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Relations Between Prenatal Testosterone and Cerebral Lateralization in Children

Authors:
Gina Grimshaw at Victoria University of Wellington
Gina Grimshaw
Philip Bryden at University of Waterloo
Philip Bryden
Jo-Anne Finegan
Jo-Anne Finegan
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Abstract

Several theorists have proposed that the sex steroid testosterone acts on the fetal brain during a critical period of development to influence cerebral lateralization (N. Geschwind & A. M. Galaburda, 1987; M. Hines & C. Shipley, see PA, Vol 71:8996; S. F. Witelson, see PA, Vol 79:26441. In the present study. relations were examined between prenatal testosterone levels in 2nd trimester amniotic fluid and lateralization of speech, affect, and handedness at age 10. Girls with higher prenatal testosterone levels were more strongly right-handed and had stronger left-hemisphere speech representation. Boys with higher prenatal testosterone levels had stronger right-hemisphere specialization for the recognition of emotion. This pattern of results is most consistent with Witelson's (1991) claim that prenatal testosterone leads to greater lateralization of function. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
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... There is ongoing debate around the effects of prenatal and postnatal hormones, particularly testosterone (T) on the lateralization of the developing brain (Grimshaw et al., 1995, Lust et al., 2011Hollier et al., 2014;Beking et al., 2018;Mercure et al., 2009;Pfannkuche et al., 2009). Because atypical lateralization is often present in lefthanders (Papadatou-Pastou, 2011), some have proposed that prenatal T exposure could influence handedness, though theories disagree on the predicted direction of the effect (see Papadatou-Pastou et al., 2017 andRichards et al., 2021 for reviews). ...
... The few studies conducted on the links between prenatal testosterone, handedness and laterality show mixed results (Grimshaw et al., 1995;Lust et al., 2011;Richards et al., 2021;Tan & Tan, 2001). As prenatal T is difficult to measure, some have used the ratio of the lengths of the 2nd and 4th digits of the hand (2D4D) as a proxy of prenatal testosterone exposure. ...
No association between adult sex steroids and hand preference in humans
Article
Full-text available
  • May 2021
Background: There is ongoing debate about the effects of hormones on the lateralization of the developing brain. In humans, there are conflicting theories of how testosterone during development should affect lateralization. Empirical studies linking prenatal and postnatal testosterone levels to hand preference (a proxy for lateralization) are similarly mixed. Links between hand preference and health may also suggest a mediating role of steroid hormones such as testosterone and estradiol. Studies to date of adult steroid hormones and handedness have been hindered by samples that contain small numbers of non-right-handers. Results: In the largest study of the phenomenon to date, I find that the testosterone (n = 7290) and estradiol (n = 3700) levels of left- and mixed-handed adults are no different to those of right-handers. All Bayesian 95% highest density intervals contained 0. Discussion and conclusions: The results have implications for studies that show elevated risk of hormonal-related mental and physical disorders in left-handed individuals.
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... Efforts to assess the second to fourth digit ratio (2D:4D) have extended to speci c sub-populations, including schizophrenia patients, with research revealing a distinct feminization of the ratio among Asian schizophrenia patients (Grimshaw et al., 1995;Jabeen et al. 2019). However, in our study, no feminization of the 2D:4D ratio was observed in schizophrenia patients when compared to healthy volunteers, even when strati ed by gender. ...
The Ulnar Left Second Digital Ridge Count Poorly Predicts the Risk for Schizophrenia
Preprint
Full-text available
  • May 2024
Background Anthropometric measurements, reflecting the interplay of nutritional, environmental, and genetic factors, are commonly used to study human physical traits. Despite previous research suggesting their potential as indicators of neurodevelopmental processes and genetic influences, their role in predicting schizophrenia risk remains uncertain. This study aims to address this gap by investigating the predictive value of the ulnar left second digital ridge count in assessing the risk for schizophrenia, contributing to our understanding of the association between anthropometric variables and schizophrenia risk. Method Digit lengths were measured from the basal crease of the digit to the fingertip using a digital sliding caliper (MicroMak, USA). A digital scanner (Digital Persona, China) was utilized to capture the fingerprint pattern. Ridge count was determined by counting the ridges diagonally within a 5 mm × 5 mm area on the fingertip surface, located on the radial and ulnar sides of the distal regions of each finger. Results The proportion of the loop fingerprint pattern (ulnar and radial) on the left fourth finger of schizophrenia patients was significantly higher than that observed among the healthy volunteers. Generally, a smaller 2D:4D ratio was observed among male schizophrenia patients compared to female schizophrenia patients. The ridge counts in the second and fourth digits were significantly different among the patients compared to the healthy volunteers, except for the radial ridge counts on the left second digit. Conclusion Despite the varying degrees of association observed between the assessed anthropometric variables and schizophrenia risk, the diagnostic performance of each variable, as evaluated through ROC curve analysis, was consistently poor. Overall, these findings suggest that the sensitivity and specificity of these measurements in effectively distinguishing the disease remain inadequate. Further research is warranted to explore additional predictive factors and improve diagnostic accuracy in schizophrenia risk assessment.
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... Richards et al. found that prenatal sex hormone exposure was not associated with the direction of hand preference in either males or females [96]. Other research has also failed to find a relationship between prenatal testosterone levels and the direction of lateralization in humans [97,98]. In a large study on human adults, there were also no differences in levels of testosterone and estradiol between left-, mixed-, and right-handers [99]. ...
Why Are Most Humans Right-Handed? The Modified Fighting Hypothesis
Article
Full-text available
  • Apr 2023
Humans show a population-level preference for using the right hand. The fighting hypothesis is an influential theory that suggests that left-handedness persists because its rarity provides a surprise advantage in fighting interactions, and that left-handedness is less frequent because it has a health cost. However, evidence for the health cost of left-handedness is unsubstantiated, leaving the greater frequency of right-handers unexplained. Research indicates that homicide may have been common in early hominins. We propose that the hand used to hold a weapon by early hominins could have influenced the outcome of a fight, due to the location of the heart and aorta. A left-handed unilateral grip exposes the more vulnerable left hemithorax towards an opponent, whereas a right-hand unilateral grip exposes the less vulnerable right hemithorax. Consequently, right-handed early ancestors, with a preference for using the right forelimb in combat, may have had a lower risk of a mortal wound, and a fighting advantage. This would explain their greater frequency. In accordance with the original fighting hypothesis, we also suggest that left-handed fighters have a surprise advantage when they are rare, explaining their persistence. We discuss evidence for the modified fighting hypothesis, its predictions, and ways to test the theory.
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... Die Forschung zur pränatalen Androgenexposition hat gerade in den letzten Jahrzehnten einen starken Aufschwung erfahren. Es wird heute davon ausgegangen, dass die pränatale Exposition gegenüber Androgenen, wie Testosteron, im Mutterleib einen Einfluss auf die Entwicklung des embryonalen Gehirns hat (Grimshaw et al., 1995). Dies wirkt sich zum einen auf die strukturelle Organisation aus, wie zum Beispiel die Händigkeit, unabhängig vom Geschlecht des Embryos (Cohen-Bendahan et al., 2004). ...
Der Zusammenhang von 2D:4D als Marker für pränatale Testosteronexposition und dem Erfolgs-, Macht-, und Zugehörigkeitsmotiv von Erwachsenen erfasst durch den impliziten Assoziationstest
Thesis
  • Jan 2022
Background and Aims The ratio of the 2nd to 4th finger length (2D:4D) as an indicator for prenatal androgen exposure has been the topic of numerous studies throughout many fields of research. This study concentrates on the effect of the prenatal androgen on the development of implicit motives, namely the need for achievement, need for affiliation and need for power. Previous studies examining the 2D:4D ratio and implicit motives used the Picture Story Exercise and were limited in sample size mainly because of the time-consuming testing and scoring process. This study tries to replicate and extend preceding findings using the Implicit Association Test (IAT), an easily accessible and objectively assessable alternative to the Picture Story Exercise to quantify implicit motives. Methods This study was conducted on 203 individuals, 102 female and 101 male, ranging from ages 18 to 65. Each individuals’ hands were scanned for the assessment of 2D:4D, following a questionnaire using, among other tests, three IATs, as well as assessing Cognitive Reflection and time estimation as suggested analogues for the Activity Inhibition, as measured in the Picture Story Exercise. Results The 2D:4D ratio alone was not significantly correlated to any of the implicit motives. However, when separated into groups of high and low impulsivity based on time estimation or the Cognitive Reflection Test, there was a significant negative correlation in the male cohort between the need for power and the 2D:4D ratio (rsp = -0,284, p = 0,032 for time underestimation; rsp = - 0,244, p = 0,048 for high cognitive reflection), thus reproducing the results previously made using the Picture Story Exercise in the group of high Activity Inhibition. The data on IAT and 2D:4D separately for males and females were also compared to the literature for validation. Conclusion The results found in this study are in line with previous findings, indeed confirming a certain influence of prenatal androgen exposition on the development of implicit motives in male adults, when separated for high cognitive reflection / time underestimation reflecting low impulsivity. As the results are similar to those produced in studies using the Picture Story Exercise. This might indicate that the Implicit Association Test in combination with the Cognitive Reflection Test or time estimation is a valid alternative to the Picture Story Exercise and Activity Inhibition
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... Compared to control girls, girls with CAH showed greater bilateral amygdala activation when viewing negative (fearful and angry) faces than when viewing neutral faces; amygdala activation in girls with CAH was not statistically different from that of control boys (Ernst et al., 2007). This is broadly consistent with work showing that amniotic testosterone is positively linked to male-typed right lateralization of emotion processing in a typical sample (Grimshaw et al., 1995). ...
Prenatal androgen influences on the brain: A review, critique, and illustration of research on congenital adrenal hyperplasia
Article
  • Jun 2021
Sex hormones, especially androgens, contribute to sex and gender differences in the brain and behavior. Organizational effects are particularly important because they are thought to be permanent, reflecting hormone exposure during sensitive periods of development. In human beings, they are often studied with natural experiments in which sex hormones are dissociated from other biopsychosocial aspects of development, such as genes and experiences. Indeed, the greatest evidence for organizational effects on sex differences in human behavior comes from studies of females with congenital adrenal hyperplasia (CAH), who have heightened prenatal androgen exposure, female‐typical rearing, and masculinized toy play, activity and career interests, spatial skills, and some personal characteristics. Interestingly, however, neuroimaging studies of females with CAH have revealed few neural mechanisms underlying these hormone‐behavior links, with the exception of emotion processing; studies have instead shown reduced gray matter volumes and reduced white matter integrity most consistent with other disease‐related processes. The goals of this narrative review are to: (a) describe methods for studying prenatal androgen influences, while offering a brief overview of behavioral outcomes; (b) provide a critical methodological review of neuroimaging research on females with CAH; (c) present an illustrative analysis that overcomes methodological limitations of previous work, focusing on person‐specific neural reward networks (and their associations with sensation seeking) in women with CAH and their unaffected sisters in order to inform future research questions and approaches that are most likely to reveal organizational hormone effects on brain structure and function.
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... Season of birth could influence handedness through the fetal experience during the last weeks of pregnancy for at least two reasons. First, hormone level varies with the length of photoperiod, and hormone level has sometimes been shown to influence brain lateralization for language and handedness [41], with sex differences regarding this effect [38,42]. Second, a combination of more sun and lighter clothing of the mother during the warm seasons might induce more reinforcement of a right-hand tendency due to a better sight of their moving right arm by fetuses born during these seasons. ...
Is Handedness at Five Associated with Prenatal Factors?
Article
Full-text available
The goal of the study was to investigate some of the factors suspected to be related to children’s handedness: presentation during the last weeks of gestation and at birth (cephalic or breech), side of presentation (right or left), number of weeks of gestation, season of birth, parents’ handedness and sex. We analyzed the relationships between these factors and the child’s handedness at five years. Children (n = 1897) from the EDEN cohort participated in the study, among which 1129 were tested for handedness at five. The father’s handedness, but not the mother’s, was significantly related to the child’s hand preference. The percentage of left-handed children was significantly larger when the father was non-right-handed compared to right-handed, and tended to be larger among children in non-left-cephalic presentation compared to left-cephalic presentation. Girls, but not boys, were significantly less lateralized when they were born before 37 weeks of pregnancy than after. Finally, children born in winter or spring were slightly but significantly less lateralized than children born in summer or autumn. All six children who were not lateralized at 5 presented one or several of these factors. These results are discussed in light of the mixed model of handedness.
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The ratio of second and fourth finger lengths (2D:4D) can determine handedness
Article
  • Nov 2023
Objective: The human body exhibits both structural and functional asymmetry. One measure of this asymmetry is the ratio of 2D:4D, which is the proportion of measurements of the 2nd (2D) and 4th finger (4D). In this research, our objective is to investigate the potential association between the ratio of 2D:4D and handedness with voluntary individuals. Methods: A total of 312 individuals volunteered to take part in the research, where their left and right hand's 4th and 2nd finger lengths were measured using a precise digital caliper. The "Edinburgh Handedness Inventory" was used to determine hand lateralization. To determine the significance between the two independent groups, the Mann Whitney U Test was used. On the other hand, to determine the significance between the two dependent groups, the Wilcoxon Signed Rank Test was utilized. Results: Of the participants, 154 were male and 158 were female (age range 18-55, mean age=28.34). According to the Edinburgh Handedness Inventory, 275 individuals were right handed, 18 were left handed, and 19 were bimanual. The Mann Whitney U Test showed a significant result in the ratio of right hand 2D:4D between male and female participants who were right handed (z =-1.979, p = 0.048). Additionally, the Wilcoxon Signed Ranks Test demonstrated a difference between the right and the left hand ratio of 2D:4D for all participants which was significant (z = -2.822, p = 0.005), as well as for participants who were right handed (z = -2.850, p = 0.004). Conclusion: The ratio of 2D:4D finger lengths could be a significant indicator of hand preference in both male and female healthy individuals. The ratio of 2D:4D holds potential as an indicator and research tool in understanding human emotions, thoughts, and behaviors.
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The effects of sex and handedness on masturbation laterality and other lateralized motor behaviours
Article
  • Nov 2021
Masturbation is a common human behaviour. Compared to other unimanual behaviours it has unique properties, including increased sexual and emotional arousal, and privacy. Self-reported hand preference for masturbation was examined in 104 left-handed and 103 right-handed women, and 100 left-handed and 99 right-handed men. Handedness (modified Edinburgh Handedness Inventory, EHI), footedness, eyedness, and cheek kissing preferences were also measured. Seventy nine percent used their dominant hand (always/usually) for masturbation, but left-handers (71.5%) were less consistently lateralized to use their dominant hand than right-handers (86.5%). Hand preference for masturbation correlated more strongly with handedness (EHI), than with footedness, eyedness, or cheek preference. There was no difference in masturbation frequency between left- and right-handers, but men masturbated more frequently than women, and more women (75%) than men (33%) masturbated with sex aids. For kissing the preferred cheek of an emotionally close person from the viewer’s perspective, left-handers showed a left-cheek preference, and right-handers a weaker right-cheek preference. The results suggest that hemispheric asymmetries in emotion do not influence hand preference for masturbation but may promote a leftward shift in cheek kissing. In all, masturbation is lateralized in a similar way to other manual motor behaviours in left-handed and right-handed men and women.
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Controlling for Stimulus Dominance in Dichotic Listening Tests: A Modification of λ
Article
Full-text available
  • Apr 1994
Dichotic listening procedures have been used to assess cerebral lateralization in normal Ss. One particularly useful technique is the use of stimuli that fuse into a single percept. Although this procedure has many advantages over other dichotic listening methods, it is particularly susceptible to stimulus dominance, which acts as noise in a S's response data, thus reducing the power of any statistical test of the ear advantage. It is proposed that the solution to this problem is a log-linear analysis of the response data to yield a λ-type index (λ*) that is a measure of ear dominance independent of stimulus dominance. Details of the analysis are provided, as well as a sample analysis of data collected from 104 right-handed and 30 left-handed Ss. Comparisons are drawn between the log-linear analysis and other methods that have been proposed to control for stimulus dominance in this single-response dichotic fusion procedure. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
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Relations Between Prenatal Testosterone Levels and Cognitive Abilities at 4 Years
Article
Full-text available
  • Nov 1992
Relations between prenatal testosterone (T) levels and cognitive abilities at age 4 were examined for 28 girls and 30 boys. Prenatal T levels were measured in 2nd trimester amniotic fluid samples obtained by amniocentesis and were examined in relation to scores on tests of cognitive abilities. For girls, prenatal T levels showed a curvilinear (inverted U-shaped) relation to language comprehension and classification abilities. Linear relations also were observed in that prenatal T levels were inversely related to girls' scores on tasks assessing counting and number facts. Similarly, girls with high average block building scores had lower prenatal T and cognitive abilities were not observed. The observation of relations in girls and not boys is discussed, and the findings are examined in relation to theories of hormone-behavior relations. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
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Early Hormonal Influences on Cognitive Functioning in Congenital Adrenal Hyperplasia
Article
Full-text available
  • Mar 1986
Administered a cognitive test battery that emphasized spatial ability, verbal fluency, and perceptual speed and accuracy to 17 females (aged 12.7–23.2 yrs) and 8 males (aged 13–29.9 yrs) with congenital adrenal hyperplasia (CAH) and 13 normal female relatives (aged 11.4–31.1 yrs) and 14 unaffected male relatives (aged 12.5–28.8 yrs). In addition, 13 fathers and 15 mothers of CAH patients participated. Ss also completed the Progressive Matrices, a vocabulary test, and an early life activities questionnaire (ELAQ). Findings indicate that CAH females, as compared with normal females, showed significantly enhanced performance on hidden pattern, card rotation, and mental rotation tests of spatial ability. On the ELAQ, CAH females, relative to normal females, showed significantly lower frequencies of participation in activities involving verbal expression and a trend toward greater participation in spatial manipulation activities. However, differences between CAH females and normal females in early childhood activities did not account for observed differences in spatial ability, given the absence of a significant correlation between the spatial manipulation activity scale and spatial ability. There was an absence of reliable differences between male CAH patients and controls across spatial tasks. Results are consistent with an effect of pre- and perinatal androgenizing hormones on the development of spatial ability. (58 ref) (PsycINFO Database Record (c) 2012 APA, all rights reserved)
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Prenatal and intrapartum high-risk screening
Article
  • Sep 1973
  • AM J OBSTET GYNECOL
A high-risk pregnancy screening system based on a prospective analysis of prenatal, intrapartum, and neonatal factors in 738 pregnancies can predict perinatal morbidity and mortality. Factors were assigned with weighted values according to their assumed risk. Total scores for the prenatal, intrapartum, and neonatal period were dichotomized to simplify the scoring system by forming a low-risk group (scores < 10) and a high-risk group (scores ≥ 10). Three hundred and forty patients (46 per cent) were low risk during both the prenatal and intrapartum period (low/low risk group). In this group the incidence of high-risk neonates and the perinatal mortality rate was extremely low. There was no significant increase in neonatal morbidity or perinatal mortality in 135 patients (18 per cent) who were identified as high risk during the prenatal period but low risk during the intrapartum period (high/low risk group). However, in 144 patients (20 per cent) at risk only during the intrapartum period (low/high risk group) or in 119 patients (16 per cent) at risk during both prenatal and intrapartum periods (high/high risk group) there was a significant increase in the number of high-risk neonates and perinatal mortality. By a stepwise multiple regression analysis, actual intrapartum scores are most predictive of neonatal risk (days in hospital) followed by actual prenatal scores. Identifying a population as to their risk status for both the prenatal and intrapartum period has added depth to the understanding of the continuum of risk which exists within the framework of the perinatal period.
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Handedness in families
Article
  • Jul 1973
  • ANN HUM GENET
The handedness of 3644 yound adults and that of their parents and siblings is described for the incidence of left handedness in children from families classified for parental handedness and also in the relatives of right and left handers. Estimates of heritability are derived for this main sample and also for a smaller sample of parents and grandparents. A significant maternal influence is found and an association of borderline significance between sisters. Paternal influence, although smaller than maternal, is probably present especially for sons. There is a sex difference in the filial generation when the mother is right handed but not when the mother is left handed. The findings are considered in relation to theories of the determination of handedness and especially for their relevance to the view that there may be genetic influences toward right but not toward left handedness.
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Early Androgens Are Related to Childhood Sex-Typed Toy Preferences
Article
  • May 1992
Girls with cong~nital adr~nal hyp~rplasia (CAR) who w~r~ ~xpos~d to high '~v~ls 01 andro,~n in th~ pr~natal and ~arly postnatal p~riods show~d in- cr~as~dp/Qy with boys' toys and r~duc~d play with girls' toys compar~d with th~ir un~xpos~d I~ma/~ r~/atives at a,~s 3 to 8. Boys with CAR did not differ from th~ir ma/~ r~/atives in play with boys' or girls' toys. Th~se r~sults sugg~st that early hormon~ exposur~ in/~males has a masculinizing ~ff~ct on s~x-typ~d toy pr~/erences. the patient or control status of subjects. We hypothesized that CAH girls would show 8feater preference for boys' toys than their unaffected female relatives, and reduced preference for girls' toys. We did not predict effects for CAH boys because androgen treatment has incon. sistent effects in male experimental ani- mals (Baum &. Schretlen, 197.5; Dia. mond. Llacuna, & Wong, 1973).
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The inheritance of left-handedness
Article
  • Jan 1928
In 55 families in which the mother was left-handed, 13.77% of the offspring were left-handed. In 82 families in which the father was left-handed 9.7% of the offspring were left-handed. In 33 families in which both parents were left-handed 46% of the offspring were left-handed. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
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