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As we know, textbooks have a difficult time keeping up with social changes, (clips were provided on Gender Revolution, and a Ted Talk on anatomy defining us) to supplement. Based on your book, article, and what you saw addressed in the clips; what topics would you have liked for the textbook, article, or the clips to address about gender roles/identity? Where do you think there is still insensitivity? How will you address this insensitivity if you have the opportunity? How would you educate parents on gender roles/identity? What resources would you recommend for us to use when talking to parents about gender identity/ roles? https://www.facebook.com/katiecouric/videos/gender…
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How Early Hormones Shape Gender Development
Sheri A. Berenbauma and Adriene M. Beltzb
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Abstract
Why are the sexes different? How does the prenatal environment set the stage for postnatal
development? How does behavior result from transactions between the brain and the social
world? All three questions are the focus of contemporary work in the behavioral sciences, and
they converge in questions regarding prenatal sex hormone effects on gender development,
which includes characteristics that show sex differences and that relate to being female or male.
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Foundation
Human work linking hormones and behavior borrows heavily from work in nonhuman species
showing that exposure to sex hormones early in development has permanent effects on sexrelated behavior, and reproductive anatomy and function [reviewed in 1,2,3]. Thus, early
development represents a sensitive period for hormones to organize the brain.1 Studying prenatal
hormonal influences on gender development is challenging: hormones cannot be manipulated
experimentally, and human behavior is strongly influenced by social context.
Fortunately, several methods are available to meet these challenges, as shown in Table 1.
Evidence using those methods has accrued to demonstrate that levels of androgens during
prenatal development are related (in varying degrees) to characteristics that show sex
differences; this evidence is described in recent reviews [4–6], and summarized in Table
2 (Column 1). Recent progress, discussed below and summarized in Table 2 (Column 2), has
examined the limits of the effects, and considered the psychological and neural mechanisms
mediating them. Ongoing and planned work involves expansion of those themes, novel methods,
and incorporation of recent lessons from animal studies. Given the challenges of studying these
questions, this field moves more slowly than many others, so we extend our review beyond the
past two years.
Table 1
Key Methods for Studying Androgen Effects on Gender Development
Natural
Experiments
Strengths
Limitations
Used to Study
Congenital Adrenal
Separation of prenatal
Physical virilization
Prenatal androgens
Hyperplasia (CAH)
androgens and rearing
Abnormalities in other hormones
versus rearing in girls
(social) sex in girls
(e.g., glucocorticoids)
and women
Complete Androgen
Separation of prenatal
Confounding of androgens and
Prenatal androgens
Insensitivity
androgens and sex
rearing (social) sex (both female-
versus genes on the sex
Syndrome (CAIS)
chromosomes
typical)
chromosomes
Typical Samples
Strengths
Limitations
Used to Study
Amniotic Hormones
Natural variations in
Single sample of hormones at
Effects of within-sex
Opposite-Sex Twins
hormones No confounding varying gestational ages Selected
variations in prenatal
disease factors
sample
hormones
Natural variations in
Unclear whether and how
Effects of within-sex
hormones No confounding hormones transferred between
disease factors
fetuses Twins share postnatal
social environment
variations in prenatal
hormones
Genital Anatomy
Natural variations in
No direct evidence linking
Effects of within-sex
androgens Measured
anatomy to prenatal androgens in
variations in prenatal and
postnatally
human beings
early postnatal
androgens
Digit Ratio
Easy to measure Differs in
Does not reflect within-sex
Should not be used
groups known to differ in
variation in prenatal androgen
prenatal androgen
exposure
exposure
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Table 2
Summary of Prenatal Androgen Effects on Gender Development
Reviewed in 2011
Effect
Confirmed in Recent Studies?
Evidence
Size
Activity Interests &
large
Participation
Gender Identity
small
Effect
Evidence
Size
Source
Strength
Natural Expt
+++
Amniotic T
++
Natural Expt
+++
large
small
Source
Strength
Natural Expt
+++
Amniotic T
—
Natural Expt
+++
Reviewed in 2011
Effect
Confirmed in Recent Studies?
Evidence
Size
Sexual Orientation
moderate
Effect
Evidence
Size
Source
Strength
Natural Expt
+++
Source
Natural
Strength
—
Expt
Spatial Abilities
small-
Natural Expt
++
small-
Natural
+++
moderate
OS twins
+
moderate
Expt
++
OS Twins
+
Amniotic
T
Psychopathology:
“Autistic” Traits
Autism Diagnosis
moderate
Natural Expt
+
Amniotic T
+
large
Amniotic T
+
no effect
Natural Expt
+
Reviewed in 2011
Effect
Confirmed in Recent Studies?
Evidence
Size
Effect
Evidence
Size
Source
Strength
Source
Strength
Substance Use
small
OS Twins
+
Disordered Eating
small-
OS Twins
+
moderate
Modified from [4].
Source (of evidence): Natural Expt: Natural experiments (e.g., CAH); Amniotic T: Typical samples with direct
measure of testosterone in amniotic fluid; OS Twins: Typical samples of opposite versus same-sex twins
Strength (of evidence), based on number of studies and ability to infer causation about androgen from design (e.g.,
more weight given to data from natural experiments than twins): + weak; ++ moderate; +++ strong; — insufficient
new evidence
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Nature and Psychological Mechanisms of Prenatal Androgen Effects on
Gendered Behavior
Confidence has increased that early androgens affect gender development, in light of recent
studies that confirm, extend, and clarify previous findings. Most promising, research has moved
from asking whether hormones influence human behavior to asking how they do so.
Activity interests and participation – from childhood toy preferences to adult hobbies and
occupations – continue to be strongly linked to prenatal androgen exposure [e.g., 7,8], with two
notable recent findings. First, androgen effects on interest and engagement in male-typed
occupations was seen to have economic consequences: women with exposure to high levels of
prenatal androgens due to congenital adrenal hyperplasia (CAH) were more likely than controls
to have income in the top 20th percentile, reflecting employment in male-typical, higher-paying
jobs (despite having lower education, and more psychosocial problems) [9]. Second, the
sensitive period for androgen effects on activity interests was extended to the early postnatal
months, as seen in links between parent-reported child play and urinary testosterone during the
first six postnatal months [10], and penile length at a similar time (marking the postnatal
testosterone surge also known as mini-puberty) [11].
Speculations about the affective and cognitive processes that underlie children’s sextyped toy
preferences have been stimulated by evidence that those preferences are paralleled in rhesus
monkeys (male monkeys, like boys, strongly preferred wheeled toys, whereas female monkeys,
like girls, had variable preferences, leading to sex differences in preference for wheeled versus
plush toys) [12, 13]. Recent work has documented early sex differences in propulsive movement
(hitting versus cradling an object), with sex-typed activities suggested to develop “from
socialization mechanisms that build on a male predisposition to imitate propulsive motion” [14,
p. 262]. Furthermore, sex differences in occupational choices (e.g., male-predominance in
science and engineering, female-predominance in social service) appear to be driven in part by
androgen effects on interest in things versus people [15].
Spatial abilities are facilitated by exposure to high levels of prenatal androgens. Performance on
several spatial tests was higher in two samples of females with CAH compared to typical females
[16,17]. Inconsistencies in early studies were clarified: androgen facilitation of spatial abilities
may be countered by adverse effects of the disease during early life [17]. Converging evidence
comes from typical samples. Spatial abilities were positively related to amniotic testosterone in
girls for one measure, but not two others, perhaps due to small sample [18]. Spatial performance
was also higher in females with a male co-twin than a female co-twin, thought to reflect transfer
of testosterone during gestation [19,20]; importantly, one study controlled for postnatal
socialization effects by showing that females with a (non-twin) brother did not have better spatial
ability than those with a sister [19].
Sex-related psychiatric disorders are suggested to result, in part, from sex hormones. Prenatal
androgens have been invoked to explain male predominance of externalizing disorders, such as
attention-deficit hyperactivity disorder (ADHD) [e.g., 21] and substance use, and of autism
[e.g., 22]; it is not specified when prenatal androgens trigger ADHD or autism, although genes
presumably play a role. Population registry-based studies of psychiatric morbidity in individuals
with CAH in Sweden produced results not easily reconciled with early androgen effects.
Although girls and women with CAH had a higher rate of substance misuse than female controls,
the rate was also higher than male controls; moreover, other conditions that show female
predominance (stress and adjustment disorders) were increased, but ADHD and autism spectrum
disorders were not [23]. Boys and men with CAH also had higher rates of psychiatric disorder
than controls [24].
Overall, the increased psychopathology seen in males and females with CAH reflects the
limitations of natural experiments (i.e., other disease factors contribute to behavior), so it is
important to note indirect evidence for prenatal androgen effects on some forms of sex-related
psychopathology. Consistent with male predominance of substance use and female
predominance of disordered eating, females with a male co-twin had more alcohol use [25,26],
and less disordered eating [27] than females with a female co-twin; importantly, these studies
included siblings to control for postnatal environmental effects. “Autistic” traits were associated
with amniotic testosterone [28], but interpretation is not simple because some traits show sex
differences in the normal range and would be expected to relate to prenatal hormones for that
reason.
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Neural Substrates of Prenatal Androgen Effects on Gendered Behavior
Neuroimaging has come to human behavioral neuroendocrinology, as to other areas of
behavioral science, with increasing interest in aspects of brain anatomy and activation that are
related to sex and sex hormones [reviewed and discussed in 29]. In a magnetic resonance
imaging (MRI) study of typical boys aged 8–11, brain structures that show sex differences were
examined in relation to amniotic testosterone, with effects for regional gray matter volume in
some areas, but not to midsaggital corpus callosum size [30,31]. The behavioral significance of
the effects is not clear (anatomy was not examined in relation to behavior). It is also unclear why
girls were not studied since they were included in other aspects of the study linking amniotic
testosterone to behavior.
Brain activation patterns during cognitive and affective tasks were also examined in relation to
prenatal androgens in natural experiments and a typical sample, with most using functional MRI.
(Few studies considered potential confounding effects of postnatal androgens.) Evidence for
androgen effects on two aspects of sex-typed brain responses comes from women with complete
androgen insensitivity syndrome (CAIS) who have a Y chromosome but do not have effective
androgen exposure (due to lack of functional androgen receptors). In two separate samples,
women with CAIS had female-typical brain responses to mental rotation [32] and to sexuallyarousing stimuli [33]; their brain activation patterns were different than those of men and similar
to those of typical women, consistent with their low androgen responsiveness and not with
possessing a Y chromosome.
Other studies linking androgens to brain activation were not as clear. For example, in a positron
emission tomography study, women with and without CAH did not differ in neural response to
olfactory stimuli [34].
Several studies focused on characteristics related to psychopathology, consistent with the
approach of understanding psychiatric disorders in terms of underlying dimensions of observable
behavior and neurobiology [35–37]. For example, the male predominance of childhood-onset
externalizing problems suggests that early androgens masculinize reward systems. In one set of
studies focused on emotion in faces [38,39], girls with CAH had greater amygdala activation
while viewing negative facial emotions and less hippocampal activation while recalling
emotional faces than did typical girls, but the groups also differed in performance. In a study of
typical boys (those whose structure was described above), amniotic testosterone was linked to
striatal responses to valenced facial cues, and to behavioral approach (on a questionnaire
measure of impulsivity/fun-seeking, drive, and reward responsivity) through striatal activity (but
not directly to behavioral approach, perhaps due to low statistical power) [40]. Interpretation
would have been enhanced with data from girls to evaluate sex differences and because
testosterone is often seen to have within-sex effects in females [4].
Overall, the zeal for neuroimaging studies has yet to be matched by findings, with few clear and
consistent patterns regarding androgen effects on brain structure and activation. Advances will
likely come from studying neural systems underlying sex-related behavior and likely to be
influenced by androgens, and directly linking brain measures to behavior. But, links between
hormones and neural systems do not necessarily imply causality; for example, a brain region
may be larger or more active during a specific task in women with versus without CAH simply
because that region changes in response to behavior or environmental input that differs between
the groups. Furthermore, a given behavioral endpoint may emerge through a variety of
trajectories; androgens may affect the path to an outcome but not necessarily the outcome itself
(the sexes may get to the same outcome through different paths) [e.g., 41].
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Ongoing Work & Future Directions
This is an exciting time to study how hormones shape gender development. The field is poised
for some significant advances, and we highlight topics that represent opportunities based on
animal studies, tantalizing recent findings noted above, and related trends in other areas of
science.
First, there is need to understand variations in androgen effects across behaviors and across
people. For example, why is gender identity less affected by early androgens than are activity
interests; what differentiates the women with CAH who are bisexual from the majority who are
heterosexual; why would high prenatal androgen levels produce autism in some children, ADHD
in others, and normal development in most?
Second, findings from animal studies [e.g., 41–46] can be used to guide work in human beings,
as illustrated with some examples. The importance of later sensitive periods for hormone effects,
such as puberty and pregnancy [e.g., 43, 46] might be tested in studies of cognition and affect in
children receiving drugs to suppress puberty because of precocious puberty or gender identity
concerns, and in women raising biological versus adopted children (the latter differentiates
changes due to pregnancy hormones from childrearing). The evidence for a behavioral role of
genes on the sex chromosomes [e.g., 42,45] can be extended to human behavior by studying
women with CAIS. The notion that the sexes use different paths to get to the same outcome
[e.g., 41] might be understood through studies combining neuroimaging and behavioral
measures, e.g., identifying sex differences in links between brain activation during a cognitive
task and performance on a related task outside the scanner.
Third, it is important to pursue additional windows into prenatal androgen exposure. Natural
experiments, particularly CAH and CAIS, have yielded valuable data, but they are not perfect.
(Unfortunately, most criticisms [e.g., 47] are narrow, ignore the consistency of the evidence, and
fail to capture the difference between cause and effect [discussed in 48]). Methods involving
direct measures of prenatal hormones (e.g., from amniotic fluid) have both promise and pitfalls
[49]. Importantly, most methods relying on indirect indicators of prenatal hormones create more
confusion than clarification. It is time to stop using digit ratio to mark variations in prenatal
androgen exposure because such use is not supported by evidence [as detailed
elsewhere, 50,51,52]. For example, in one study [50], women with CAIS who have no effective
androgen exposure had only moderately feminized digit ratio compared to men, were not
significantly different from typical women (who have some effective androgen exposure), and
showed variability in digit ratio despite minimal variability in androgen exposure; furthermore,
digit ratios did not even provide high discrimination between control men and women, despite
the marked sex difference in prenatal androgen exposure. It is necessary to obtain validity data
on other purported markers, such as otoacoustic emissions, before using them on a large scale
[53].
Promising measures include aspects of genital anatomy, which reflect early androgen action, and
thus are likely to relate to later behavior in people as they do in nonhuman animals. Anogenital
distance reflects prenatal androgen exposure [54–57], although it may be modified by postnatal
androgen [58], and has been linked to boys’ parent-reported play in one study [11]. Penile length,
especially change during the first months of life, may mark the early postnatal testosterone surge
in boys, and has also been linked to parent-reported play [5,11].
Fourth, we need to understand how hormones work jointly with socialization to influence gender
development [48]. Children are socialized in ways that reflect their characteristics, and the social
world does not affect all children equally with regard to gender development [e.g., 59,60]. Girls
with CAH provide a unique opportunity to uncouple effects on gender development of biological
and rearing sex, to ask how girls with CAH are socialized (e.g., whether they are socialized in
female-typical ways consistent with their rearing sex and identity, or in atypical ways in relation
to their masculinized activity interests), and whether socialization has different effects on girls
with and without CAH [8,48,61]. This question is ideally suited for biomarkers: imagine what
we could learn if we could easily identify children at birth in terms of their early androgen
exposure and then study how they elicit different socialization and respond differently to the
same socialization.
These questions represent pieces of the large puzzle to identify the neural, psychological, and
developmental paths linking prenatal androgens to behavior, and studying how varying
trajectories develop from the interplay of hormones and the social environment at different
sensitive periods, as represented in Figure 1. The figure highlights the hypothesized biological
and psychosocial contributors to gender development, and how different paths can lead to similar
endpoints; for example, male-typed activity interests may result primarily from increased
exposure to prenatal androgens for some girls (such as those with CAH), but from gendered
socialization experiences for other girls. The figure also calls attention to the interplay between
biological and social processes, and the psychological and neural mechanisms that mediate links
between causes and outcomes. But, empirical evidence is needed to test most of the paths in the
figure; most extant data concern simple links between behavior and prenatal androgens or
gendered socialization.
Figure 1
Simple process model delineating the link between prenatal androgens and sex-typed behaviors (gray
boxes) by considering neural and psychological mediators of the link and including the influence of
gendered socialization (white boxes) on the process. Path magnitudes change with development and vary
for different behaviors, contexts, and individuals.
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Relevance to Important Psychological Questions
There are broad implications of identifying how hormones shape gender development, as
illustrated in Figure 1. Sex and gender are crucial to identity and a range of characteristics,
psychological and physical, in health and disease [62,63]. Prenatal programming provides a
window into development and, ultimately, an opportunity to facilitate optimal development
[e.g., 64,65]. Gender development clearly represents the interplay of biology and socialization,
so provides a nice model for psychological development more broadly. We illustrate with several
examples.
First, sex matters for mental illness susceptibility, prevalence, age of onset, and form. It is likely
that understanding how hormones contribute to sex-related psychopathology will provide
information fundamental to the development of personalized interventions [35–37].
Second, controversy surrounds the causes of women’s underrepresentation in science, math,
engineering, and technology (STEM) careers [e.g., 66,67]. There is little doubt that social
structure (e.g., discrimination, child care policies) contributes to the problem [e.g., 68], but it is
likely that sex differences in interests also play a role. Prenatal androgen effects on the tendency
to prefer careers that involve things versus people [15] reinforce other suggestions [69,70] that
women might be engaged by STEM when emphasis is placed on its social relevance.
Third, optimal care of children with variations in gender expression (e.g., disorders of sex
development, transgender identity) requires more evidence on the ways that hormones are
modified by genes and social factors, best studied in systematic, long-term follow-up studies
[71]. A pressing question concerns the development and causes of gender identity: it is not
simply related to prenatal androgens [as confirmed recently, 72,73], and appears to be plastic,
with adolescence a key period for the development of nonnormative identity [74].
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Conclusions
Work on hormonal influences on gender development provides a nice model for understanding
psychological development in general. Identifying mechanisms by which sex and gender matter
can tell us about the ways that the prenatal environment primes us to elicit and respond to our
social worlds, and how our biology and experiences transact across development to shape brain
structure and function that guide behavior.
Highlights
Prenatal androgens influence sex-related characteristics to varying degrees
Androgens facilitate male-typed activities through interest in things vs. people
Androgens are associated with some aspects of brain structure and activation
Current work is focused on interplay of hormones and social environment
Relevant to questions regarding sex-related psychopathology, prenatal programming
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Acknowledgements
Funding for our research was provided by grants from the National Institutes of Health
HD19644, HD044398, HD057930, and MH099617. Adriene Beltz is currently supported by
National Science Foundation grant 1157220.
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Footnotes
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1
In nonhuman and human primates, androgens facilitate masculinization during the prenatal period
[reviewed in 3,75]. Estrogens probably do not have effects during prenatal development because both
sexes are exposed to estrogens from the mother [76], but they may have effects at later sensitive periods.
Therefore, our terminology reflects the focus on androgens, while acknowledging the potential role for
estrogens (and perhaps other hormones) at other periods.
Conflict of Interest
Nothing declared
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