Time of pubertal onset, testosterone levels and intelligence in 47,XXY males Netley C. Time of pubertal onset, testosterone levels and intelligence in 47,XXY males. Clin Genet 1992: 42: 31-34.
C. Netley Department of Psychology, Lakehead University, Thunder Bay, Ontario, Canada
This study examined the relations between verbal and performance IQs, time of pubertal onset and testosterone levels from 13 to 16 years of age in a sample of 30 males with a supernumerary X chromosome. The findings indicated that verbal IQs measured prior to puberty, during puberty and at mid-adolescence were strongly related to relatively early pubertal onset and testosterone levels. Performance IQs had little or no relationship with the same variables. m e results are discussed in terms of several different psychobiological models.
A number of investigators (Anne11et al. 1970, Netley & Rovet 1982, Ratcliffe et al. 1982, Walzer et al. 1986) have reported that males with a 47,XXY
karyotype frequently have verbal IQ (V1Q)s that are significantly lower than their performance IQ (P1Q)s. However, other studies (Funderburk & Ferjo 1978, Robinson et al. 1982) have not found such discrepancies in the intellectual abilities of extra X males and, even in those which have reported mean differences in IQs, specific deficits in verbal ability have not been present in all cases (Walzer et al. 1986). A colleague and I in a previous publication reported findings which accounted for a portion of this variability in pre-pubertal 47,XXY males; VIQs were particularly depressed in cases with a distinctive dermatoglyphic anomaly and atypical patterns of hemispheric organization (Netley & Rovet 1987). In this paper data are presented that point to additional correlates of VIQ in extra X males, both prior to puberty and later during the course of sexual maturation. This line of enquiry was suggested by findings indicating that the timing of pubertal onset and the androgenic events which accompany sexual maturation are sometimes associated with intra-individual differences in verbal and performance intellectual abilities in chromosomally normal males and females (Karlson 1990, Waber 1976, 1977). Subjects and methods
The intellectual, pubertal and hormonal data available for analysis were collected during the course
Key words: intelligence - puberty
- 47Jm
- testosterone
Prof. C. Netley, Dept. of Psychology. Lakehead University, Thunder Bay, Ontario, Canada, P7B 5El Received 23 May 1991. revised 7 February, accepted for publiition 12 February 1992
of a longitudinal study of individuals with X and Y aneuploid conditions, all of whom were identified by neonatal screening (Stewart et al. 1986). Thirty extra X males (47,XXY, n =26;47,XXY/ 46XY, n = 4) with complete intellectual assessments were the focus of the present study. They had been tested with the Wechsler Intelligence Scale for Children-Revised (WISC-R, 1974) prior to puberty (PP) at a mean age of 9.3 years (SD= 1.3), during puberty (DP) at a mean age of 13.4 years (SD= 1.4) and at a mean age of 16.6 years (SD= 1.2) when the majority had reached the limits of their sexual maturity (SM). In some cases, the last assessments were conducted using the Wechsler Adult Intelligence Scale-Revised (WAIS-R, 1981). There were no significant differences between the VIQs and PIQs of the boys with 47,XXY karyotypes and those with 47,xXY/46,xX karyotypes at the PP, DP and SM assessments. For this reason, their results were combined in subsequent analyses. Observations concerning pubertal development and hormonal functioning were obtained at annual assessments carried out as close as possible to each boy’s birthday. Blood samples, drawn from 13 to Table 1. Mean (SD) verbal la (via)$., mean (SD) performance IQ(PQs prior to puberty (PP), during puberty (DP) and at sexual maturity (SM) of 30 males with supernumerary X chromosome
PP DP SM
via
Pia
t
P
85.2 (14.9) 84.9 (15.2) 82.2 (13.7)
101.7 (13.1) 101.0 (12.9) 98.9 (13.5)
5.50 6.12 6.13
CO.01 CO.01 C 0.01
31
Netley Table 2. Correlations between VIQ and PI0 prior to puberty (PP). during puberty (DP) and at Sexual maturity (SM) in 30 extra X males. P values in brackets
PP
-
via DP
PP
via
PP DP SM
0.91 (0.00) 0.86 (0.00)
0.92 (0.00)
-
Pia
PP DP SM
0.45 (0.00) 0.46 (0.01) 0.54 (0.00)
0.52 (0.00) 0.48 (0.00) 0.53 (0.00)
0.45 (0.00) 0.44 (0.01) 0.53 (0.00)
-
16 years in all but a few cases, were analyzed by a radioimmunoassay procedure to provide measurements of testosterone (T). In addition, assessments of pubertal status using the criteria of Tanner and his associates (Tanner & Whitehouse 1976) were conducted annually and the age at which pubic hair development began (P2) was noted. It is recognized that this methodology was not perfectly precise since assessments were conducted at 12-month intervals. However, any errors of measurement were unlikely to be systematic. There were no significant differences between 47,XXY boys and 47,XXY/46,XY in P2 or T values from 13 to 16 years of age. Their data were combined in later analyses. Resutts
The intelligence test results obtained at the three testings are presented in Table 1. They indicate that the mean VIQs were lower than the corresponding mean PIQs at the three stages of development and imply a stable pattern of intellectual functioning from prior to puberty to maturity. This conclusion is supported by the intercorrelations between the various IQs which are presented in Table 2; internal correlations between the VIQ and PIQ scores are high across the three ages of testing (above 0.85 for VIQ and above 0.68 for PIQ). The correlations between VIQs and PIQs are somewhat lower, implying some degree of independence between these abilities in extra X males. The mean of pubertal onset as indicated by the development of pubertal hair (p2) and the mean levels of T from 13 to 16 years of age are shown in Table 3. None of these values is outside normal limits (Gupta et al. 1975, Tanner & Whitehouse 1976). The correlations between these variables are presented in Table 4 and are generally statistically significant if the measurements were obtained at similar times, but tend to fall to insignificance as the ages at assessment diverge. Intercorrelations between the intellectual variables, VIQ and PIQ, and those reflecting pubertal change are presented in Table 5. They indicate
32
SM
0.89 (0.00) 0.71 (0.00)
Pta DP
SM
-
-
0.69 (0.00)
the development of pubic hair (P2) is negatively correlated with VIQs at all three assessments and, further, that VIQs at all ages are positively correlated with T levels at all but one combination of maturational stage and T (SM and T at 13 years). In contrast, PIQs at all ages are unrelated to P2 and also unrelated to T levels at most ages.
Discussion The findings in this study are significant for a number of reasons. First, they indicate that the age of pubertal onset and subsequent levels of testosterone are related to intellectual functioning in extra X males. Second, they show that these relationships are much stronger for verbal ability than for nonverbal ability. Third, the relationships between the behavioural and biological variables are evident at widely different points in times of measurement. (By way of contrast, it should be noted that this is not true of the biological variables themselves since their associations are significant only when they are proximal in terms of times of measurement.) Fourth, the relationships observed do not depend on sexual maturation, as VIQ prior to puberty is related to subsequent pubertal events. Finally, the findings have a bidirectional character, in that early hormonal events and the timing of puberty are related to later intellectual abilities, and early IQs are related to later pubertal events. Several mechanisms have been proposed to account for results similar to the present ones in clinical groups with idiopathic precocious puberty (Money & Meredrith 1967, Meyer-Bahlburg et al.
Table 3. Mean (SD) age of P2 pubic hair development (P2) and mean (SD) testosterone levels (nmoVI from 13 to 16 years in extra X males) ~
p2 (YS) T (13 yrs) T (14 Yrs)
T (16 (15 Yyrs) W
~
Mean (SD)
N
12.61 (1.24) 4.70 (4.87) 9.93 (9.75) 12.76 (5.49) 15.28 (5.22)
30 29 28 28 29
Time of pubertal onset Table 4. Intercorrelations between age of pubc hair onset (P2) and testosterone levels (T) from 13 to 16 years in extra X males. Sample size and significance levels shown in brackets
T P2 13 yrs 14 yrs 15 yrs 16 yrs
13 yrs
14 yrs
15 yrs
16 yrs
-0.66 (29, 0.00) -0.46 0.65 (28. 0.01) (28, 0.00) -0.32 0.41 0.47 (28, 0.05) (28, 0.02) (27, 0.01) -0.23 0.25 0.31 0.61 (29, NS) (28. NS) (27. NS) (28. 0.00)
1985) as well as nonclinical samples (Waber 1976, 1977)'. One of these postulates a direct neurochemical effect of hormones on central nervous system functioning (Gordon & Lee 1986, Hier & Crowley 1982). This is .improbable in the case of extra X males since the associations between variables reflecting sexual maturation and abilities exist prior to the onset of puberty and also when these functions are measured at widely different points of time. A second mechanism proposed to explain associations between pubertal events and abilities is more plausible. This makes reference to maturation rates and argues that the speed of biological development has consequences not only for sexual growth but also for brain function and, therefore, abilities (Weber 1976, 1977). If this is the case in extra X males, it is probable that puberty and Table 5. Correlations of age of pubic hair onset (P2) and testosterone levels (T) from 13 to 16 years with verbal ia (via). performance ia ( P q prior to puberty (PP). during puberty (DP) and at sexual maturity (SM) in extra X males. Upper panel shows Via correlations and h e r panel PIQ correlations. Sample sizes and signifiice levels presented in brackets PP
DP
SM
via P2 13 yrs
T
14yn 75 yrs 16 yn
-0.45 (30. 0.01) -0.37 (30.0.02) -0.35 (30, 0.03) 0.35 (29. 0.03) 0.36 (29, 0.03) 0.29 (29, NS) 0.42 (28, 0.01) 0.44 (28, 0.01) 0.33 (28, 0.04) 0.52 (28. 0.00) 0.53 (28. 0.00) 0.43 (28, 0.011 0.47 (29. 0.01) 0.46 (29, 0.01) 0.36 (29, 0.03)
Pia
P2 T
'
13 yrs 1 4 p 15 yn 16 yrs
0.12 (30, NS) -0.08 (30, NS) -0.18 (30, NS) 0.37 (29, 0.03) 0.32 (29. 0.05) 0.18 (29, NS) 0.11 (28, NS) 0.08 (28, NS) 0.02 (28, NS) 0.23 (28, NS) 0.24 (28, NS) 0.25 (28, NS) 0.25 (29, NS) 0.32 (29, 0.04) 0.15 (29, NS)
An explanation framed in terms of genetic mechanisms, such as an adverse effect on brain development directly proportional to the amount of extra X material present, is unlikely to be correct, as the 47,XXY and the 47.XXYJ46.XY boys do not differ in terms of VIQ or PIQ.
subsequent levels of T do not have direct effects on their intellectual functioning. Rather, they appear to serve as markers for maturational processes which are operative prior to puberty as well as later during development. Given our previously reported findings that a prenatally fixed dermatoglyphic index of fetal growth is related to cerebral organization and intellectual functioning in prepubertal extra X males (Netley & Rovet 1982, Netley & Rovet 1987), it is possible that individual differences in a maturational gradient from conception to maturity are responsible for variations in their abilities, especially their verbal abilities, both prior to puberty and afterwards.
References Annell AL, Gustavson KH, Tenstam J. Symptomatology in schoolboys with positive sex chromatin (the Klinefelter syndrome). Acta Psychiatr Scand 1970 46: 71-80. Funderburk SJ, Ferjo N. Clinical observations in Klinefelter (47,XXY) syndrome. J Ment Defic Res 1978: 22: 207-212. Gordon, HW, Lee PA. A relationship between gonadotropins and visuospatial function. Neuropsychologia 1986 2 4 563-576. Gupta D, Attanasio A, Raaf A. Plasma estrogen and androgen concentrations in children during adolescence. J Clin Endocrho1 Metab 1975: 40: 636-643. Hier DB, Crowley WF. Spatial ability in androgen deficient men. N Engl J Med 1982: 306: 1202-1205. Karlson JA. Time of puberty onset and intellectual and neuropsychological functioning. In: Holmes CS, ed. Psychoneuroendocrinology: Brain, behavior and hormonal interactions. New York Springer-Verlag, 1990. Meyer-Bahlburg HFL, Bruder GE, Feldman JF, Ehrhardt AA, Healey JM, Bell J. Cognitive abilities and hemispheric lateralization in females following idiopathic precocious puberty. Develop Psychol 1985: 21: 878-887. Money J, Merednth T. Elevated verbal IQ and idiopathic precocious sexual maturation. Pediatr Res 1967: 1: 59-65. Netley C, Rovet J. Verbal deficits in children with 47,XXY and 47,XXX karyotypes: a descriptive and experimental study. Brain t a n g 1982 17: 58-72. Netley C, Rovet J. Relations between a dermatoglyphic measure, hemispheric specialization and intellectual abilities in 47,XXY males. Brain Cognit 1987: 6: 153-160. Ratcliffe SG, Bancroft J, Axworthy D, McLaren W. Klinefelter's syndrome in adolescence. Arch Dis Child 1982: 57: 6-12. Robinson A, Bender B, Borelli J, Puck M, Salbenblatt V, Webber ML. Sex chromosomal abnormalities (SCA): a prospective and longitudinal study of newborns identified in an unbiased manner. Birth Defects 1982: 18: 7-39. Stewart DA, Bailey JD, Netley CT,Rovet J, Park E. Growth and development from early to mid-adolescence of children with X and Y chromosome aneuploidy: the Toronto study. Birth Defects 1986: 22: 119-182. Tanner JM, Whitehouse RH. Clinical longitudinal standards for height, weight, height velocity, weight velocity, and stages of puberty. Arch Dis Child 1976: 51: 170-179. Waber DP. Sex differences in cognition: a function of maturation rate? Science 1976: 1929: 572-574. Waber DP. Sex differences in mental abilities, hemispheric lateralization. and rate of physical growth at adolescence. Develop Psychol 1977: 13: 29-38.
33
Netley Walzer S. Bashir A. Graham 1, Silbert A, Lange N, De Napoli M, Richmond J. Behavioral development of boys with X chromosome aneuploidy: impact of reactive style on the educational intervention for learning deficits. Birth Defects 1986: 2 2 1-21.
34
Wechsler Intelligence Scale for Children-Revised. New York The Psychological Corporation. 1974. Wechsler Adult Intelligence Scale-Revised. New York: The Psychological Corporation, 198 I.
C. Netley Department of Psychology, Lakehead University, Thunder Bay, Ontario, Canada
This study examined the relations between verbal and performance IQs, time of pubertal onset and testosterone levels from 13 to 16 years of age in a sample of 30 males with a supernumerary X chromosome. The findings indicated that verbal IQs measured prior to puberty, during puberty and at mid-adolescence were strongly related to relatively early pubertal onset and testosterone levels. Performance IQs had little or no relationship with the same variables. m e results are discussed in terms of several different psychobiological models.
A number of investigators (Anne11et al. 1970, Netley & Rovet 1982, Ratcliffe et al. 1982, Walzer et al. 1986) have reported that males with a 47,XXY
karyotype frequently have verbal IQ (V1Q)s that are significantly lower than their performance IQ (P1Q)s. However, other studies (Funderburk & Ferjo 1978, Robinson et al. 1982) have not found such discrepancies in the intellectual abilities of extra X males and, even in those which have reported mean differences in IQs, specific deficits in verbal ability have not been present in all cases (Walzer et al. 1986). A colleague and I in a previous publication reported findings which accounted for a portion of this variability in pre-pubertal 47,XXY males; VIQs were particularly depressed in cases with a distinctive dermatoglyphic anomaly and atypical patterns of hemispheric organization (Netley & Rovet 1987). In this paper data are presented that point to additional correlates of VIQ in extra X males, both prior to puberty and later during the course of sexual maturation. This line of enquiry was suggested by findings indicating that the timing of pubertal onset and the androgenic events which accompany sexual maturation are sometimes associated with intra-individual differences in verbal and performance intellectual abilities in chromosomally normal males and females (Karlson 1990, Waber 1976, 1977). Subjects and methods
The intellectual, pubertal and hormonal data available for analysis were collected during the course
Key words: intelligence - puberty
- 47Jm
- testosterone
Prof. C. Netley, Dept. of Psychology. Lakehead University, Thunder Bay, Ontario, Canada, P7B 5El Received 23 May 1991. revised 7 February, accepted for publiition 12 February 1992
of a longitudinal study of individuals with X and Y aneuploid conditions, all of whom were identified by neonatal screening (Stewart et al. 1986). Thirty extra X males (47,XXY, n =26;47,XXY/ 46XY, n = 4) with complete intellectual assessments were the focus of the present study. They had been tested with the Wechsler Intelligence Scale for Children-Revised (WISC-R, 1974) prior to puberty (PP) at a mean age of 9.3 years (SD= 1.3), during puberty (DP) at a mean age of 13.4 years (SD= 1.4) and at a mean age of 16.6 years (SD= 1.2) when the majority had reached the limits of their sexual maturity (SM). In some cases, the last assessments were conducted using the Wechsler Adult Intelligence Scale-Revised (WAIS-R, 1981). There were no significant differences between the VIQs and PIQs of the boys with 47,XXY karyotypes and those with 47,xXY/46,xX karyotypes at the PP, DP and SM assessments. For this reason, their results were combined in subsequent analyses. Observations concerning pubertal development and hormonal functioning were obtained at annual assessments carried out as close as possible to each boy’s birthday. Blood samples, drawn from 13 to Table 1. Mean (SD) verbal la (via)$., mean (SD) performance IQ(PQs prior to puberty (PP), during puberty (DP) and at sexual maturity (SM) of 30 males with supernumerary X chromosome
PP DP SM
via
Pia
t
P
85.2 (14.9) 84.9 (15.2) 82.2 (13.7)
101.7 (13.1) 101.0 (12.9) 98.9 (13.5)
5.50 6.12 6.13
CO.01 CO.01 C 0.01
31
Netley Table 2. Correlations between VIQ and PI0 prior to puberty (PP). during puberty (DP) and at Sexual maturity (SM) in 30 extra X males. P values in brackets
PP
-
via DP
PP
via
PP DP SM
0.91 (0.00) 0.86 (0.00)
0.92 (0.00)
-
Pia
PP DP SM
0.45 (0.00) 0.46 (0.01) 0.54 (0.00)
0.52 (0.00) 0.48 (0.00) 0.53 (0.00)
0.45 (0.00) 0.44 (0.01) 0.53 (0.00)
-
16 years in all but a few cases, were analyzed by a radioimmunoassay procedure to provide measurements of testosterone (T). In addition, assessments of pubertal status using the criteria of Tanner and his associates (Tanner & Whitehouse 1976) were conducted annually and the age at which pubic hair development began (P2) was noted. It is recognized that this methodology was not perfectly precise since assessments were conducted at 12-month intervals. However, any errors of measurement were unlikely to be systematic. There were no significant differences between 47,XXY boys and 47,XXY/46,XY in P2 or T values from 13 to 16 years of age. Their data were combined in later analyses. Resutts
The intelligence test results obtained at the three testings are presented in Table 1. They indicate that the mean VIQs were lower than the corresponding mean PIQs at the three stages of development and imply a stable pattern of intellectual functioning from prior to puberty to maturity. This conclusion is supported by the intercorrelations between the various IQs which are presented in Table 2; internal correlations between the VIQ and PIQ scores are high across the three ages of testing (above 0.85 for VIQ and above 0.68 for PIQ). The correlations between VIQs and PIQs are somewhat lower, implying some degree of independence between these abilities in extra X males. The mean of pubertal onset as indicated by the development of pubertal hair (p2) and the mean levels of T from 13 to 16 years of age are shown in Table 3. None of these values is outside normal limits (Gupta et al. 1975, Tanner & Whitehouse 1976). The correlations between these variables are presented in Table 4 and are generally statistically significant if the measurements were obtained at similar times, but tend to fall to insignificance as the ages at assessment diverge. Intercorrelations between the intellectual variables, VIQ and PIQ, and those reflecting pubertal change are presented in Table 5. They indicate
32
SM
0.89 (0.00) 0.71 (0.00)
Pta DP
SM
-
-
0.69 (0.00)
the development of pubic hair (P2) is negatively correlated with VIQs at all three assessments and, further, that VIQs at all ages are positively correlated with T levels at all but one combination of maturational stage and T (SM and T at 13 years). In contrast, PIQs at all ages are unrelated to P2 and also unrelated to T levels at most ages.
Discussion The findings in this study are significant for a number of reasons. First, they indicate that the age of pubertal onset and subsequent levels of testosterone are related to intellectual functioning in extra X males. Second, they show that these relationships are much stronger for verbal ability than for nonverbal ability. Third, the relationships between the behavioural and biological variables are evident at widely different points in times of measurement. (By way of contrast, it should be noted that this is not true of the biological variables themselves since their associations are significant only when they are proximal in terms of times of measurement.) Fourth, the relationships observed do not depend on sexual maturation, as VIQ prior to puberty is related to subsequent pubertal events. Finally, the findings have a bidirectional character, in that early hormonal events and the timing of puberty are related to later intellectual abilities, and early IQs are related to later pubertal events. Several mechanisms have been proposed to account for results similar to the present ones in clinical groups with idiopathic precocious puberty (Money & Meredrith 1967, Meyer-Bahlburg et al.
Table 3. Mean (SD) age of P2 pubic hair development (P2) and mean (SD) testosterone levels (nmoVI from 13 to 16 years in extra X males) ~
p2 (YS) T (13 yrs) T (14 Yrs)
T (16 (15 Yyrs) W
~
Mean (SD)
N
12.61 (1.24) 4.70 (4.87) 9.93 (9.75) 12.76 (5.49) 15.28 (5.22)
30 29 28 28 29
Time of pubertal onset Table 4. Intercorrelations between age of pubc hair onset (P2) and testosterone levels (T) from 13 to 16 years in extra X males. Sample size and significance levels shown in brackets
T P2 13 yrs 14 yrs 15 yrs 16 yrs
13 yrs
14 yrs
15 yrs
16 yrs
-0.66 (29, 0.00) -0.46 0.65 (28. 0.01) (28, 0.00) -0.32 0.41 0.47 (28, 0.05) (28, 0.02) (27, 0.01) -0.23 0.25 0.31 0.61 (29, NS) (28. NS) (27. NS) (28. 0.00)
1985) as well as nonclinical samples (Waber 1976, 1977)'. One of these postulates a direct neurochemical effect of hormones on central nervous system functioning (Gordon & Lee 1986, Hier & Crowley 1982). This is .improbable in the case of extra X males since the associations between variables reflecting sexual maturation and abilities exist prior to the onset of puberty and also when these functions are measured at widely different points of time. A second mechanism proposed to explain associations between pubertal events and abilities is more plausible. This makes reference to maturation rates and argues that the speed of biological development has consequences not only for sexual growth but also for brain function and, therefore, abilities (Weber 1976, 1977). If this is the case in extra X males, it is probable that puberty and Table 5. Correlations of age of pubic hair onset (P2) and testosterone levels (T) from 13 to 16 years with verbal ia (via). performance ia ( P q prior to puberty (PP). during puberty (DP) and at sexual maturity (SM) in extra X males. Upper panel shows Via correlations and h e r panel PIQ correlations. Sample sizes and signifiice levels presented in brackets PP
DP
SM
via P2 13 yrs
T
14yn 75 yrs 16 yn
-0.45 (30. 0.01) -0.37 (30.0.02) -0.35 (30, 0.03) 0.35 (29. 0.03) 0.36 (29, 0.03) 0.29 (29, NS) 0.42 (28, 0.01) 0.44 (28, 0.01) 0.33 (28, 0.04) 0.52 (28. 0.00) 0.53 (28. 0.00) 0.43 (28, 0.011 0.47 (29. 0.01) 0.46 (29, 0.01) 0.36 (29, 0.03)
Pia
P2 T
'
13 yrs 1 4 p 15 yn 16 yrs
0.12 (30, NS) -0.08 (30, NS) -0.18 (30, NS) 0.37 (29, 0.03) 0.32 (29. 0.05) 0.18 (29, NS) 0.11 (28, NS) 0.08 (28, NS) 0.02 (28, NS) 0.23 (28, NS) 0.24 (28, NS) 0.25 (28, NS) 0.25 (29, NS) 0.32 (29, 0.04) 0.15 (29, NS)
An explanation framed in terms of genetic mechanisms, such as an adverse effect on brain development directly proportional to the amount of extra X material present, is unlikely to be correct, as the 47,XXY and the 47.XXYJ46.XY boys do not differ in terms of VIQ or PIQ.
subsequent levels of T do not have direct effects on their intellectual functioning. Rather, they appear to serve as markers for maturational processes which are operative prior to puberty as well as later during development. Given our previously reported findings that a prenatally fixed dermatoglyphic index of fetal growth is related to cerebral organization and intellectual functioning in prepubertal extra X males (Netley & Rovet 1982, Netley & Rovet 1987), it is possible that individual differences in a maturational gradient from conception to maturity are responsible for variations in their abilities, especially their verbal abilities, both prior to puberty and afterwards.
References Annell AL, Gustavson KH, Tenstam J. Symptomatology in schoolboys with positive sex chromatin (the Klinefelter syndrome). Acta Psychiatr Scand 1970 46: 71-80. Funderburk SJ, Ferjo N. Clinical observations in Klinefelter (47,XXY) syndrome. J Ment Defic Res 1978: 22: 207-212. Gordon, HW, Lee PA. A relationship between gonadotropins and visuospatial function. Neuropsychologia 1986 2 4 563-576. Gupta D, Attanasio A, Raaf A. Plasma estrogen and androgen concentrations in children during adolescence. J Clin Endocrho1 Metab 1975: 40: 636-643. Hier DB, Crowley WF. Spatial ability in androgen deficient men. N Engl J Med 1982: 306: 1202-1205. Karlson JA. Time of puberty onset and intellectual and neuropsychological functioning. In: Holmes CS, ed. Psychoneuroendocrinology: Brain, behavior and hormonal interactions. New York Springer-Verlag, 1990. Meyer-Bahlburg HFL, Bruder GE, Feldman JF, Ehrhardt AA, Healey JM, Bell J. Cognitive abilities and hemispheric lateralization in females following idiopathic precocious puberty. Develop Psychol 1985: 21: 878-887. Money J, Merednth T. Elevated verbal IQ and idiopathic precocious sexual maturation. Pediatr Res 1967: 1: 59-65. Netley C, Rovet J. Verbal deficits in children with 47,XXY and 47,XXX karyotypes: a descriptive and experimental study. Brain t a n g 1982 17: 58-72. Netley C, Rovet J. Relations between a dermatoglyphic measure, hemispheric specialization and intellectual abilities in 47,XXY males. Brain Cognit 1987: 6: 153-160. Ratcliffe SG, Bancroft J, Axworthy D, McLaren W. Klinefelter's syndrome in adolescence. Arch Dis Child 1982: 57: 6-12. Robinson A, Bender B, Borelli J, Puck M, Salbenblatt V, Webber ML. Sex chromosomal abnormalities (SCA): a prospective and longitudinal study of newborns identified in an unbiased manner. Birth Defects 1982: 18: 7-39. Stewart DA, Bailey JD, Netley CT,Rovet J, Park E. Growth and development from early to mid-adolescence of children with X and Y chromosome aneuploidy: the Toronto study. Birth Defects 1986: 22: 119-182. Tanner JM, Whitehouse RH. Clinical longitudinal standards for height, weight, height velocity, weight velocity, and stages of puberty. Arch Dis Child 1976: 51: 170-179. Waber DP. Sex differences in cognition: a function of maturation rate? Science 1976: 1929: 572-574. Waber DP. Sex differences in mental abilities, hemispheric lateralization. and rate of physical growth at adolescence. Develop Psychol 1977: 13: 29-38.
33
Netley Walzer S. Bashir A. Graham 1, Silbert A, Lange N, De Napoli M, Richmond J. Behavioral development of boys with X chromosome aneuploidy: impact of reactive style on the educational intervention for learning deficits. Birth Defects 1986: 2 2 1-21.
34
Wechsler Intelligence Scale for Children-Revised. New York The Psychological Corporation. 1974. Wechsler Adult Intelligence Scale-Revised. New York: The Psychological Corporation, 198 I.
