Medical Hypotheses 76 (2011) 384387

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Medical Hypotheses
journal homepage: www.elsevier.com/locate/mehy

The roots of sexual arousal and sexual orientation

Yehuda Salu
Department of Physics and Astronomy, Howard University, 2235 6th Street NW, Washington, DC 20059, United States

a r t i c l e

i n f o

Article history:
Received 23 June 2010
Accepted 29 October 2010

a b s t r a c t
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 denes the basic mechanisms
and their role in developing individual sexuality. It is suggested that three brain areas host the roots of
human sexuality: the auditory area, which provides stimuli that serve as cues for the identication 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 lls a gap in the understanding of human sexuality knowledge that would benet individuals, the medical profession, and
society as a whole.
2010 Elsevier Ltd. All rights reserved.

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
Tel.: +1 202 806 6025; fax: +1 202 806 5830.
E-mail address: ysalu@howard.edu
0306-9877/$ - see front matter 2010 Elsevier Ltd. All rights reserved.
doi:10.1016/j.mehy.2010.10.048

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.
Pavlovs experiment): the unconditioned stimulus US (taste of
food), the unconditioned response UR (salivation), and the conditioned stimulus CS (bells ring). The unconditioned stimulus US
and its response UR are already a part of the brains information
system. Then, the unconditioned stimulus US 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 the US 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 USs and URs are the root of human sexuality;

Y. Salu / Medical Hypotheses 76 (2011) 384387

they determine the sexuality of the individual. Unlike in Pavlovs

experiments, the innate sexual USs and URs 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 USs 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 USs 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 USs 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
proles 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 [710].
Several morphological and functional brain differences between
the sexes have been observed [11], but their roles in sexual activities need clarication.
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 (uoxetine) 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 mens sweat is approximately 10 time greater than in womens, and the estrogen-like steroid estra-1,3,5(10),
16-tetraen-3-ol (EST), which was detected in womens urine,
elicited different responses, concurrent with sexual orientation, in
the hypothalamus of HeW and HoM, but not it HeM. [2] and in
HoWs 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,

385

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 specic features that cause the arousal
may be subjective [20]. Overall, it is difcult 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 ts these specications. 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 womens voice. When the boy hears a womans voice, features of that
woman are conditioned and become cues of the boys 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 mens voice, in HoM they are tuned to mens
voice, in HoW they are tuned to womens 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

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Y. Salu / Medical Hypotheses 76 (2011) 384387

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 loosing 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 mothers 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 USs 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 USs 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 adults 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 inuenced 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 mufe 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 USs and URs around which
individual sexuality is developed. The rst developmental stage occurs from childhood to puberty, and it relies on asexual individual
experiences. During this period, asexual cues that are typical to the
childs 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 USs and URs 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 813% shorter than those of males [28]. Otoacoustic
emission (OAE) is sound generated by the cochlea in response to
external sound. It enhances features of 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 [3032]. Other morphological changes in the hypothalamus and the pre-optic 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

Y. Salu / Medical Hypotheses 76 (2011) 384387

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 USs
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 sufcient, 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 mens and
womens 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?
Conicts of interest statement
None declared.
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