 83(2):189-201.

(26) Berman JR.  Physiology of female sexual function and dysfunction. International Journal of Impotence Research 2005; 17, S44–S51.

(27) Woods DL, Alain C. Functional imaging of human auditory cortex. Curr Opin Otolaryngol Head Neck Surg. 2009;17(5):407-11

(28) McFadden D. Masculinization of the Mammalian Cochlea. Hear Res. 2009;252(1-2): 37–48.

(29) McFadden D, Champlin CA. Comparison of auditory evoked potentials in heterosexual, homosexual, and bisexual males and females. J Assoc Res Otolaryngol. 2000;1(1):89-99.

(30) Tobet  S, Knoll G, Hartshor C, et al.  Brain sex differences and hormone influences; A moving experience? J Neuroendocrinol. 2009; 21(4): 387–392.

(31) Tobet SA, Hanna IK. Ontogeny of sex differences in the mammalian hypothalamus and preoptic area. Adv Exp Med Biol. 2002;511:75-100; discussion 100-5.

(32) Swaab DF, Chung WC, Kruijver FP, Hofman MA, Ishunina TA. Sexual differentiation of the human hypothalamus. Adv Exp Med Biol. 2002;511:75-100; discussion 100-5.

(33) Cahill L, Uncapher M, Kilpatrick L, Alkire M, Turner J. Sex-Related Hemispheric Lateralization of Amygdala Function in Emotionally Influenced Memory: An fMRI Investigation. Learn Mem. 2004; 11(3): 261–266.

(34) Giedd JN, Castellanos FX, Rajapakse JC, Vaituzis AC, Rapoport JL. Sexual dimorphism of the developing human brain. J Am Acad Child Adolesc Psychiatry. 2001;40(9):1012-20.

(35) Durston S, Hulshoff Pol HE, Casey BJ, Giedd JN, Buitelaar JK, van Engeland H. Anatomical MRI of the developing human brain: what have we learned? J. Am. Acad.Child Adolesc. Psychiatry, 2001; 40(9):1012–1020.

(36) Kisilevsky BS, Hains SM, Brown CA, et al. Fetal sensitivity to properties of maternal speech and language. Infant Behav Dev. 2009;32(1):59-71.