A brief historic overview of sexual and gender diversity in neuroscience: past, present, and future

A brief historic overview of sexual and gender diversity in neuroscience: Past, present, and futureAbstractThis opinion paper is informed by the brief history of sexual and gender diversity in neuroscience and suggested future directions. Employing a bibliographic search of relevant literature, the authors identified an upward trend in the representation of neuroscience and LGBTQIA+ issues in scientific literature. Providing a chronological timeline of significant developments, the paper among others considers how the field distinguishes itself from psychiatry and neuroscience. Indeed, the field has moved from historically lobotomizing gay men to control their sexuality to a now wider biopsychosocial and cultural scientific perspective embracing and celebrating the sexually and gender-diverse, more broadly. Early studies were concerned with biological, abnormal, and disordered aspects of behavior, primarily related to sexual orientation. This was followed by attempts at redefinition and reclassification. Increased critiques of biological and individual perspectives morphed into more integrative theories and greater acknowledgement of social determinants of health. Notably, trans- and gender diversity-related research only feature significantly after the year 2000, with affirmative approaches coming to the fore in the decade 2011-2020 onwards. Looking to the future, the authors offer insights into the state of knowledge, identify potential research gaps, and suggest directions for further exploration in this interdisciplinary field.Keywords: Key developments; LGBTQIA+; Neuroscientific; Bibliographic literature search; Research trends; Sexual and gender diversity; SOGI IntroductionFor decades, scholars across disciplines, including researchers, scientists, and clinicians, have exhibited a keen interest in exploring the neuroscientific underpinnings of sexual and gender diversity. The purpose of this paper is thus to provide an overview and opinion on the evolution of related research. To achieve this, the authors conducted a bibliographic search of the literature in MEDLINE and PsycInfo from inception to September 2023 with specific keywords, including “neuroscience”, and variations of “lesbian, gay, bisexual, transgender, queer, intersex, asexual, and people with other sexual orientations and forms of gender expression (LGBTQIA+)”. The results presented in Figure 1 show that there is an increase in neuroscience and LGBTQIA+ concerns represented in the scientific literature. In particular, the decade from 1991 to 2000 saw a significant growth in related publications, with the field of neuroscience establishing itself as distinct from psychiatry. However, 2011-2020 was the most prolific decade in the history of sexual and gender diversity in neuroscience. In summary, there were 1167 records (i.e., scientific articles, book chapters, opinion letters, among others) corresponding to a collective sample of 444,249 individuals on the LGBTQIA+ spectrum. Most research centered on gay men (32%) or transgender people (24.3%), and only a few addressed lesbian (1.1%), bisexual (1.3%), or other identities (1.1%). When mixed samples were included, the majority corresponded to gay and lesbian people (15.3%). The most common topics were brain development (34.6%), general biological aspects (31.8%), and human immunodeficiency virus (HIV)-related research (27.5%). In addition, articles focused on social (19%), psychological (15.9%), and neuropsychological (13.3%) aspects of sexual and gender identity. Animal studies accounted for 7.8% of research.Insert Figure 1 hereBefore considering the future of neuroscience of sexual and gender diversity, we first provide a chronological overview of select related key developments in the field.Overview of select key developments in sexual and gender diversity in neuroscienceEarly workThe first record we identified appeared in 1917 in the context of mental disorders suggesting that brain pathology could be related with sexual behavior (Meyer, 1917). Until 1950, only nine publications captured by this search focused on human sexuality, and as complex and multi-determined by biological, psychological, and sociological aspects (Morselli, 1931). This literature indicated that structural damages have an impact on sexual behavior. For instance, “bad thyroid gland may cause queer behavior in the human” (Moss, 1932). During the same period, homosexuality was, in fact, classified as part of psychiatric syndromes (Rosanoff, 1938) and this continued to be the case until 1973. Lobotomy was offered as an option for treating the so-called “sex psychopaths” (Banay and Davidoff, 1942). From 1951 to 1960, seven publications addressed topics linking sexuality to brain abnormalities. For instance, records theorized upon associations linking disturbed cerebral functioning with bisexuality and schizophrenia (Potzl, 1951) and the Klüver-Bucy syndrome with “homosexual advances” following the removal of the temporal lobes (Terzian & Dalle Ore, 1955). Later, scientific research on the same syndrome indicates that it is characterized by increased nonselective sexual behavior, and not homosexuality itself. However, it was interpreted as homosexual behavior at the time the study was conducted. Between 1961 and 1970, six records were found on topics such as gender identity in gay males and psychosexual functioning of the brain (Money, 1965), the use of hypothalamotomy for sexual disorders (Anonymous, 1969), and literature suggesting a link between criminality and psychiatric disorders, with homosexuality being considered one of them (Guze, Goodwin, & Crane, 1969).Redefining research and classification systems (1970s and 1990s)Informed by changing social and scientific attitudes and theories about sexual orientation, in 1973, homosexuality as a mental disorder was officially removed from the Diagnostic and Statistical Manual of Mental Disorders (DSM). From 1971 to 1980, 33 records included topics studying the use of electroencephalographic techniques to document pleasure in men (Heath, 1972) and transgender people (Nussselt & Kockott, 1976), as well as brain functioning differences between gay men and heterosexual men (Wilson, Zung, & Lee, 1973). During this time, neurochemistry studies flourished. This included the role of brain monoamines in male sexual behavior (Gessa & Tagliamonte, 1974), the role of hormones as an explanation for homosexuality in men (Dorner, Rohde, Stahl, Krell, & Masius, 1975), and animal models of homosexuality in rats and rabbits that experimented on serotonin levels (Fratta, Biggio, & Gessa, 1977). Brain injury studies included the link between homosexuality and early brain damage (Holzer, 1976) and there were studies linking “latent homosexuality” with schizophrenia in males (Sigal, 1978). In addition, we find the first reference to “patients with the problem of intersexuality” when endocrine problems can “masculinize” females and “demasculinize” males (Ehrhardt & Meyer-Bahlburg, 1979). From the period between 1981 and 1990, the search led to 173 records. And yet, there was only one study addressing neuroendocrine contributions to male and female homosexuality (MacCulloch & Waddington, 1981). A few studies also provided a more nuanced approach and considered sex-related brain differences as a mosaic of both male and female "characteristics" influenced by hormones (Neumann & Elger, 1981). The 1980s also marked the beginning of investigations on samples of gay men to document opportunistic infections of the central nervous system associated with HIV (Anderson, Atlas, Ahern, & Weisbrot, 1983; Handler, Ho, Whelan, & Budzilovich, 1983). Despite changes in psychiatric nomenclature, psychopathological views persisted. For instance, a study suggested a relationship between decreased serotonergic activity and “delusional ideas of homosexual content” in individuals with paranoid schizophrenia (Rinieris, Markianos, Hatzimanolis, & Stefanis, 1985). Yet, during this decade, researchers also started to question studies focusing on the biological basis of homosexuality as tainted by personal beliefs and cultural prejudices (Ricketts, 1984). Furthermore, the traditional nature/nurture debate around the genesis of sexual behaviors (homosexual, bisexual, and heterosexual) was enriched by new concepts, such as “critical-period/nurture” in brain development and social influences on behavior (Money, 1986). Another study suggested a change in sexual preference following brain injuries involving limbic system structures (Miller, Cummings, McIntyre, Ebers, & Grode, 1986). More integrative theories started to appear classifying sexual orientation as a complex phenomenon determined by genetic-hormonal, pharmacological, maternal stress, immunological, and social experiential variables (Ellis & Ames, 1987). An integrative book consolidating multiple perspectives to explain sexual orientation was published during this decade (Money, 1988). Interestingly, this period was also the beginning of theories linking a cluster of cells located in the preoptic area of the hypothalamus with sexual orientation and gender identity (Swaab & Hofman, 1988).The decade from 1991 to 2000 showed a significant explosion in scientific productivity as compared to the previous decades with 273 records. A new clinical interest started to emerge leading to neurorehabilitation approaches specifically tailored for the needs of gay and lesbian people with brain injuries (Mapou, 1990). Investigating the neural correlates of sexual orientation and gender identity were not as important anymore as finding alternatives to meet LGBTQIA+ health and wellness needs following a brain injury. With the proliferation of neuroscience emerging as a field separate from psychiatry, the results of neuroanatomical and neuropsychological studies began to be used in perspectives that were less pathologizing. In this manner, there were studies suggesting a neurobiological component related to hemispheric functional lateralization with an over-representation of left-handedness in gay men and lesbian women (McCormick, Witelson, & Kingstone, 1990). The results of a neuroanatomical study also showed that the midsagittal plane of the anterior commissure in gay men was 18% larger than in heterosexual women and 34% larger than in heterosexual men (Allen & Gorski, 1992). In addition, the number of cells in the suprachiasmatic nucleus of the hypothalamus in gay men was indicated as twice as large in comparison to heterosexual individuals (Swaab, Gooren, & Hofman, 1995), while a female-sized volume of the central subdivision of the bed nucleus of the stria terminalis was found in male-to-female transsexuals (Kruijver et al., 2000; Zhou, Hofman, Gooren, & Swaab, 1997). Critiques of genetic (Hamer & Copeland, 1994) and hormonal studies (Garnets & Kimmel, 1993) concerning human sexual orientation started to appear during this time. This perspective essentially argued against “nature” as a single biological determinant of sexual orientation (Banks & Gartrell, 1995; Byne & Parsons, 1993; Gooren, 1995) and instead considered a multitude of biopsychosocial factors (Bancroft, 1994; Byne, 1997; Doell, 1995; Friedman & Downey, 1993; Looy, 1995). These changes were also reflected in animal models of homosexuality with an alternative bio-social program of research on the development of sexual behavior in animals (Fausto-Sterling, 1995). Notwithstanding, genetic studies with Drosophila models of sexual orientation continued to flourish (Ferveur, Stortkuhl, Stocker, & Greenspan, 1995; Ito et al., 1996; Yamamoto, Ito, & Fujitani, 1996). There were also animal models of homosexuality in rams and sheep (Perkins & Fitzgerald, 1997), and rat models of bisexuality (Aron, 1999). Critics also called attention to the fact that this research excluded females/women and ethnic minorities and denied the political, cultural, and historical dimensions of sexuality (Hegarty, 1997). 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