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Sex-related variation in human behavior and the brain

2010; Elsevier BV; Volume: 14; Issue: 10 Linguagem: Inglês

10.1016/j.tics.2010.07.005

1879-307X

Melissa Hines,

Neuroendocrine regulation and behavior

Male and female fetuses differ in testosterone concentrations beginning as early as week 8 of gestation. This early hormone difference exerts permanent influences on brain development and behavior. Contemporary research shows that hormones are particularly important for the development of sex-typical childhood behavior, including toy choices, which until recently were thought to result solely from sociocultural influences. Prenatal testosterone exposure also appears to influence sexual orientation and gender identity, as well as some, but not all, sex-related cognitive, motor and personality characteristics. Neural mechanisms responsible for these hormone-induced behavioral outcomes are beginning to be identified, and current evidence suggests involvement of the hypothalamus and amygdala, as well as interhemispheric connectivity, and cortical areas involved in visual processing. Male and female fetuses differ in testosterone concentrations beginning as early as week 8 of gestation. This early hormone difference exerts permanent influences on brain development and behavior. Contemporary research shows that hormones are particularly important for the development of sex-typical childhood behavior, including toy choices, which until recently were thought to result solely from sociocultural influences. Prenatal testosterone exposure also appears to influence sexual orientation and gender identity, as well as some, but not all, sex-related cognitive, motor and personality characteristics. Neural mechanisms responsible for these hormone-induced behavioral outcomes are beginning to be identified, and current evidence suggests involvement of the hypothalamus and amygdala, as well as interhemispheric connectivity, and cortical areas involved in visual processing. Why do males and females differ behaviorally? Certainly, there is much differential socialization of the sexes, but is there an inborn element as well? Darwin's sexual selection theory [1Darwin C. The Descent of Man and Selection in Relation to Sex. John Murray, 1871Crossref Google Scholar] suggests that competition for mates and discriminative mate choices have shaped the evolution of sex differences [2Geary D.C. Male, Female: the Evolution of Human Sex Differences. APA Press, 2010Crossref Google Scholar]. Efforts to apply this theory to understanding sex differences in human behavior have been controversial [3Laland K.N. Brown G. Sense and Nonsense: Evolutionary Perspectives on Human Behavior. Oxford University Press, 2002Google Scholar], and because they are distal explanations of behavior, evolutionary theories can be difficult to subject to direct scientific scrutiny. However, whatever distal genetic forces have shaped the evolution of human sex differences, they appear to act through proximal mechanisms that can be evaluated more directly. Prominent among these mechanisms are differences in the amount of testosterone to which male and female fetuses are exposed. The hypothesis that prenatal testosterone influences human neural and behavioral development derives from thousands of experimental studies in non-human mammals. In these studies, animals are assigned at random to various hormonal manipulations during critical periods of early development and influences on brain and behavior are observed (Box 1). These studies show that prenatal or neonatal levels of gonadal hormones are a major determinant of sex differences in brain development and in subsequent behavior, with direct genetic effects playing a smaller role. The hypothesis that hormones exert similar influences on human neurobehavioral development has been debated, but recent studies provide convincing evidence that prenatal androgen exposure influences children's sex-typed play behavior. In addition, there is growing evidence that other behaviors that show sex differences, including sexual orientation, core gender identity, personality characteristics and motor performance are similarly influenced, and the neural underpinnings of these hormonal influences on behavior are being identified. This article reviews evidence substantiating the role of testosterone in the development of children's sex-typed behavior, discusses other behaviors that appear to be similarly influenced by prenatal testosterone exposure, and considers neural mechanisms that could mediate these effects.Box 1Gonadal hormones organize the mammalian brain during early development; after puberty, they activate previously organized neural systemsThousands of studies have manipulated hormones during early development in non-human mammals and assessed the impact of these manipulations on brain structure and behavior later in life. These studies have included species ranging from rodents, such as rats, mice and guinea pigs, to non-human primates, such as rhesus monkeys. Across all these species, early levels of testosterone and hormones produced from testosterone, shape brain development in regions with receptors for these hormones. Because these hormonal influences are written into the structure of the brain, they manifest in behavior across the lifespan.For instance, the female offspring of rhesus monkeys treated with testosterone during pregnancy show increased male-typical, rough-and-tumble play as juveniles, and increased male-typical and reduced female-typical sexual behavior as adults [73Goy R.W. McEwen B.S. Sexual Differentiation of the Brain. MIT Press, 1980Google Scholar]. Similar effects are seen in rats, both for play behavior and for sexual behavior. These hormone treatments also influence neural structure, enlarging brain regions that are larger in males, and reducing those that are larger in females [12McCarthy M.M. et al.Sexual differentiation of the brain: mode, mechanisms, and meaning.in: Pfaff D.W. Hormones, Brain and Behavior. 2nd edn. Academic Press, 2009: 1707-1744Crossref Scopus (61) Google Scholar]. In rodents, structures thought to be involved in sexual behavior, such as the sexually-dimorphic nucleus of the preoptic area (SDN-POA) and the bed nucleus of the stria terminalis (BNST), are affected, as is the medial amygdala, a region linked to rough-and-tumble play [12McCarthy M.M. et al.Sexual differentiation of the brain: mode, mechanisms, and meaning.in: Pfaff D.W. Hormones, Brain and Behavior. 2nd edn. Academic Press, 2009: 1707-1744Crossref Scopus (61) Google Scholar, 23Hines M. Brain Gender. Oxford University Press, 2004Google Scholar]. In research in non-human mammals, experimental techniques, such as castration and hormone replacement, are used to control the adult hormone environment, allowing separation of the early and permanent, organizational effects of hormones on brain and behavior from the later and transient, activational effects of hormones that occur after puberty [23Hines M. Brain Gender. Oxford University Press, 2004Google Scholar, 73Goy R.W. McEwen B.S. Sexual Differentiation of the Brain. MIT Press, 1980Google Scholar]. Similar adult manipulations are not possible in humans, making pre-pubertal behaviors, such as childhood toy preferences, particularly attractive for studying organizational influences of hormones on human behavior. Thousands of studies have manipulated hormones during early development in non-human mammals and assessed the impact of these manipulations on brain structure and behavior later in life. These studies have included species ranging from rodents, such as rats, mice and guinea pigs, to non-human primates, such as rhesus monkeys. Across all these species, early levels of testosterone and hormones produced from testosterone, shape brain development in regions with receptors for these hormones. Because these hormonal influences are written into the structure of the brain, they manifest in behavior across the lifespan. For instance, the female offspring of rhesus monkeys treated with testosterone during pregnancy show increased male-typical, rough-and-tumble play as juveniles, and increased male-typical and reduced female-typical sexual behavior as adults [73Goy R.W. McEwen B.S. Sexual Differentiation of the Brain. MIT Press, 1980Google Scholar]. Similar effects are seen in rats, both for play behavior and for sexual behavior. These hormone treatments also influence neural structure, enlarging brain regions that are larger in males, and reducing those that are larger in females [12McCarthy M.M. et al.Sexual differentiation of the brain: mode, mechanisms, and meaning.in: Pfaff D.W. Hormones, Brain and Behavior. 2nd edn. Academic Press, 2009: 1707-1744Crossref Scopus (61) Google Scholar]. In rodents, structures thought to be involved in sexual behavior, such as the sexually-dimorphic nucleus of the preoptic area (SDN-POA) and the bed nucleus of the stria terminalis (BNST), are affected, as is the medial amygdala, a region linked to rough-and-tumble play [12McCarthy M.M. et al.Sexual differentiation of the brain: mode, mechanisms, and meaning.in: Pfaff D.W. Hormones, Brain and Behavior. 2nd edn. Academic Press, 2009: 1707-1744Crossref Scopus (61) Google Scholar, 23Hines M. Brain Gender. Oxford University Press, 2004Google Scholar]. In research in non-human mammals, experimental techniques, such as castration and hormone replacement, are used to control the adult hormone environment, allowing separation of the early and permanent, organizational effects of hormones on brain and behavior from the later and transient, activational effects of hormones that occur after puberty [23Hines M. Brain Gender. Oxford University Press, 2004Google Scholar, 73Goy R.W. McEwen B.S. Sexual Differentiation of the Brain. MIT Press, 1980Google Scholar]. Similar adult manipulations are not possible in humans, making pre-pubertal behaviors, such as childhood toy preferences, particularly attractive for studying organizational influences of hormones on human behavior. Why study sex differences in children's play? First, children spend the majority of their waking life playing, producing interest in the causes and consequences of individual differences in play preferences. Second, there are large sex differences in children's play, including in preferences for toys, such as dolls and trucks (Box 2). Third, children's play behavior can be assessed readily and reliably. Fourth, sex differences in children's play are evident early in life, providing scope for influence on subsequent behavior, and during a period of hormonal quiescence, allowing examination of the permanent, organizational influences of hormones on brain development before the transient, activational influences of hormones in adulthood have begun (Box 1).Box 2What human behaviors show sex differences and how large are these differences?Sex differences in core gender identity, sexual orientation and childhood play are larger than those in cognition or personality, and are larger than the familiar sex difference in height (Table I).Table IThe sizes of sex differences in human behavior/psychological characteristics that have been studied in relation to the early hormone environmentBehavior/psychological characteristicApproximate size in standard deviation units (d)Core gender identity 23Hines M. Brain Gender. Oxford University Press, 2004Google Scholar, 74Deogracias J.J. et al.The gender identity/gender dysphoria questionnaire for adolescents and adults.J. Sex Res. 2007; 44: 370-379Crossref PubMed Scopus (170) Google Scholar11.0–13.2Sexual orientation 24Hines M. et al.Androgen and psychosexual development: core gender identity, sexual orientation and recalled childhood gender role behavior in women and men with congenital adrenal hyperplasia (CAH).J. Sex Res. 2004; 41: 75-81Crossref PubMed Scopus (276) Google Scholar, 75Meyer-Bahlburg H.F.L. et al.Gender development in women with Congenital Adrenal Hyperplasia as a function of disorder severity.Arch. Sex Behav. 2006; 35: 667-684Crossref PubMed Scopus (164) Google Scholar6.0–7.0Childhood playPlay with girls' toys 8Pasterski V.L. et al.Prenatal hormones and postnatal socialization by parents as determinants of male-typical toy play in girls with congenital adrenal hyperplasia.Child Dev. 2005; 76: 264-278Crossref PubMed Scopus (186) Google Scholar1.8Play with boys' toys 8Pasterski V.L. et al.Prenatal hormones and postnatal socialization by parents as determinants of male-typical toy play in girls with congenital adrenal hyperplasia.Child Dev. 2005; 76: 264-278Crossref PubMed Scopus (186) Google Scholar2.1Feminine preschool games 76Zucker K.J. Measurement of psychosexual differentiation.Arch. Sex Behav. 2005; 34: 375-388Crossref PubMed Scopus (104) Google Scholar1.1Masculine preschool games 76Zucker K.J. Measurement of psychosexual differentiation.Arch. Sex Behav. 2005; 34: 375-388Crossref PubMed Scopus (104) Google Scholar0.7–1.8Playmate preferences 76Zucker K.J. Measurement of psychosexual differentiation.Arch. Sex Behav. 2005; 34: 375-388Crossref PubMed Scopus (104) Google Scholar2.3–5.6Composite of sex-typed play (PSAI) 77Golombok S. et al.Developmental trajectories of sex-typed behavior in boys and girls: a longitudinal general population study of children aged 2.5-8 years.Child Dev. 2008; 79: 1583-1593Crossref PubMed Scopus (92) Google Scholar, 78Hines M. et al.Prenatal stress and gender role behavior in girls and boys: a longitudinal, population study.Horm. Behav. 2002; 42: 126-134Crossref PubMed Scopus (50) Google Scholar2.7–3.2Cognitive and motor abilities (adolescents/adults)Targeting 37Hines M. et al.Spatial abilities following prenatal androgen abnormality: Targeting and mental rotations performance in individuals with congenital adrenal hyperplasia (CAH).Psychoneuroendocrinology. 2003; 28: 1010-1026Abstract Full Text Full Text PDF PubMed Scopus (182) Google Scholar, 38Collaer M.L. et al.Motor development in individuals with congenital adrenal hyperplasia: Strength, targeting, and fine motor skill.Psychoneuroendocrinology. 2009; 34: 249-258Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar, 79Jardine R. Martin N.G. Spatial ability and throwing accuracy.Behav. Genet. 1983; 13: 331-340Crossref PubMed Scopus (47) Google Scholar, 80Watson N.V. Kimura D. Right-hand superiority for throwing but not for intercepting.Neuropsychologia. 1989; 27: 1399-1414Crossref PubMed Scopus (75) Google Scholar, 81Watson N.V. Kimura D. Nontrivial sex differences in throwing and intercepting: relation to psychometrically-defined spatial functions.Personality Individual Differences. 1991; 12: 375-385Crossref Scopus (135) Google Scholar1.1–2.0Fine motor skill 38Collaer M.L. et al.Motor development in individuals with congenital adrenal hyperplasia: Strength, targeting, and fine motor skill.Psychoneuroendocrinology. 2009; 34: 249-258Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar, 82Strauss E. et al.A Compendium of Neuropsychological Tests. Oxford University Press, 2006Google Scholar, 83Yeudall L.T. et al.Normative data stratified by age and sex for 12 neuropsychological tests.J. Clin. Psychol. 1986; 42: 918-946Crossref Scopus (155) Google Scholar0.5–0.6Mental rotations 84Linn M.C. Petersen A.C. Emergence and characterization of sex differences in spatial ability: a meta-analysis.Child Dev. 1985; 56: 1479-1498Crossref PubMed Google Scholar, 85Voyer D. et al.Magnitude of sex differences in spatial abilities: a meta-analysis and consideration of critical variables.Psychol. Bull. 1995; 117: 250-270Crossref PubMed Scopus (2051) Google Scholar0.3–0.9Spatial perception 84Linn M.C. Petersen A.C. Emergence and characterization of sex differences in spatial ability: a meta-analysis.Child Dev. 1985; 56: 1479-1498Crossref PubMed Google Scholar, 85Voyer D. et al.Magnitude of sex differences in spatial abilities: a meta-analysis and consideration of critical variables.Psychol. Bull. 1995; 117: 250-270Crossref PubMed Scopus (2051) Google Scholar0.3–0.6Spatial visualization 84Linn M.C. Petersen A.C. Emergence and characterization of sex differences in spatial ability: a meta-analysis.Child Dev. 1985; 56: 1479-1498Crossref PubMed Google Scholar, 85Voyer D. et al.Magnitude of sex differences in spatial abilities: a meta-analysis and consideration of critical variables.Psychol. Bull. 1995; 117: 250-270Crossref PubMed Scopus (2051) Google Scholar0.0–0.6SAT mathematics 86Hyde J.S. et al.Gender differences in mathematics performance: a meta-analysis.Psychol. Bull. 1990; 107: 139-155Crossref PubMed Scopus (1101) Google Scholar0.4Computational skills 86Hyde J.S. et al.Gender differences in mathematics performance: a meta-analysis.Psychol. Bull. 1990; 107: 139-155Crossref PubMed Scopus (1101) Google Scholar0.0Math concepts 86Hyde J.S. et al.Gender differences in mathematics performance: a meta-analysis.Psychol. Bull. 1990; 107: 139-155Crossref PubMed Scopus (1101) Google Scholar0.0Verbal fluency 87Kolb B. Whishaw I.Q. Fundamentals of Human Neuropsychology. W.H. Freeman and Co, 1985Google Scholar, 88Spreen O. Strauss E. A Compendium of Neuropsychological Tests. Oxford University Press, 1991Google Scholar0.5Perceptual speed 89Feingold A. Cognitive gender differences are disappearing.Am. Psychologist. 1988; 43: 95-103Crossref Scopus (355) Google Scholar0.3–0.7Vocabulary 90Hyde J.S. Linn M.C. Gender differences in verbal ability: a meta-analysis.Psychol. Bull. 1988; 104: 53-69Crossref Scopus (1024) Google Scholar0.0SAT Verbal 90Hyde J.S. Linn M.C. Gender differences in verbal ability: a meta-analysis.Psychol. Bull. 1988; 104: 53-69Crossref Scopus (1024) Google Scholar0.0Personality (assessed with questionnaires)Tendencies to physical aggression 35Pasterski V.L. et al.Increased aggression and activity level in 3- to 11-year-old girls with congenital adrenal hyperplasia (CAH).Horm. Behav. 2007; 52: 368-374Crossref PubMed Scopus (113) Google Scholar, 91Hyde J.S. How large are gender differences in aggression? A developmental meta-analysis.Dev. Psychol. 1984; 20: 722-736Crossref Scopus (317) Google Scholar0.4–1.3Empathy 34Chapman E. et al.Fetal testosterone and empathy: Evidence from the Empathy Quotient (EQ) and the 'Reading the mind in the eyes' test.Soc. Neurosci. 2006; 1: 135-148Crossref PubMed Scopus (254) Google Scholar, 92Feingold A. Gender differences in personality: a meta-analysis.Psychol. Bull. 1994; 116: 429-456Crossref PubMed Scopus (1398) Google Scholar0.3–1.3Dominance/assertiveness 92Feingold A. Gender differences in personality: a meta-analysis.Psychol. Bull. 1994; 116: 429-456Crossref PubMed Scopus (1398) Google Scholar0.2–0.8 Open table in a new tab In addition, the sizes of gender differences in cognition and personality can vary across different measures of the same construct. In the realm of personality, sex differences assessed with the NEO, a measure of what are called the big five personality traits, tend to be smaller than those assessed with Cattell's 16 PF, a measure of 16 primary personality factors. These differences between tests can make sex differences seem smaller in meta-analyses that combine tests than they are on some individual tests [23Hines M. Brain Gender. Oxford University Press, 2004Google Scholar, 35Pasterski V.L. et al.Increased aggression and activity level in 3- to 11-year-old girls with congenital adrenal hyperplasia (CAH).Horm. Behav. 2007; 52: 368-374Crossref PubMed Scopus (113) Google Scholar]. Sex differences in some cognitive abilities seem to have declined over time [89Feingold A. Cognitive gender differences are disappearing.Am. Psychologist. 1988; 43: 95-103Crossref Scopus (355) Google Scholar]. For the SAT Mathematics, the sex ratio among those scoring at the upper extreme has declined from 13 boys to one girl in 1982 to 2.8 boys to one girl more recently [93Halpern D.F. et al.The science of sex differences in science and mathematics.Psychol. Sci. Public Interest. 2007; 8: 1-51Google Scholar]. Sex differences in some areas also grow larger or smaller with age. For instance the sex difference in childhood play increases from ages 2.5 to 5 years [77Golombok S. et al.Developmental trajectories of sex-typed behavior in boys and girls: a longitudinal general population study of children aged 2.5-8 years.Child Dev. 2008; 79: 1583-1593Crossref PubMed Scopus (92) Google Scholar], whereas the sex difference in physical aggression appears to be larger in children than in adults [91Hyde J.S. How large are gender differences in aggression? A developmental meta-analysis.Dev. Psychol. 1984; 20: 722-736Crossref Scopus (317) Google Scholar]. Sex differences in core gender identity, sexual orientation and childhood play are larger than those in cognition or personality, and are larger than the familiar sex difference in height (Table I).Table IThe sizes of sex differences in human behavior/psychological characteristics that have been studied in relation to the early hormone environmentBehavior/psychological characteristicApproximate size in standard deviation units (d)Core gender identity 23Hines M. Brain Gender. Oxford University Press, 2004Google Scholar, 74Deogracias J.J. et al.The gender identity/gender dysphoria questionnaire for adolescents and adults.J. Sex Res. 2007; 44: 370-379Crossref PubMed Scopus (170) Google Scholar11.0–13.2Sexual orientation 24Hines M. et al.Androgen and psychosexual development: core gender identity, sexual orientation and recalled childhood gender role behavior in women and men with congenital adrenal hyperplasia (CAH).J. Sex Res. 2004; 41: 75-81Crossref PubMed Scopus (276) Google Scholar, 75Meyer-Bahlburg H.F.L. et al.Gender development in women with Congenital Adrenal Hyperplasia as a function of disorder severity.Arch. Sex Behav. 2006; 35: 667-684Crossref PubMed Scopus (164) Google Scholar6.0–7.0Childhood playPlay with girls' toys 8Pasterski V.L. et al.Prenatal hormones and postnatal socialization by parents as determinants of male-typical toy play in girls with congenital adrenal hyperplasia.Child Dev. 2005; 76: 264-278Crossref PubMed Scopus (186) Google Scholar1.8Play with boys' toys 8Pasterski V.L. et al.Prenatal hormones and postnatal socialization by parents as determinants of male-typical toy play in girls with congenital adrenal hyperplasia.Child Dev. 2005; 76: 264-278Crossref PubMed Scopus (186) Google Scholar2.1Feminine preschool games 76Zucker K.J. Measurement of psychosexual differentiation.Arch. Sex Behav. 2005; 34: 375-388Crossref PubMed Scopus (104) Google Scholar1.1Masculine preschool games 76Zucker K.J. Measurement of psychosexual differentiation.Arch. Sex Behav. 2005; 34: 375-388Crossref PubMed Scopus (104) Google Scholar0.7–1.8Playmate preferences 76Zucker K.J. Measurement of psychosexual differentiation.Arch. Sex Behav. 2005; 34: 375-388Crossref PubMed Scopus (104) Google Scholar2.3–5.6Composite of sex-typed play (PSAI) 77Golombok S. et al.Developmental trajectories of sex-typed behavior in boys and girls: a longitudinal general population study of children aged 2.5-8 years.Child Dev. 2008; 79: 1583-1593Crossref PubMed Scopus (92) Google Scholar, 78Hines M. et al.Prenatal stress and gender role behavior in girls and boys: a longitudinal, population study.Horm. Behav. 2002; 42: 126-134Crossref PubMed Scopus (50) Google Scholar2.7–3.2Cognitive and motor abilities (adolescents/adults)Targeting 37Hines M. et al.Spatial abilities following prenatal androgen abnormality: Targeting and mental rotations performance in individuals with congenital adrenal hyperplasia (CAH).Psychoneuroendocrinology. 2003; 28: 1010-1026Abstract Full Text Full Text PDF PubMed Scopus (182) Google Scholar, 38Collaer M.L. et al.Motor development in individuals with congenital adrenal hyperplasia: Strength, targeting, and fine motor skill.Psychoneuroendocrinology. 2009; 34: 249-258Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar, 79Jardine R. Martin N.G. Spatial ability and throwing accuracy.Behav. Genet. 1983; 13: 331-340Crossref PubMed Scopus (47) Google Scholar, 80Watson N.V. Kimura D. Right-hand superiority for throwing but not for intercepting.Neuropsychologia. 1989; 27: 1399-1414Crossref PubMed Scopus (75) Google Scholar, 81Watson N.V. Kimura D. Nontrivial sex differences in throwing and intercepting: relation to psychometrically-defined spatial functions.Personality Individual Differences. 1991; 12: 375-385Crossref Scopus (135) Google Scholar1.1–2.0Fine motor skill 38Collaer M.L. et al.Motor development in individuals with congenital adrenal hyperplasia: Strength, targeting, and fine motor skill.Psychoneuroendocrinology. 2009; 34: 249-258Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar, 82Strauss E. et al.A Compendium of Neuropsychological Tests. Oxford University Press, 2006Google Scholar, 83Yeudall L.T. et al.Normative data stratified by age and sex for 12 neuropsychological tests.J. Clin. Psychol. 1986; 42: 918-946Crossref Scopus (155) Google Scholar0.5–0.6Mental rotations 84Linn M.C. Petersen A.C. Emergence and characterization of sex differences in spatial ability: a meta-analysis.Child Dev. 1985; 56: 1479-1498Crossref PubMed Google Scholar, 85Voyer D. et al.Magnitude of sex differences in spatial abilities: a meta-analysis and consideration of critical variables.Psychol. Bull. 1995; 117: 250-270Crossref PubMed Scopus (2051) Google Scholar0.3–0.9Spatial perception 84Linn M.C. Petersen A.C. Emergence and characterization of sex differences in spatial ability: a meta-analysis.Child Dev. 1985; 56: 1479-1498Crossref PubMed Google Scholar, 85Voyer D. et al.Magnitude of sex differences in spatial abilities: a meta-analysis and consideration of critical variables.Psychol. Bull. 1995; 117: 250-270Crossref PubMed Scopus (2051) Google Scholar0.3–0.6Spatial visualization 84Linn M.C. Petersen A.C. Emergence and characterization of sex differences in spatial ability: a meta-analysis.Child Dev. 1985; 56: 1479-1498Crossref PubMed Google Scholar, 85Voyer D. et al.Magnitude of sex differences in spatial abilities: a meta-analysis and consideration of critical variables.Psychol. Bull. 1995; 117: 250-270Crossref PubMed Scopus (2051) Google Scholar0.0–0.6SAT mathematics 86Hyde J.S. et al.Gender differences in mathematics performance: a meta-analysis.Psychol. Bull. 1990; 107: 139-155Crossref PubMed Scopus (1101) Google Scholar0.4Computational skills 86Hyde J.S. et al.Gender differences in mathematics performance: a meta-analysis.Psychol. Bull. 1990; 107: 139-155Crossref PubMed Scopus (1101) Google Scholar0.0Math concepts 86Hyde J.S. et al.Gender differences in mathematics performance: a meta-analysis.Psychol. Bull. 1990; 107: 139-155Crossref PubMed Scopus (1101) Google Scholar0.0Verbal fluency 87Kolb B. Whishaw I.Q. Fundamentals of Human Neuropsychology. W.H. Freeman and Co, 1985Google Scholar, 88Spreen O. Strauss E. A Compendium of Neuropsychological Tests. Oxford University Press, 1991Google Scholar0.5Perceptual speed 89Feingold A. Cognitive gender differences are disappearing.Am. Psychologist. 1988; 43: 95-103Crossref Scopus (355) Google Scholar0.3–0.7Vocabulary 90Hyde J.S. Linn M.C. Gender differences in verbal ability: a meta-analysis.Psychol. Bull. 1988; 104: 53-69Crossref Scopus (1024) Google Scholar0.0SAT Verbal 90Hyde J.S. Linn M.C. Gender differences in verbal ability: a meta-analysis.Psychol. Bull. 1988; 104: 53-69Crossref Scopus (1024) Google Scholar0.0Personality (assessed with questionnaires)Tendencies to physical aggression 35Pasterski V.L. et al.Increased aggression and activity level in 3- to 11-year-old girls with congenital adrenal hyperplasia (CAH).Horm. Behav. 2007; 52: 368-374Crossref PubMed Scopus (113) Google Scholar, 91Hyde J.S. How large are gender differences in aggression? A developmental meta-analysis.Dev. Psychol. 1984; 20: 722-736Crossref Scopus (317) Google Scholar0.4–1.3Empathy 34Chapman E. et al.Fetal testosterone and empathy: Evidence from the Empathy Quotient (EQ) and the 'Reading the mind in the eyes' test.Soc. Neurosci. 2006; 1: 135-148Crossref PubMed Scopus (254) Google Scholar, 92Feingold A. Gender differences in personality: a meta-analysis.Psychol. Bull. 1994; 116: 429-456Crossref PubMed Scopus (1398) Google Scholar0.3–1.3Dominance/assertiveness 92Feingold A. Gender differences in personality: a meta-analysis.Psychol. Bull. 1994; 116: 429-456Crossref PubMed Scopus (1398) Google Scholar0.2–0.8 Open table in a new tab In addition, the sizes of gender differences in cognition and personality can vary across different measures of the same construct. In the realm of personality, sex differences assessed with the NEO, a measure of what are called the big five personality traits, tend to be smaller than those assessed with Cattell's 16 PF, a measure of 16 primary personality factors. These differences between tests can make sex differences seem smaller in meta-analyses that combine tests than they are on some individual tests [23Hines M. Brain Gender. Oxford University Press, 2004Google Scholar, 35Pasterski V.L. et al.Increased aggression and activity level in 3- to 11-year-old girls with congenital adrenal hyperplasia (CAH).Horm. Behav. 2007; 52: 368-374Crossref PubMed Scopus (113) Google Scholar]. Sex differences in some cognitive abilities seem to have declined over time [89Feingold A. Cognitive gender differences are disappearing.Am. Psychologist. 1988; 43: 95-103Crossref Scopus (355) Google Scholar]. For the SAT Mathematics, the sex ratio among those scoring at the upper extreme has declined from 13 boys to one girl in 1982 to 2.8 boys to one girl more recently [93Halpern D.F. et al.The science of sex differences in science and mathematics.Psychol. Sci. Public Interest. 2007; 8: 1-51Google Scholar]. Sex differences in some areas also grow larger or smaller with age. For instance the s