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Digit ratio and faculty membership: implications for the relationship between prenatal testosterone and academia.

The aim of this study was to examine an emerging index of prenatal sex hormone exposure, digit ratio, in relation to academic discipline. This was pertinent as the cognitive abilities theorized to be influenced by prenatal sex hormone exposure are the same as the cognitive abilities used to characterize academic disciplines.

The sexually dimorphic nature of digit ratio has been recognized for over 130 years (Cohen-Bendahan, van de Beek, & Berenbaum, 2005; Ecker, 1875) although the genetic basis to the differentiation of the digit pattern is more recent. The HOX gene family is required for the growth and patterning of digits and the differentiation of the genital bud. Hoxd and Hoxa genes are strongly expressed in the gonads and are also required for the growth and differentiation of digits. This sharing of causal factors in digit and gonad differentiation allows patterns of digit formation to be a marker for prenatal sex hormone concentration (Manning, Scutt, Wilson, & Lewis-Jones, 1998). The length of the fourth digit (ring finger) is thought to be an index of prenatal testosterone exposure relative to the length of the second digit (index finger), which is thought to represent an index of prenatal oestrogen exposure. The 2D:4D ratio (second digit length divided by fourth digit length) therefore provides an index of prenatal testosterone exposure relative to prenatal oestrogen exposure. Digit ratio is thought to be fixed in utero and relative digit lengths remains constant throughout development from the age of 2 (Manning, 2002). Sex hormones have been obtained from stored samples of amniotic fluid and found to significantly correlate with digit ratio in 2-year-old children (Lutchmaya, Baron-Cohen, Raggatt, Knickmeyer, & Manning, 2004). Digit ratio is sexually dimorphic with males having a mean of 0.98; that is, 4D longer than 2D and females having a mean of 1.00 (equal length fingers; Manning et al., 1998). There are also differences in digit ratio across different ethnicity groupings, however, the sexually dimorphic properties are consistent across all cultures and are independent of age or height (Lippa, 2003; Manning, Stewart, Bundred, & Trivers, 2004).

It is argued that behavioural and physiological advantage, together with an influence on subsequent fertility, is conferred upon a male foetus exposed to high prenatal testosterone and low oestrogen, and upon a female foetus exposed to the converse--low prenatal testosterone and high oestrogen (Manning et al., 2000). In males, the 2D:4D ratio is related to sperm count (a lower 2D:4D ratio indicating higher exposure to testosterone relates to higher sperm count; Manning et al., 1998). Manning et al. report a negative correlation for males between 2D:4D ratio and number of children in an English sample, indicating that lower 2D:4D (higher testosterone) is associated with a greater number of children (the opposite pattern was identified for females).

In addition to fertility, prenatal gonadal hormones exert long-lasting organizational influences on brain and behaviour in humans (Collaer & Hines, 1995). Consequently, digit ratio is hypothesized to relate to gender differences in cognitive abilities as exposure to prenatal testosterone is theorized to encourage the development of areas of the right hemisphere while slowing the development of the corresponding areas in the left hemisphere, thereby enhancing visual spatial abilities relative to language abilities (Geschwind & Behan, 1982; Geschwind & Galaburda, 1987). Geschwind and his colleagues' theoretical account linking prenatal testosterone exposure with gender differences in cognition also attempted to account for patterns in handedness, developmental disorders and immune disorders. Research investigating the relationship of prenatal testosterone with cognition and developmental disorders has been mixed (Grimshaw, Bryden, & Finegan, 1995; Grimshaw, Sitarenios, & Finegan, 1995; Lutchmaya, Baron-Cohen, & Raggatt, 2002a, 2002b; Manning, Baron-Cohen, Wheelwright, & Sanders, 2001; Moffat & Hampson, 1996; see Baron-Cohen, Lutchmaya, & Knickermeyer, 2004 for a review). Bryden, McManus, and Bulman-Fleming (1994) provide an extensive critique of the relationship between handedness and immune functioning. The first part of this critique provides an analysis of the concept and assessment of handedness itself as an indicator or prenatal testosterone exposure. Subsequent meta-analysis then finds some support for a relationship between handedness and some immune disorders (such as allergies or asthma) but not others. In a commentary upon Bryden et al.'s critique, Hampson and Moffat (1994) note that little attention is paid to the relationship between prenatal testosterone and enhancement of cognitive abilities (as a consequence of right hemisphere development). Bryden et al. themselves pointed out the lack of research into this aspect of the theory. Hampson and Moffat conclude that it would be unfortunate if the Bryden et al. critique discouraged research into hormone-brain-behaviour relationships. Given the variability in the conceptualization and assessment of handedness, it may be the case that digit ratio provides a more consistent index of prenatal testosterone exposure than handedness. Two recent reviews of the research examining the relationship between digit ratio with health and cognition have reported inconsistencies in the findings (Cohen-Bendahan et al., 2005; Putz, Gaulin, Sporter, & McBurey, 2004). Cohen-Bendahan et al. conclude that 'studies of finger ratio are promising, if complicated' (p. 375). One of the complications is the variability in identifying gender differences in cognitive abilities theorized to be affected by prenatal testosterone exposure.

Whilst some studies support a verbal advantage for females and a spatial advantage for males (see Halpern, 2000; Maccoby & Jacklin, 1974), other studies fail to replicate such findings. The elusive nature of gender differences can revolve around task classification. Among verbal tasks, vocabulary per se is gender-neutral and among spatial tasks, females excel in object location (Hyde & Linn, 1988; James & Kimura, 1997). Sanders, Sjodin, and de Chasterlaine (2002) argue that it is the pattern of significant outcomes that is important, and that around 80% of studies report an advantage for females in verbal abilities and males in visual spatial abilities, pointing to the reality of gender differences within this relatively crude dichotomy of cognition. Additionally, gender differences do not represent two mutually exclusive levels of performance, as there are overlaps between the range of male and female performance on these tasks.

Male advantage in visual spatial abilities such as mental rotation, spatial visualization, mathematical and mechanical reasoning are theorized to reflect an underlying male advantage in folk physics or systemizing (Baron-Cohen, 2002; Lawson, Baron-Cohen, & Wheelwright, 2004). Folk physics or, more recently, systemizing is an intuitive everyday understanding of how things work; an understanding the properties of physical objects, including their causal impact on other objects (Baron-Cohen, 2002, 2003; Baron-Cohen, Richler, Bisarya, Gurunathan, & Wheelwright, 2003; Baron-Cohen, Wheelwright, Skinner, Martin, & Clubley, 2001; Baron-Cohen, Wheelwright, & Spong, 2001). Folk physics is independent from what Baron-Cohen terms folk psychology or more recently empathizing, that is an intuitive everyday understanding of how people work; the understanding of how actions are caused by mental/intentional states of others (Baron-Cohen, 2002, 2003; Baron-Cohen & Wheelwright, 2004). Both folk physics and folk psychology are naturally developing forms of knowledge not explicitly taught and acquired universally. Thus, folk physics is different from academic physics as it is found in children prior to formal education although the principles derived from folk physics are developed within the academic disciplines of mathematics, computer science and physics. Baron-Cohen conceives of a continuum from folk physics through to folk psychology upon which males are more proficient in folk physics and females are more proficient in folk psychology, thereby providing a theoretical account for the male domination of science. Baron-Cohen (2002, p. 72) argues that '... all the sciences utilize systemizing as their basis, and all are dominated by men'. This male domination occurs from undergraduate through to the professoriate (2.5% are female in the UK) and Fellowship of the Royal Society (3.6% are female). When females do select science, there is a tendency to select life sciences, such as biology, and particularly social science, such as psychology (Brosnan, 1998; Mellor, 2001). Baron-Cohen extends this sexually dimorphic model of evolved brain types to provide an account of the developmental disorder of autism as an extreme male brain--excelling in folk physics but with a deficit in folk psychology. Whilst children with autism have deficits in language and communication, visual spatial abilities can exceed normal levels (Frith, 1997; Happe, 1999). An extreme male digit ratio has been identified in children with autism (0.94), suggesting prenatal testosterone as a contributory factor in the aetiology of autism (Manning et al., 2001).

Baron-Cohen proposes an association between the autistic condition and science/maths skills (Baron-Cohen et al., 2001; Baron-Cohen, Wheelwright, Stone, & Rutherford, 1999). Mathematicians and children attending a mathematics Olympiad obtained high scores upon assessments of autism (Baron-Cohen et al., 2001), and children with Asperger Syndrome demonstrate superior ability within the domain of physics (Baron-Cohen et al., 2001). Central to this conceptualization is the extreme male brain theory of autism (Baron-Cohen, 2002). Individuals with autistic qualities have superior systemizing skills but a relatively poor level of empathizing skills. These biases appear to a lesser extent in scientists/mathematicians and continue along the continuum to the opposing biases of greater empathizing abilities to the detriment of systemizing abilities, which is argued to be a more female-typical profile.

Such a linear conceptualization is supported by Sanders et al. (2002) who found a negative correlation between digit ratio and visual spatial ability. However, a linear relationship between testosterone and spatial ability is challenged by the work of Kimura (1999), which suggests that the optimal level of testosterone for spatial ability performance is the lower male range. Improvements in visual spatial tasks are associated with increases in circulating testosterone in females and decreases in circulating testosterone in males. To resolve this apparent contradiction, Sanders et al. (2002, p. 151) propose that 'the relationship between the 2D:4D ratio and spatial ability may reveal a U-shaped curve'. This is consistent with some theorists' proposal of non-monotonic effects of exposure to prenatal testosterone (McFadden, 2002). Geschwind and Galaburda (1987) also hypothesized that very high levels of prenatal testosterone may impede the development of both hemispheres, leading to diminished spatial abilities and consequently a curvilinear relationship between prenatal testosterone and spatial ability. This begs the question of what constitutes the higher male digit ratio range. A mean of 0.98 is typically identified with a standard deviation of 0.02 to 0.04 (N = 2000, Lippa, 2003; N = 800, Manning et al., 1998; N = 200, Manning et al., 2004; N = 758 across ethnicities, Manning et al., 2004). If the higher male digit ratio range is towards a standard deviation from the mean, this would produce a typical value of approximately 1.00 to 1.02. That is to say, although the male-typical profile is described as comprising superior visual spatial abilities relative to the female-typical profile, it is males with the female-typical digit ratio profile that are theorized to demonstrate superior visual spatial abilities.

From the above, we would predict that those from the science faculty who have been characterized as more extreme systemizers resultant from exposure to prenatal testosterone typical of the lower normal male range will have a digit ratio in the higher male range (towards 1.0 to 1.02)--when compared with those from other faculties. A second study will further examine fertility, psychological conditions and handedness.

Method

Participants

Participants were 107 respondents from all departments and all academic grades who responded to a request to complete an Internet-based questionnaire asking for basic demographic information and a self-assessment of 2D and 4D digit length of the right and left hand. There are 500 academics working at the university, giving a response rate of 21.4%. Of these, 22.4% (N = 24) of respondents were female, which accurately reflects the proportion of female academics in the university (20%). There were 31 responses from the Engineering faculty, 33 from the Humanities and Social Science (HaSS)/Management faculty and 43 from the Science faculty, again reflecting the distribution of staff within the university. Ages ranged from 23 to 62 with a mean of 44 years (SD = 10 years). Participants were not asked to report their ethnicity, but from the University population, over 94% of academics who have registered their ethnicity with Human Resources identified themselves as 'white'. The remaining ethnicities are spread comparably between faculties. The University of Bath is an institution focusing on science and engineering (there is no Arts faculty) and this will be reflected in the sample.

Design

Digit ratio was calculated by dividing the length of the second digit (2D) by the length of the fourth digit (4D) for the left and right hand separately and then calculating the mean of these two ratios. Digit length was measured from the basal crease of each finger to the centre of top of each finger to the nearest 0.5 mm (Lippa, 2003).

Validation of data

As participants submitted their Internet data, they were asked if they would submit a photocopy of their hands and undertake an additional questionnaire. The questionnaire assessed academic history, whether the person was a biological parent and whether there were any psychologically diagnosed conditions within this immediate (genetically related) family. The questions were: 'how many children are you the biological parent of?' and 'do you or any genetic relations (parents, siblings, children) have a formal diagnosis of any psychological conditions (e.g. dyslexia, Aspergers, etc.)' and then asked to complete a two-column table with the headings: condition (e.g. dyslexia, Aspergers, etc.) and relationship (e.g. myself, my son, etc.). Finally, handedness was assessed using a 36-item questionnaire with five possible responses from strongly right through to strongly left (Elias, Bryden, & Bulman-Fleming, 1998). There were 18 respondents who forwarded a photocopy of their hands that were measured using vernier callipers, digitally recording distances in millimetres to two decimal places. Each measurement was undertaken twice. The correlation between the self-measurement and the measurement of the photocopy was extremely significant (r = .82, p < .001). This is consistent with previous research that has found self-measurement to be a successful protocol for digit ratio data (Wilson, 1983), which used 10% of the original sample for an analysis of validity (e.g. Putz et al., 2004), and it has been concluded that digit ratios calculated from photocopies are essentially the same as those measured directly from fingers (Manning et al., 2000; though see Manning, Fink, Neave, & Caswell, 2005).

Of the participants, 49 (46% of the original sample) responded to an invitation to complete an additional questionnaire detailing their academic history and family demographics. An examination of degrees indicated that the vast majority of academics were working within the faculty in which they had studied. Of these, 84.4% academics had a first degree in a discipline of their present faculty, 80% had a masters degree within a discipline of their present faculty and 92.5% had a PhD within a discipline of their faculty.

Results

An ANOVA was conducted to identify whether there were between-group differences in gender (two levels), faculty (three levels: Engineering, Science, HaSS/Management) or pay scale (four levels: lecturer, senior lecturer, reader, professor) that related to differences in digit ratio. This showed that there was a significant difference between the faculties in digit ratio, F(2, 90) = 3.52,p = 0.03. A Tukey HSD post hoc analysis revealed that the significant difference was between the Science faculty and the HaSS/Management faculty (p = .02), with the Engineering faculty averaging between the other two faculties. To three decimal places, the mean ratio for the Science faculty was 0.996 (SD = 0.03), HaSS/Management = 0.977 (SD = 0.03) and for Engineering = 0.984 (SD = 0.03). There were no significant main effects for gender: mean for men = 0.987, SD = 0.03, mean for women = 0.984, SD = 0.02; F(1, 90) = 0.002, ns; nor scale: lecturer to professor means range from 0.978 to 0.989, F(3, 90) = 2.044, ns; and there were no significant interactions. The means are displayed in Table 1.

Descriptive Analysis by Department: The mean digit ratio was 0.986 (SD = 0.03). An examination of those departments with means of 1.00 (above 0.995) and below 0.980 (to exclude those around the mean and identify those around the population norms for men and women) revealed the following two groups of departments:

Group 1: Above 0.995: (N = 26, 81% men)

Chemical Engineering, Chemistry, Computer Science, Mathematical Science, Physics.

Group 2: Below 0.98: (N = 38, 66% men)

Architecture, Economics, Education, Management, Psychology, Sports Science, Social and Policy Sciences.

Obviously, constructing headings for these two groups is going to be a crude approximation, not least because of the overlaps in skills between academics from different departments. Given this proviso, there does seem to be a more folk physics/systemizing orientation to the first grouping and a more folk psychology/empathizing orientation to the latter grouping as described through the work of Baron-Cohen in the Introduction. However, the first group has a digit ratio at the higher end of the normal male range (indicative of lower levels of prenatal testosterone), consistent with the work of Kimura that suggests this is the optimal level for enhanced visual spatial skills that underpin folk physics and subsequent academic development.

Follow-up questionnaire

Previous research has found that men with children have a significantly lower digit ratio when compared with men without children (with age as a covariate). The trend was in this direction in the present study: seven men with no children, mean digit ratio = 0.996, SD = 0.02; 27 men with children, mean digit ratio = 0.982, SD = 0.03, F(1, 31) = 3.89, p < .06. Of those who believed themselves to be biological parents, the next question asked if any (genetically related) immediate family members had any psychological conditions. Six replied 'yes' (dyslexia) with a mean digit ratio of 1.004 (SD = 0.01), 43 replied 'no' with a mean digit ratio of 0.985 (SD = 0.03). Again, this difference was statistically significant (t = 2.71, p < .02: two-tailed; equal variances not assumed; therefore, df = 12). Finally, handedness was not a significant correlate of digit ratio for the whole group (r = .09, p = .55) or any of the subgroups. The left and right digit ratios separately both correlated with the average digit ratio (p < .001) and there was no discernable pattern of left hand digit ratio correlating more significantly for lefthanders and right-hand digit ratio for right-handers. Left- and right-handers both had a mean digit ratio of 0.988. Manning, Bundered, Newton, and Flanagan (2003) suggest calculating right-hand digit ratio minus left-hand digit ratio (termed DR-1) to investigate left-/right-hand differences. This calculation yields a mean of 0.004, with no significant differences between left and right-handers, again indicating the similarity of the right and left hands.

Discussion

Digit ratio was significantly different between members of the Science Faculty and members of the HaSS/Management Faculty. This was consistent with prediction based upon the circulating testosterone literature (e.g. Kimura, 1999). Existing theory predicted that those with proficient folk physics/systemizing skills associated with scientists and mathematicians would have an index of prenatal testosterone within the higher male range (lower prenatal testosterone). The present study found this to be the case when compared with academics from other disciplines (Humanities and Social Science/Management). Academic level was not significant (lecturers, senior lecturers, readers and professors), suggesting that testosterone levels do not predict achievement within the chosen discipline (this was also the case when controlling for age).

It was interesting that the women in academia averaged a digit ratio (0.984) similar to the male norm reported elsewhere for larger, more diverse populations (0.98), suggesting a link between prenatal testosterone and an academic orientation in women. Possibly as a consequence of this, digit ratio was not sex dimorphic in the academic sample studied here. A similar lack of gender difference has also been reported in academic undergraduate samples (Austin, Manning, McInroy, & Mathews, 2002, Study 1). This was associated with an unexpected lack of gender differences in verbal fluency. The present study suggests that academic discipline may represent a confound when using an academic sample and should be controlled for. If the sampling of male and female students reflects the demographics of the student population, we would expect more of the women to be drawn from the social sciences and more of the men to be drawn from the 'hard' sciences (Brosnan, 1998; Mellor, 2001). The present study suggests that this may bias the range of digit ratios sampled.

The range of digit ratios was pertinent as the present study's findings relating to prenatal testosterone exposure are also consistent with the research concerning circulating testosterone, which raises a significant issue that needs to be accounted for. If testosterone is implicated in the aetiology of gender differences in cognition, why does the male in the lower testosterone range (more female-typical) demonstrate the cognitive profile most distinct from the female-typical cognitive profile. A non-monotonic relationship between testosterone (circulating and prenatal) and cognition may explain this apparent contradiction (Grimshaw et al., 1995; Lutchmaya et al., 2002a; Moffat & Hampson, 1996; Sanders et al., 2002). Such a relationship may also explain variations in the significance of linear correlational analyses (see Putz et al., 2004, for a review). If digit ratio constitutes a reliable index of prenatal testosterone exposure, its assessment provides an accessible methodology to research the relationship between prenatal sex hormone exposure and cognition. In utero, testosterone in converted into oestrogen (estradiol) by a process called aromatization. In males, most oestrogen is made from androgens (testosterone; see Baron-Cohen et al., 2004). Whilst the impact of aromatization upon digit ratio is yet to be fully understood, these processes do provide a framework to potentially explain how an index of testosterone can have differential implications for males and females. Additionally, Manning et al. (2003) highlight that the response to prenatal testosterone is not only dependent upon the amount exposed to but also the sensitivity to the hormone. The authors report that digit ratio is related to sensitivity to testosterone, such that a low digit ratio is associated with high sensitivity to testosterone (assessed through a DNA examination of the X-linked androgen receptor gene in males; see Manning et al., 2003). It is likely (e.g. Goy & McEwen, 1980) that this prenatal index interacts with circulating levels of hormones such that males and females with a digit ratio of 1.0 may be comparably sensitive to testosterone, but even males within the low circulating testosterone range for males have higher levels of circulating testosterone than females. Males typically have higher levels of circulating testosterone than females throughout the day (e.g. Moffat & Hampson, 1996 report means of circulating testosterone around 80 pg/ml for males [SD around 20] and 20pg/ml for females [SD between 6 and 15]). When sampling prenatal testosterone, the highest female recording can be lower than the lowest male recording (e.g. Grimshaw et al., 1995).

Previously, digit ratio has been linked with higher sperm counts and fertility in males. The present data was consistent with this, since there was a trend for males with lower 2D:4D ratios (more prenatal testosterone) to have children. The study failed to utilize sexuality as variable as current research is conflicting (Lippa, 2003; Robinson & Manning, 2000), but the results are consistent with data suggesting that lower digit ratios are associated with reproductive success. Digit ratio was also significantly different between those with children who have a psychological diagnosis in the family (dyslexia, digit ratio = 1.004) and those with children who do not have a psychological diagnosis in the family. This complements the work of Manning et al. (2001) who identified an extreme male digit ratio in children with autism (0.94) and their immediate family members (0.96). Opposing digit ratios being associated with autism and dyslexia is consistent with an opposing pattern of performance on the embedded figures test demonstrated by the two developmental disorders (Brosnan et al., 2002; Shah & Frith, 1983).

As noted in the Introduction, spatial ability is a crude categorization, which may be exemplified by architecture appearing in the second grouping of academic disciplines (folk psychology/empathizing). Architecture would expect to benefit from effective visuospatial capacities, though not necessarily systemizing. A better understanding of the crude cognitive labels is required and the relationship between specific spatial abilities and the systemizing theorized to underpin them. One theoretical account provided by Geschwind and his colleagues is argued to be compromised by the use of handedness as an index of prenatal testosterone exposure (Bryden et al., 1994). Digit ratio may provide an alternative index to examine the relationship between prenatal sex hormonal exposure and specific aspects of cognitive abilities.

Baron-Cohen and his colleagues have identified that scientists/mathematicians and individuals with Asperger syndrome are both high on systemizing abilities. A U-shaped non-monotonic relationship between digit ratio and systemizing would suggest that, although mathematicians/physicists/computer scientists and children with autism may excel at the same abilities, there are different explanatory frameworks for these similar profiles. If prenatal testosterone serves to suppress the neural circuits associated with folk psychology/empathy (see Singer et al., 2004) the development of folk physics/systemizer skills could be a compensatory mechanism (Belmonte, 2002) for a deficit in folk psychology--a possibility acknowledged by Baron-Cohen, Stone, Wheelwright, and Rutherford (1999). This may constitute a separate mechanism by which mathematicians/physicists/computer scientists not associated with autism develop these abilities. It could be the case therefore that a mathematician/physicist/computer scientist may have autistic tendencies (Baron-Cohen et al., 1999) or may not, dependent upon the presence or absence of folk psychology/empathizing abilities. Whilst Baron-Cohen conceives of a single continuum from extreme systemizer to extreme empathizer, he acknowledges that the inter relationship of the two variables has yet to be fully understood.

In sum, it was argued in the Introduction that all sciences utilize systemizing as their basis, indicating that this study is examining variance within a restricted range of ability. Despite this, the present study has identified differences between faculties, and that those in faculties requiring higher systemizing abilities and without any indication of autism in the family have an index of low prenatal exposure to testosterone. This contrasts with Baron-Cohen's findings that those with high systemizing abilities with autism in the family have an index of high exposure to prenatal testosterone. Consistent with theory, this could be related to a U-shaped relationship between exposure to prenatal testosterone and the abilities that underpin systemizing. As lower ratios have been associated with autism, it is particularly interesting that higher ratios have been associated with dyslexia in this study, which warrants further investigation to further evaluate the proposal that digit ratio can facilitate diagnosis of autism and dyslexia at birth (Manning & Bundred, 2000).

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Received 29 June 2004; revised version received 31 October 2005

Mark J. Brosnan*

Department of Psychology, University of Bath, UK

*Correspondence should be addressed to M. J. Brosnan, Department of Psychology, University of Bath, Bath BA2 7AY, UK (e-mail: M.J.Brosnan@Bath.ac.uk).
Table 1. Mean digit ratios and standard deviations for sample subgroups

Factor   N   Level                   Mean digit ratio  SD

Gender   83  Male                    0.987             0.03
         24  Female                  0.984             0.02
Faculty  33  HaSS/Management         0.977             0.03
         43  Science                 0.996             0.03
         31  Engineering             0.984             0.03
Level    46  Lecturer                0.987             0.03
         27  Senior Lecturer         0.987             0.03
         11  Reader                  0.978             0.03
         23  Professor               0.989             0.03
Males     7  with no children        0.996             0.02
Males    27  with children           0.982             0.03
Parent    6  Child with dyslexia     1.004             0.01
Parent   43  Child without dyslexia  0.985             0.03
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Author:Brosnan, Mark J.
Publication:British Journal of Psychology
Date:Nov 1, 2006
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