Psychology, Evolution & Gender 2.3 December 2000 pp.

241252

Biological in uences on
homosexuality
Current ndings and future directions

Joel E. Alexander
Western Oregon University

Abstract
Recently, structural and functional differences have been found in
subjects categorized as homosexual in their sexual behaviour. This article
summarizes much of these ndings, indicates possible directions for
future studies, and addresses various issues related to research that
attempts to nd a relationship between biological factors and
homosexuality. It is concluded that this is still a very unexplored area that
has prompted unreasonable praise and criticism so early in what will turn
out to be a long process of identifying potential biological correlates of
sexual orientation.

Keywords: homosexuality, biology, ERP, EEG, MEG, hypothalamus

Introduction

Criticism and disregard for the research regarding biological influences

on homosexuality are at an all-time high. Perhaps surprising to some,
researchers in this area would, for the most part, tend to agree with many
of the criticisms. To date only three brain structure and four brain function
studies have produced ndings of differing results. Moreover, the research
involves establishing double confirmations, which requires verifying a
biological difference between heterosexual males and females and then using
that nding as a reference to match, control, and/or contrast the homosexual
sample. As most neuroscientists know, it is dif cult to nd sex differences
Psychology, Evolution & Gender
ISSN 1461-6661 print/ISSN 1470-1073 online 2000 Taylor & Francis Ltd
http://www.tandf.co.uk/journals
DOI: 10.1080/14616660010024607

242 Joel E. Alexander

in general given the enormous variability within each sex. To then make
these male and female subjects the control group, and on top of which to
make judgment about two more groups (gay and lesbian) that also have
enormous within-group variability seems at rst glance to be foolhardy.
Many reviews of the literature surrounding biological influences or
associations with homosexuality tend to focus on the three classic structural ndings of the early 1990s, and are reviewed below brie y as they have
been cited in other reviews. However, in addition to these structural
ndings, functional measures of brain activity also need to be considered.
Additionally, some of the controversy that follows this area of research will
be reviewed, with some possible direction for future structural and functional research that use populations of differing sexual orientation.
Past research

The past biological research on sexual orientation can easily be grouped

into two categories: structural and functional biological paradigms. No
research to date has attempted to combine the two into one paradigm that
utilizes the same samples. Common among these studies is the approach
mentioned above in which some form of sexual dimorphism is established
between heterosexual males and females, which then is compared with the
homosexual group(s).
Structural studies

Sex differences in the brain have been a long-sought project for both good
and bad reasons. Physicians in the nineteenth century noted that females
had smaller brains than males (Burnham 1977). This early finding was
revealed to the public and perpetuated, if not enhanced, the bias against
women and their intellectual abilities. We must naturally expect that man,
surpassing woman in volume of brain, must surpass her in at least a
proportionate degree in intellectual power (Popular Science Monthly 1879,
as cited in Russett 1989: 16). Although it is true that male brains are somewhat larger (12 per cent heavier and 2 per cent larger at birth) than female
brains, this is the rst example of a structural difference that does not evince
a measurable behavioural difference. According to Halpren (1992), there is
no evidence at all that larger brains outperform smaller brains. Indeed once
the size of the brain has been normalized according to body weight, the
female brain has been found to be larger than male brains (Halpren 1992).
Regardless, this nding did spawn research aimed at establishing similar
differences among sex variants early in the twentieth century.
As early as the 1930s, the Committee for the Study of Sex Variants in New
York City assessed homosexual populations using various psychological

Biology and homosexuality 243

tests, hormonal measurements, and physiological measurements of the

genitalia and other body parts including skull circumference. In part,
these physical measurements were designed in an attempt to show the
masculinization that had been found years before via the skull circumference
studies that compared males and females (Henry 1948). The authors
reluctantly acknowledged that the physical examinations produced inconclusive evidence by which to determine whether an individual woman was
a sex variant (Henry 1948). As a group, there were some morphological
differences between homosexual and heterosexual women (lesbian populations having slightly larger skull circumference). But the variance within
the sex variant group was so large that many lesbian females had physical
characteristics identical with those of heterosexual females and many
heterosexual females also had large head circumference similar to the lesbian
subjects (Henry 1948).
The next revolution in physiological studies of differences between the
sexes came about with the nding of sexually dimorphic areas in rodent
brains. With advancements made in cellular biology, it became possible
to look at speci c areas of the brain for sexual dimorphism. Gorski, Gordon,
Shryne and Southam (1978) found that a part of the pre-optic area,
the sexually dimorphic nucleus (SDN-POA), was larger in male compared
to female rats. This has been found in other, but not in all of the species
investigated. However, to date, there has been no causal connection made
in respect to functional brain activity (Bancroft 1994). Indeed, as Swaab and
Hofman (1995) point out, lesions to the SDN-POA produce a change in
some components of masculine behaviour, and there is a positive correlation
between testosterone level and size of the SDN-POA; yet, the extent
of changes in behaviour following lesioning is so small that it is quite likely
that the major function of the SDN-POA has not been established. The
structure/function issue thus continues to be a major empirical as well as
theoretical problem.
With the SDN-POA identi ed as different in male and female rats, it was
only a matter of time before this finding and sexual differentiation in
humans would be investigated. Although mixed results have been obtained,
this same area has been identi ed as existing in humans and was originally
identi ed as the intermediate nucleus of the hypothalamus (Braak and Braak
1987). Hofman and Swaab (1989) examined the morphometric qualities
of the intermediate nucleus of the hypothalamus and found that the volume
is more than twice as large in young adult males as it is in females. Additionally, it was found that there are twice the number of cells comprising this
area of the hypothalamus in males compared to that of females (Hofman
and Swaab 1989). The magnitude of this sex difference varied according to
age such that the difference was largest for subjects aged 2045. Male and
female subjects between the ages of 50 and 70 years were similar in cell

244 Joel E. Alexander

number with a noticeable sex difference reappearing with a sharp decrease

in the number of SDN-POA cells in females aged 70 and older. This suspected age-dependent change in the hypothalamus has been identi ed as
the reason why a study by Allen, Hines, Shryne and Gorski (1989) did
not nd a sex difference in this region of the hypothalamus when they used
a sample that had a large proportion of middle-aged adults (Swaab and
Hofman 1995). However, they did nd two other areas more posterior in
the hypothalamus that were sexually dimorphic in volume. Because Allen
et al. (1989) found multiple sexually dimorphic cell groups, they decided
not to call them some form of the SDN-POA acronym. Instead, they used
the term interstitial nucleus of the anterior hypothalamus (INAH) and subscribed the numbers 1 (i.e. INAH1) to the original location that was found
to be sexually dimorphic by Hofman and Swaab (1989) and the numbers
2 and 3 (i.e. INAH2 and INAH3) to the locations found to be sexually
dimorphic in their study (Allen et al. 1989; Swaab and Hofman 1995).
This state of affairs produced three names for the same area: intermediate nucleus of the hypothalamus, SDN-POA, and INAH1. The highly
publicized study of LeVay (1991) also failed to replicate the SDNPOA (INAH1) nding of Hofman and Swaab (1989), as well as failing to
replicate the INAH2 nding of Allen et al. (1989), although Le Vay (1991)
did replicate the sexually dimorphic characteristics of the INAH3 from the
Allen et al. (1989) study. This variability of ndings is suspect, but Swaab
and Hofman (1995) point out that the Allen et al. (1989) and LeVay (1991)
studies did not measure number of cells, only volume of these areas of the
hypothalamus. Additionally, the age-dependent changes mentioned above
may have confounded the replicability of results. Even though sexually
dimorphic structures have been found, failure to replicate, varied sample
selections, and differing measurement techniques have all led to an inconsistency in the biology of sex differences literature.
The early 1990s was a remarkably productive period of time for research
into sexual dimorphism of brain areas. In addition to the above studies, the
volume of the darkly staining posteriomedial component of the bed nucleus
of the stria termanalis (BNST-dspm) was found to be 2.5 times larger in
males than females (Allen and Gorski 1990). The next year another sexually
dimorphic area was found in that the anterior commissure was found to
be 12 per cent larger in females. Additionally, in the same study, the interthalamic adhesion, a gray structure that transverses the third ventricle
between the two thalami, was present in 10 per cent more females than
males (Allen and Gorski 1991). Taken together, these ndings indicate that
sexually dimorphic structures can be found in many different areas of the
brain.
With a number of studies finding sexually dimorphic structures in a
relatively short period of time, the stage was set to look at sexual orientation

Biology and homosexuality 245

relative to brain structure. The first major finding was by Swaab and
Hofman (1990) in which clear differences in the suprachiasmatic nucleus
(SCN) of the hypothalamus were found such that the subpopulation
of vasopressin-containing neurons was twice as large in homosexual men
compared with heterosexual men. LeVay (1991) followed the next year with
a working hypothesis that these cell groups are more responsive to sexual
orientation rather than biological sex differences. The LeVay (1991) study
found that the INAH3 was twice as large in homosexual compared with heterosexual males. The third study involving structural differences according
to sexual orientation is the Allen and Gorsky study of 1992 in which the
anterior commissure (found to be sexually dimorphic larger in females)
also was different according to sexual orientation such that it was larger
in homosexual males compared with both heterosexual males and females.
Since the homosexual group did not fall between or have identical size to
the female group, this outcome gave rise to another working hypothesis of
a third sex the gay sex.
The next wave

After these initial major reports, for approximately 5 to 6 years, few

studies into the structural sexual dimorphism between males and females
and/or heterosexuals and homosexuals occurred. However, a new set of
studies has been conducted in which hormonal influences are tied to
structural differences. For example Cooke, Tabibna and Breedlove (1999)
found a sexual dimorphism in the volume of a brain nucleus in rats that they
attribute exclusively to adult sex differences in circulating androgen. The
posterodorsal nucleus of the medial amygdala (MePD) was found to have
a greater volume in male rats than in females, but adult castration of males
caused the volume to shrink to female values within four weeks. In contrast,
androgen treatment of adult females for the same period enlarges the MePD
to levels equivalent to normal males. This report demonstrates that adult
hormone manipulations can completely reverse a sexual dimorphism in
brain regional volume in a mammalian species.
Oka et al. (1999) utilized MRI to study sexual dimorphism of the human
corpus callosum (CC). They analyzed a midsaggital cut for morphometry
differences in 67 adults and established four speci c angles of the CC. All
four of these angles in 34 females and 33 age-matched males showed a significant difference between females and males in the angular orientation of
corpus callosum. These results suggest that the search for sexually dimorphic
areas of the brain is far from over, thus future sexual orientation studies will
undoubtedly, and hopefully, follow.
Finally, Breedlove (1997) studied castrated male rats implanted with
testosterone- lled silastic capsules. The rats were divided into two groups

246 Joel E. Alexander

such that for 27 days the copulators were given receptive females and the
non-copulators were paired with non-receptive females. The spinal cords of
both male groups were stained with thionin to reveal motor neurons in the
spinal nucleus of the bulbocavernosus (SNB). These motor neurons and
their striated target muscles are active during male copulatory behaviour
(Breedlove and Arnold 1980). They found that copulatory experience can
alter the size of neurons and their somata. Given that both groups had the
exact same levels of androgens, the only connection that can be made is
that sexual experience changed the size of these nuclei. Breedlove concludes
that it is possible that differences in sexual behavior cause, rather than are
caused by, differences in brain structure (Breedlove 1997: 801).
Context is needed for these structural results. Harrison, Everall, and
Catlan (1994) reviewed this literature during the peak frenzy of research in
this area and pointed out that these studies need replication and extension.
Additionally, they noted that consistency among methodologies and an
increase in details regarding the clinical information on the subjects is
needed. In sum, it was still too early to feel con dent about sexual differentiation in the brain let alone sexual orientation differences.
Functional studies

Another area of research that followed on the heels of the structural studies
of the early 1990s comprised four functional studies. The first study
conducted by Alexander and Sufka (1993) recorded electroencephalographic (EEG) activity over four left and four right cerebral hemispheric
locations while subjects performed verbal and spatial cognitive tasks.
Male homosexuals had a greater asymmetry in their pattern of alpha
power compared with both heterosexual males and females during baseline
recording. Different hemispheric patterns of alpha activity also were
observed between homosexual and heterosexual males during affective
judgments of both verbal and spatial stimuli, but not between homosexual
males and heterosexual females. The homosexual males had greater
inhibition of activity across the right hemisphere compared with heterosexual males during the verbal task and greater activation across the left
hemisphere during spatial tasks compared to heterosexual males who had
marked inhibition in the left hemisphere. Similar to the structural studies,
a dichotomy between males and females was established and then the
homosexual group was added for comparison. Unfortunately, this study
did not use a lesbian population and looked at only one bandwidth of EEG
activity at only eight recording locations, so the interpretation of the ndings
is limited.
Reite, Sheeder, Richardson and Teale (1995) recorded MEG auditory
M100 source location in the left and right hemispheres of eight strictly

Biology and homosexuality 247

homosexual and nine strictly heterosexual males. This M100 had been
found to be sexually dimorphic in previous studies (Reite, Teale, Goldstein,
Whalen and Linnville 1989; Baumann et al. 1991). MEG elds evoked by
auditory tone pips were recorded from left and right hemispheres in
response to contralateral ear stimulation. The authors found an auditory
asymmetry difference between heterosexual males, who were signi cantly
further anterior in the right hemisphere compared to the left hemisphere;
however, homosexual males did not exhibit signi cant interhemispheric
asymmetry. Their ndings suggest an anatomic and/or functional difference
in the superior temporal gyrus of at least some homosexual men (Reite et al.
1995). Heterosexual and homosexual females were not included in the study.
Wegesin (1998) assessed event-related potentials (ERPs) recorded at 10
locations on the scalp from 20 heterosexual males, 20 heterosexual females,
20 homosexual males, and 20 homosexual females. To elicit sex differences
in behavioural responses, a mental rotation task assessing spatial ability, and
a divided-visual-eld lexical-decision/semantic monitoring task assessing
verbal ability and relative degrees of language lateralization were used. Slow
wave activity recorded during mental rotation was greater for heterosexual
males than for heterosexual females and homosexual males. N400 asymmetries recorded during the lexical decision/semantic monitoring task
revealed that homosexual males demonstrated a mixed pattern of verbal
asymmetry, showing patterns resembling those of females for lexical decision
and patterns resembling those of heterosexual males for semantic processing.
Results for the homosexual females indicated that, similar to heterosexual
males, they produced a high level of slow-wave activity during the mental
rotation task. This study is perhaps the most comprehensive functional
study involving sexual orientation as a factor to date given that they
used cognitive tasks rmly established to have speci c sex differences and
time locked the presentation of these tasks to the recording of the brain
activity.
Recently, McFadden and Champlin (2000) reported sexual orientation
differences in both males and females for auditory evoked potentials
(AEPs). AEPs are different than ERPs in that AEPs do not require an overt
behavioural response from the subject. AEPs are beneficial in diagnosis
of neurological impairment of structures from the cochlea up through the
brainstem and even into subcortical and cortical areas of the brain. A series
of these peaks, or burst of activity, at certain latencies have been related to
speci c structures through the brain stem up to cortical areas of the brain.
Within the rst 20 ms auditory brainstem responses (ABRs) have provided
very consistent evidence regarding the function of these brainstem areas.
In their study McFadden and Champlin found that some of the components measured (mostly ABRs) were different in amplitude and/or latency.
Unfortunately, owing to sample size homosexual and bisexual groups were

248 Joel E. Alexander

combined to produce adequate Ns. The directionality of the results is of

interest. Homosexual/bisexual female AEPs showed masculinization (i.e.
more similar to heterosexual males than heterosexual females), whereas
homosexual/ bisexual males show hypermasculinization (i.e. results that are
directionally different than all groups). The direction of these results brings
up the specter of the third-sex hypothesis again, at least with respect to the
male homosexual/bisexual group.
All four of these studies have limitations but each provides some tantalizing preliminary indications that differences can be found with respect to
brain activation patterns between differing sexual orientation groups. More
EEG bandwidths could still be explored in studies similar to the Alexander
and Sufka study (1993) and numerous ERP components could still be
evaluated for both amplitude and latency differences in studies like the
Wegesen (1998) study. Reite et al. (1995) differs from the other two in that
it uses a paradigm that evokes functional brain activity in which recordings
are made in an event-related fashion. The use of other cognitive tasks
that elicit sex differences should also be explored. Both the Reite et al. (1995)
and the Alexander and Sufka (1993) studies used only homosexual males
and not homosexual females with regard to sexual orientation, so obviously
the inclusion of homosexual females is important in future studies.
Although the pooling of homosexual and bisexual groups in the McFadden
and Champlin (2000) study is troubling, the ABRs have clear sex differences
that last throughout life thus providing a rm base for comparison of homosexual data.
Current status

With newly identi ed sexually dimorphic areas of the brain having been
discovered, further studies need to be conducted with respect to sexual
orientation. With improved techniques in both the structural and
functional analyses, a new round of approaches that examine biological
correlates of sexual orientation will prove very informative. These studies
should continue to use the double con rmation method of establishing a
sexual dimorphism prior to establishing sexual orientation differences.
Unfortunately, dichotomous variable designs derived out of what most
would assume to be a continuous variable (sexual orientation) are bound
to produce marginal, mixed, and/or null results. If sexual behaviour is categorized into an either/or designation when it undoubtedly changes along
multiple continuums, then inaccurate conclusions will follow. Thus,
multivariate and covariate analyses should be used whenever possible,
although a major problem is finding an evaluation instrument that can
differentiate levels of sexual orientation in a more precise manner than
simple seven-point Kinsey-like scales (Kinsey, Pomeroy and Martin 1948).

Biology and homosexuality 249

Despite these dif culties and issues, it is the case that 100 per cent of the
studies to date that attempted to nd biological correlates have found them.
Three structural and four functional studies all indicated some finding
regarding biological correlates of sexual orientation. Unfortunately, by the
end of the 1990s only seven structural/functional studies had actually been
conducted with reference to sexual orientation. This is important to note
given the restorm that seems to follow this issue. All of the studies to date
have found some differences; however, they are limited in number and
scope. Moreover, causality is dif cult if not impossible to determine in these
quasi-experimental designs.
Future directions

There are three main areas that need to be studied with regard to biological
correlates of homosexuality. First, studies that search for sexually dimorphic
structures must continue. Fortunately, various groups seem to be engaged
in just such a venture (e.g. Cooke et al. 1999; Oka et al. 1999). These studies
will probably need to use both animal and human models to identify
probable structures. Replication and multiple measurement techniques are
necessary to establish the sexual dimorphism prior to making the switch to
sexual orientation correlates. Second, studies investigating the relationship
between structure and function utilizing existing scanning technology
are needed. This is not an easy area to investigate. It is very dif cult to nd
oneone relationships between a structural scan and a functional scan (King,
Isaacson and Alexander 1999). These studies need not be directly related to
sexual dimorphism or orientation, but basic research is needed in this area
to establish rmly areas and paradigms in which we can clearly see structure
function relationships with our present scanning capabilities. Third, more
studies involving functional scans (e.g. ERP, SPECT, fMRI) in relation to
tasks that are traditionally found to differ between the sexes. It should be
noted with respect to the rst and third directions of research mentioned
above that it may ef cacious to go ahead and conduct studies without the
prior sexual dimorphism established, especially if the third-sex hypothesis
has potential for veri cation or if the causal relationship is such that differing
sexual activity causes changes in the brain (Breedlove 1997; LeVay 1993).
It may be the case that we nd differences in cognitive tasks (matched with
functional brain activation measures) between sexual orientation groups
that are not different between the sexes.
Conclusions

Interestingly, these seven studies, all with different methodologies and

measurement techniques, along with some behavioural and hormonal

250 Joel E. Alexander

studies, created a firestorm of controversy and spawned many reactive

articles (cf. Looy 1995; Muir 1996; Williams 1996). Indeed, much of the
writing regarding biological correlates of homosexuality in the 1990s was
not actually related to speci c studies, but conducted by armchair critics
pointing out the obvious with regard to the limitations surrounding these
early results. The complexity of the issue should be attractive to researchers,
given that resolution is not yet at hand but will be of significant public
interest as each piece of the puzzle is placed in position. The fun also lies in
the complexity, the challenge, and even in the controversy arising from the
investigation into socially sensitive areas.
When one steps back to look at all of the research thus far in this sensitive
area, predictions seem requisite, if not par for the course. Thus, it is predicted: (1) that a majority of the sexual dimorphism in structure is probably
the result of hormonal in uences deriving in part from environmental and
genetic sources, yet also in small part due to social in uences including
behaviour; (2) that brain function is of course dependent upon brain
structure but can also recursively in uence and selectively activate differing
structural areas of the brain, thus in uencing future structure in the brain;
and (3) that sexual differences and sexual orientation differences operate on
unique continuums and by classifying these groups into males and females,
heterosexual and homosexual, we are arti cially restricting and reducing
the natural variations within each group.
Address for correspondence

Joel E. Alexander, Ph.D., Department of Psychology, Western Oregon

University, Monmouth, OR 97361, USA. Tel.: +503-838-8355; fax: +503838-8618; e-mail: Alexanj@wou.edu
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