Biological in uences on homosexuality Current Ž 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 Ž ndings, indicates possible directions for future studies, and addresses various issues related to research that attempts to Ž 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 Ž 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 Žnding as a reference to match, control, and/or contrast the homosexual sample. As most neuroscientists know, it is difŽ cult to Ž nd sex differences

Psychology, Evolution & Gender 2.3 December 2000 pp. 241–252

Psychology, Evolution & Gender ISSN 1461-6661 print/ISSN 1470-1073 online © 2000 Taylor & Francis Ltd

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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 Ž rst glance to be foolhardy.

Many reviews of the literature surrounding biological influences or associations with homosexuality tend to focus on the three classic struc- tural Ž 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 Ž 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 func- tional 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 some- what larger (12 per cent heavier and 2 per cent larger at birth) than female brains, this is the Ž 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 Žnding 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

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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 incon- clusive 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 popu- lations 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 Ž nding of sexually dimorphic areas in rodent brains. With advancements made in cellular biology, it became possible to look at speciŽ 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 identiŽ 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 identiŽ ed as existing in humans and was originally identiŽ 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. Addition- ally, 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 20–45. Male and female subjects between the ages of 50 and 70 years were similar in cell

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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 sus- pected age-dependent change in the hypothalamus has been identiŽ ed as the reason why a study by Allen, Hines, Shryne and Gorski (1989) did not Ž 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 Ž 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 sub- scribed 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: interme- diate nucleus of the hypothalamus, SDN-POA, and INAH1. The highly publicized study of LeVay (1991) also failed to replicate the SDN- POA (INAH1) Žnding of Hofman and Swaab (1989), as well as failing to replicate the INAH2 Ž 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 Ž 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 incon- sistency 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 inter- thalamic 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 Ž 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

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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 het- erosexual 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 speciŽ c angles of the CC. All four of these angles in 34 females and 33 age-matched males showed a signif- icant 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-Ž lled silastic capsules. The rats were divided into two groups

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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 conŽ dent about sexual differen- tiation 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 electroencephalo- graphic (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 hetero- sexual 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 Žndings is limited.

Reite, Sheeder, Richardson and Teale (1995) recorded MEG auditory M100 source location in the left and right hemispheres of eight strictly

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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 Ž 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 signiŽ cantly further anterior in the right hemisphere compared to the left hemisphere; however, homosexual males did not exhibit signiŽ cant interhemispheric asymmetry. Their Ž 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-Želd 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 asym- metries 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 Ž rmly established to have speciŽ 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 speciŽ c structures through the brain stem up to cortical areas of the brain. Within the Ž 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 compo- nents measured (mostly ABRs) were different in amplitude and/or latency. Unfortunately, owing to sample size homosexual and bisexual groups were

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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 tanta- lizing 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 Ž rm base for comparison of homo- sexual data.

Current status

With newly identiŽ 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 conŽ 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 cate- gorized 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).

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Despite these difŽ culties and issues, it is the case that 100 per cent of the studies to date that attempted to Ž 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 Ž 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 difŽ 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 difŽ cult to Ž nd one–one 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 Ž 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 Ž rst and third directions of research mentioned above that it may efŽ cacious to go ahead and conduct studies without the prior sexual dimorphism established, especially if the ‘third-sex’ hypothesis has potential for veriŽ 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 Ž 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

Biology and homosexuality 249

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 speciŽ 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 pre- dicted: (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 artiŽ 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: +503- 838-8618; e-mail: [email protected]

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