Upload
talat
View
213
Download
1
Embed Size (px)
Citation preview
623
Intern. J. Neuroscience, 114:623–637, 2004Copyright Taylor & Francis Inc.ISSN: 0020-7454 / 1543-5245 onlineDOI: 10.1080/00207450490430499
SERUM TESTOSTERONE, GROWTHHORMONE, AND INSULIN-LIKE GROWTHFACTOR–1 LEVELS, MENTAL REACTION
TIME, AND MAXIMAL AEROBIC EXERCISEIN SEDENTARY AND LONG-TERM
PHYSICALLY TRAINED ELDERLY MALES
ZEKI ARICelal Bayar UniversityFaculty of Medicine, Department of BiochemistryManisa, Turkey
NECIP KUTLUCelal Bayar UniversityFaculty of Medicine, Department of PhysiologyManisa, Turkey
BEKIR SAMI UYANIKFATMA TANELICelal Bayar UniversityFaculty of Medicine, Department of BiochemistryManisa, Turkey
GURBUZ BUYUKYAZICelal Bayar UniversityPhysical Education School, Department of SportsManisa, Turkey
Received 21 July 2003.Address correspondence to Dr. Zeki Ari, Department of Biochemistry, Celal Bayar Univer-
sity School of Medicine, Manisa, Turkey. E-mail: [email protected]
Int J
Neu
rosc
i Dow
nloa
ded
from
info
rmah
ealth
care
.com
by
Uni
vers
ity o
f M
elbo
urne
on
10/2
9/14
For
pers
onal
use
onl
y.
624 Z. Ari et al.
TALAT TAVLICelal Bayar UniversityFaculty of Medicine, Department of CardiologyManisa, Turkey
The aim of the study was to investigate the effect of regular exercise onmaximum oxygen uptake capacity (VO
2max), reaction time (RT), testosterone
(T), growth hormone (GH), insulin-like growth factor-I (IGF-I) in ath-letes compared to sedentary controls. VO
2max, RT, T, GH, and IGF-I
levels were 31.2 ± 6.2 ml/min/kg, 106.7 ± 23.2 s, 8.3 ± 1.3 ng/mL, 1.6± 0.7 ng/mL, 106.5 ± 27.0 ng/mL in master athlete group and 18.8 ±5.1 ml/min/kg, 148.3 ± 39.3 s, 5.4 ± 1.7 ng/mL, 0.8 ± 0.3 ng/mL, 90.2± 23.8 ng/mL in sedentary control group, respectively. The differencesbetween regularly exercising males and the control group of sedentarymales were found to be statistically significant. The results showed thatlong-term exercise decreased RT and increased VO
2max, T, and GH in
elderly males; elevated serum T and GH levels may be advantageousfor brain functions.
Keywords aging, exercise, growth hormone, insulin-like growth factor-1,reaction time, testosterone
Physical work capacity (aerobic capacity) declines with aging. Thebest physiological measurement of this capacity is performed usinga maximal O
2 consumption capacity test. Because there is a decline
in all capacities with aging, a decrease in maximum oxygen uptakecapacity (VO
2max) with aging is considered normal. However, the
decline is slow in people who perform endurance training exercises.Several reports have suggested that chronic exercise may have fa-cilitating effects on cognitive function. Physical training is said toattenuate age-related differences in cognitive performance (Bashore& Goddard, 1993; Dustman, Emmerson, & Shearer, 1994; Dustmanet al., 1984, 1990; Hawkins et al., 1992; Spirduso, 1980). Age-related differences in performance of some cognitive tasks are at-tenuated in subjects performing high compared to low physical ex-ercise (Dustman et al., 1984; Spirduso, 1980; Baylor & Spirduso,1988), although sound effects are not always obtained (Blumenthal& Madden 1988; Dustman et al., 1994). Exercisers at all ages aresuperior to sedentary individuals on tests of various types of cogni-tive function, especially those cognitive functions that require infor-mation processing speed. Although findings concerning aerobic fitness
Int J
Neu
rosc
i Dow
nloa
ded
from
info
rmah
ealth
care
.com
by
Uni
vers
ity o
f M
elbo
urne
on
10/2
9/14
For
pers
onal
use
onl
y.
T, GH, IGF-I, Mental Reaction Time 625
effects on mental functioning are more contradictory for the youngthan for the old, a positive influence of aerobic fitness is also re-ported in young men (Dustman et al., 1990; Stones & Kozma, 1988).Similar to physical training, acute exercise is assumed to facilitatemental functioning.
The effects of acute exercise on cognitive performance are classi-cally explained by an activation of the central nervous system withthe assumption that exercise-induced physical arousal leads to anarrowing of attention focus (Cote et al., 1992). However, relationsbetween exercise and physical arousal do not appear to be clarifiedyet (Anderson, 1990). Moreover, the terminology of arousal andrelated states is still disputed, as well as the unidimensionality of therelationship between arousal and performance (Arcelin, Delignieres,& Brisswaiter, 1998). Uyanik et al. (1997) reported decreased serumlevels in free testosterone (FT) and total testosterone (T) in elderlymen. It is generally accepted that sex hormones may influence thecognitive performance in human beings. For example, Money andMeredith (1967) showed elevated full-scale IQ in precocious puberty.Galatzer et al. (1984) cited that high IQ is associated with bothprecocious puberty and precocious adrenarche. The sex hormoneswere also reported to alter spatial performance in rodents (Joseph etal., 1978; Stewart et al., 1975). Roof and Havens (1992) showed thesexual dimorphism in the granule cell layer of hippocampus of ratsand found a strong correlation between the size of granule cell layersand maze performance; neonatal testosterone treatment of femalesresulted in a more male-like hippo campus. Tan (1990a, 1990b)reported that nonverbal intelligence is directly related to serum totaltestosterone level in right-handed young men. Tan and Akgun (1992)confirmed these results in right-handed young men using a differentsample. Tan et al. (1993) reported that nonverbal spatial reasoningability is directly associated with the efficiency of left brain, which isfavored by testosterone in male left-handers. Moreover, it was re-ported by Tan and Tan (1998) that the serum T may be advantageousfor the fluid intelligence in men, as expected from an evolutionarystandpoint. In contrast, Moffat and Hampson (1996) pointed to aninverted U shaped curvilinear relation across sexes between T andspatial performance: males showed a distinct negative linear functionand females a positive linear function. On the other hand, Nyborg’s
Int J
Neu
rosc
i Dow
nloa
ded
from
info
rmah
ealth
care
.com
by
Uni
vers
ity o
f M
elbo
urne
on
10/2
9/14
For
pers
onal
use
onl
y.
626 Z. Ari et al.
theory (1983) accentuates the inverse U-shaped relation between T(as a precursor of estradiol) and spatial intelligence (Petersen, 1976).When all the previous reports are taken into consideration, the recentpublications point to an optimal balance between female and malehormones. In other words, superior spatial ability is associated withmore male hormones for females and less male hormones for males(Halpern, 2000). Petersen (1976) postulated an inverted U-shapedcurvelinear function between spatial ability and gonad hormones,ranging from extreme feminine to extreme masculine with androgenyat the peak. Kutlu et al. (2001) found that nonverbal intelligence (IQ)is directly related to serum total testosterone level in right-handedyoung men.
To understand better the effects of chronic exercise on brain func-tioning, mental reaction time (RT) is considered a valuable tool forthe measurement of cognitive function because it is thought to re-flect neural activity underlying basic aspects of cognition. Severalstudies have investigated the effect of aerobic fitness and exerciseon brain function activity, which can be considered an index ofcortical arousal. Mental reaction time (RT) is considered to reflectbasic cognitive processes (Donchin & Coles, 1988). To evaluate theaerobic fitness level a maximally graded exercise test is performedon a cycle ergometer in all subjects, permitting measurements ofVO
2max. Indeed, the VO
2max, which is a measure of oxygen capacity
reported in millimeters of oxygen consumption per kilogram of bodymass per minute, is generally accepted as the best single measure ofphysical fitness (Howley et al., 1995) The present study attemptedto determine whether the cognitive function T, GH, and IGF-I mightbe affected by the maximal long-time aerobic exercise in the masterathletes exercising regularly and in the sedentary elderly male.
MATERIALS AND METHODS
Master athletes exercising regularly (n = 10; age, 68 ± 6 yrs; height,167 ± 8 cm; weight, 71 ± 3 kg) and a control group living sedentarily(n = 11; age, 65 ± 5 yrs; height, 169 ± 5 cm; weight, 82 ± 11 kg)were included in present study. Astrand test (VO
2max) was applied to
the two groups, but before the test, the groups were advised not toexercise heavily. T, GH, IGF-1, and RT were measured at the same
Int J
Neu
rosc
i Dow
nloa
ded
from
info
rmah
ealth
care
.com
by
Uni
vers
ity o
f M
elbo
urne
on
10/2
9/14
For
pers
onal
use
onl
y.
T, GH, IGF-I, Mental Reaction Time 627
time and at the same fitness center. Each person was examined forthe neurological, physical, and mental aspects and was questionedfor a history of migraine, psychological disorder, diabetes, hyper-tension, epilepsy, cancer, and alcohol, and smoking habits. The VO
2max
measurement was conducted on a calibrated bicycle ergometer (Morark,860, Varberg, Sweden) using Astrand protocol (Astrand, 1986). RTwas assessed by general vocational aptitude test (Model: 1309, TakeiScientific Instruments Co. Ltd. Tokyo, Japan).
Venous blood samples were obtained from all subjects followingan overnight (10 h) fasting, and sera were stored at –70ºC for batchanalysis. Serum T levels were measured by a commercial immu-noassay method (ACS: 180 Automated Chemiluminescence Sys-tem, Chiron Diag. Corp., East Walpole, MA, USA), which is acompetitive ìmmunoassay that uses direct, chemiluminescent tech-nology. Method sensitivity was 0.1 ng/mL, with intra- and inter-assay CV% being 4.8 and 6.5, respectively (Boscato & Stuart, 1988).Serum GH concentrations were assessed by an immunometric assay(Immulite Analyzer, Diagnostic Products Corp.; DPC, Los Angeles,CA, USA). The sensitivity of this method was 0.01 ng/mL, withintra- and inter-assay CV% being 5.2 and 5.9, respectively (Na-tional Committee for Clinical Laboratory Standards, 1991). SerumIGF-I level was determined by a commercial enzyme-linked immuno-sorbent assay (ELISA, Diagnostic Systems Laboratories; DSL, Texas,USA). The method had a sensitivity of 0.01 ng/mL and intra- andinter-assay CV% of 4.9 and 7.7, respectively (Daughaday & Rot-wein, 1989).
Linear regressions analysis (Spearman’s rho) was used for serumT, GH, IGF-I levels and other parameters. Differences in analysesbetween the groups were evaluated by Mann-Whitney U test, and pvalues of less than
.05 were considered significant.
RESULTS
The means of age, body composition, fat percentage, training age,and week age properties of the study groups are shown in Table 1.The findings related to VO
2max, RT, T, GH, and IGF-I in the master
athletes and the sedentary group are summarized in Table 2. Thevalues of VO
2 in the master athletes group were 31.2 ± 6.2 ml/min/kg
Int J
Neu
rosc
i Dow
nloa
ded
from
info
rmah
ealth
care
.com
by
Uni
vers
ity o
f M
elbo
urne
on
10/2
9/14
For
pers
onal
use
onl
y.
628 Z. Ari et al.
and in the sedentary group 18.8 ± 5.1 ml/min/kg. The difference wasstatistically significant (p < .001). On the other hand, a statisticallysignificant difference (p < .05) in RT values was found between thetwo groups (106.7 ± 23.2 s in the master athletes and 148.3 ± 39.3 s inthe control group).
The T levels were found to be 8.3 ± 1.3 ng/mL in the masterathletes and 5.4 ± 1.7 ng/mL in the control group. The differencewas highly significant (p < .01). A similar statistically significantdifference (p < .01) was detected in mean ± SD of GH (1.6 ± 0.7ng/mL in the master athletes and 0.8 ± 0.3 ng/mL in the controlgroup). The mean ± SD values of IGF-I were 106.5 ± 27.0 ng/mLin the master athletes group and 90.2 ± 23.8 ng/mL in the controlgroup, with the difference of no significance. Figure 1 and Figure 2show the box plots of measured parameters in the master athletesand the sedentary group. The relationship between the training ageand T (A), GH (B), IGF-I (C) in the master athletes is exhibited inFigure 3. The relationship between RT and T (A), GH (B) in themaster athletes is shown in Figure 4.
TABLE 1. Mean and SD values of age, body composition, fat %, training age, andweek age of the two groups
Age Height Mass Fat Training age Week ageGroups (yrs) (cm) (kg) % (yrs) (hrs)
Study (n = 10) 68 ± 6 167 ± 8 71 ± 3 14 ± 2 41 ± 18 10 ± 9Control (n = 11) 65 ± 5 169 ± 5 82 ± 11* 18 ± 2** – –
All values are given as mean ± SD.*p < .05, ** p < .01 2-tailed value-Mann-Whitney U test.
TABLE 2. Mean and SD values of aerobic capacity (VO2max
), reaction time (RT), totaltestosterone (T), growth hormone (GH), and insulin-like growth factor-I (IGF-I) intwo groups
VO2max RT T GH IGF-IGroups (ml/min/kg) (s) (ng/mL) (ng/mL) (ng/mL)
Study(n = 10) 31.2 ± 6.2 106.7 ± 23.2 8.3 ± 1.3 1.6 ± 0.7 106.5 ± 27.0
Control(n = 11) 18.8 ± 5.1*** 148.3 ± 39.3* 5.4 ± 1.7** 0.8 ± 0.3** 90.2 ± 23.8
All values are given as mean ± SD.*p < .05, ** p < .01, ***p < .001 2-tailed value-Mann-Whitney U test
Int J
Neu
rosc
i Dow
nloa
ded
from
info
rmah
ealth
care
.com
by
Uni
vers
ity o
f M
elbo
urne
on
10/2
9/14
For
pers
onal
use
onl
y.
T, GH, IGF-I, Mental Reaction Time 629
(A)
(B)
(C)
FIGURE 1. Box plots of the serum T (A), GH (B) and IGF-I (C) levels in master athleteand sedentary groups.
Int J
Neu
rosc
i Dow
nloa
ded
from
info
rmah
ealth
care
.com
by
Uni
vers
ity o
f M
elbo
urne
on
10/2
9/14
For
pers
onal
use
onl
y.
630 Z. Ari et al.
FIGURE 2. Box plots of VO2 (A) and RT (B) in master athlete and sedentary groups.
Int J
Neu
rosc
i Dow
nloa
ded
from
info
rmah
ealth
care
.com
by
Uni
vers
ity o
f M
elbo
urne
on
10/2
9/14
For
pers
onal
use
onl
y.
T, GH, IGF-I, Mental Reaction Time 631
FIGURE 3. The relationship between the training age and testosterone (A; y = 6.9 +0.03x), growth hormone (B; y = 1.4 + 0.006x), IGF-I (C; y = 101.7 + 0.12x) in masterathlete group.
180
(A)
(B)
(C)
Int J
Neu
rosc
i Dow
nloa
ded
from
info
rmah
ealth
care
.com
by
Uni
vers
ity o
f M
elbo
urne
on
10/2
9/14
For
pers
onal
use
onl
y.
632 Z. Ari et al.
FIGURE 4. The relationship between the reaction time and testosterone (A; y = 234 –15.4x), growth hormone (B; y = 121 – 8.7x) in master athlete group.
Int J
Neu
rosc
i Dow
nloa
ded
from
info
rmah
ealth
care
.com
by
Uni
vers
ity o
f M
elbo
urne
on
10/2
9/14
For
pers
onal
use
onl
y.
T, GH, IGF-I, Mental Reaction Time 633
The descriptive data of aerobic capacity, RT, T, GH, and IGF-Iin the master athletes group and the sedentary group and the resultsof Spearman’s rho correlation analysis are shown in Table 3. Thecorrelations of T-RT and T-GH are of statistical significance inmaster athlete group and age-T, age-RT, and T-RT in controls.
DISCUSSION
This study planned to investigate any possible relationship betweencognitive ability and serum T, GH, and IGF-I concentrations in themaster athletes exercising regularly and in the sedentary elderly male.In several previous studies, Gouchie and Kimura (1991) and Moffatand Hampson (1996) determined the salivary FT concentrations toinvestigate the relationship between salivary FT and IQ because thesaliva contains only FT, the biologically active form of T. However,it is reasonable to measure the serum T level in studies of the cog-nitive abilities for the following reasons. It is known that serum Texists in three forms: free, albumin-bound, and sex hormone-bind-ing globulin (SHBG)-bound (Herzog, 1988). Only about 2% of T isin free form, 43–45% bound to SHBG, and 53–55% bound to albu-min. The SHBG-bound T fraction is not biologically active (Sodergardet al., 1982; Cumming & Wall, 1985). On the other hand, the large
TABLE 3. Descriptive data for VO2max
, RT, T, GH, and IGF-I in masterathletes and sedentary groups
Master athlete group Sedentary group
r p r p
Age-T .210 .561 –.710 .014*Age-GH –.077 .832 –.400 .223Age-IGF-1 –.142 .696 .196 .563Age-RT –.370 .293 .650 .030*Age-VO2max –.346 .328 –.540 .086T-RT –.800 .005** –.655 .029*T-VO2max .067 .855 .460 .154RT-VO2max .394 .260 –.141 .679T-GH .754 .012* .588 .057GH-IGF-I –.237 .510 .425 .193
*p < .05, **p < .01 Spearman’s rho correlation.
Int J
Neu
rosc
i Dow
nloa
ded
from
info
rmah
ealth
care
.com
by
Uni
vers
ity o
f M
elbo
urne
on
10/2
9/14
For
pers
onal
use
onl
y.
634 Z. Ari et al.
pool of T that is loosely bound to albumin is available to tissues(Cumming & Wall, 1985) and thus, the measurement of non-SHBG-bound T, rather than free T, may provide a more sensitive assess-ment of biologically significant androgen levels (Herzog, 1988).
It is well known that GH and IGF-I contribute to the function ofthe hippocampus, a brain structure important for the maintenance ofcognitive functions such as learning and memory. Evidence for cog-nitive deficits in GH deficient individuals has been reported in vari-ous studies, some of which cite that these deficits could be reversedby GH substitution therapy. Several studies mentioned that GH orIGF-I deficiency could contribute to the deterioration of cognitivefunctions observed in the elderly (Rollero et al., 1998; Aleman etal., 2000; Van Dam et al., 2000).
The results of the present study provided evidence that there wasa positive correlation between the serum T, GH, IGF-I and the mentalfunctions in men attending long-term exercise. This can be con-firmed by the fact that there was a positive correlation between thetraining age and T, GH, IGF-I and that there was a negative corre-lation between RT and T, GH in the master athlete group.
In a previous study (Struder et al., 1999), the mental functionsinfluenced by hypothalamic-pituitary-adrenal and -gonadal activitywere also assessed in athletes and the sedentary before and after thetraining program. In another study, an inverted U-shaped curvelinearrelationship between T and IQ was reported (Kutlu et al., 2001). This,however, is not consistent with the salivary T results, indicating aninverse relation of T to spatial ability in men, which is reported byGouchie and Kimura (1991) and Moffat and Hampson (1996).
There was no U-shaped relationship between T and IQ in seden-tary men. Instead, IQ progressively increased with T. Thus, only thelow T levels were associated with low IQ in these subjects, andhigh T levels were advantageous for this kind of intelligence, i.e.,the fluid intelligence, which was consistent with some of the previ-ous studies (Benbow, 1988; Christiansen, 1993; Christiansen & Knuss-man, 1987; Dawson, 1972; Hier & Crowley, 1982; Janowsky et al.,1994; Tan 1990a, 1990b; Tan & Akgun, 1992; Tan et al., 1993; Tan& Tan, 1998) and was inconsistent with some studies reporting aninverse correlation between T and spatial abilities in men (Gouchie& Kimura, 1991; Moffat & Hampson, 1996; Schute et al., 1983).
Int J
Neu
rosc
i Dow
nloa
ded
from
info
rmah
ealth
care
.com
by
Uni
vers
ity o
f M
elbo
urne
on
10/2
9/14
For
pers
onal
use
onl
y.
T, GH, IGF-I, Mental Reaction Time 635
The present study indicated that long-term exercise decreasedevent-related mental reaction time and increased maximal oxygenuptake capacity. Aerobic fitness was assessed by measuring VO
2max,
which is generally accepted as the best single measure of physicalfitness (Howley et al., 1995). The VO
2max in subjects performing
long-term regular exercise training was found to be greater than thatof the sedentary individuals (p < .01). The findings related to men-tal reaction time and maximal oxygen uptake capacity showed thepositive effects of exercise training on humans, being parallel tofindings in previous reports (Mucci et al., 1999). The relationshipbetween fitness and mental reaction is not yet well understood.
Physical
training was proposed to be effective in brain function by severalmechanisms, including enhanced cerebral blood flow, improved ce-rebral neurotransmitter function and balance, and enhanced neuro-endocrine and autonomic tone. Because it was suggested that thisrelationship may be explained by increased circulatory capacity, itis particularly interesting to study the effects of fitness level relatedto an aerobic physical activity such as cycling (Polich & Kok, 1995).
On the basis of the results obtained, the authors conclude thatlong-term exercise decreases RT and increases VO
2max, T, and GH
in elderly males and that the elevated serum T and GH levels maybe advantageous for brain functions because cerebral organizationmay be essential for the effect of T and GH on cognitive abilities.
REFERENCES
Anderson, K. J. (1990). Arousal and the inverted-U hypothesis: A critique of Neiss’s recon-ceptualizing arousal. Psychological Bulletin, 107, 96–100.
Aleman, A., de Vries, W. R., Deijen, J. B., van der Veen, E. A., de Haan, E. H., & Koppeschaar,H. P. (2000), Growth hormone, insulin-like growth factor I and cognitive function inadults. Growth Hormone & IGF Research, 10(Suppl B), 69–73.
Arcelin, R., Delignieres, D., & Brisswaiter, J. (1998). Selective effects of physical exer-cise on choice reaction processes. Perceptual and Motor Skills, 87, 175–185.
Astrand, P. O., & Rodahl, K. (1986). Textbook of work physiology. McGraw Hill Co.Bashore, T. R., & Goddard, P. H. (1993). Preservative and restorative effects of aerobic
fitness on the age related slowing of mental speed. In J. Cerella, J. Rhybash, & W.Hoyer (Eds.), Adult information processing: Limits on loss (pp. 205–228). New York:Academic Press.
Baylor, N. M., & Spirduso, W. W. (1988). Systematic aerobic exercise and components ofreaction time in older women. Journal of Gerontology: Psychological Sciences, 43,121–126.
Benbow, C. P. (1988). Sex differences in mathematical reasoning ability in intellectually
Int J
Neu
rosc
i Dow
nloa
ded
from
info
rmah
ealth
care
.com
by
Uni
vers
ity o
f M
elbo
urne
on
10/2
9/14
For
pers
onal
use
onl
y.
636 Z. Ari et al.
talented preadolescents: Their nature, effects, and possible causes. Behavioral and BrainSciences, 2, 169–232.
Blumenthal, J., & Madden, D. (1988). Effects of aerobic exercise training, age, and physi-cal fitness on memory-search performance. Psychology and Aging, 3, 280–285.
Boscato, L. M., & Stuart, M. C. (1988). Heterophylic antibodies: A problem for all immu-noassays. Clinical Chemistry, 34, 27–33.
Christiansen, K. (1993). Sex hormone-related variations of cognitive performance in KungSan Huntergatherers of Namibia. Neuropsychobiology, 27, 97–107.
Christiansen, K., & Knussman, R. (1987). Sex hormones and cognitive functioning in men.Neuropsychobiology, 18, 27–36.
Cote, I., Salmela, J., & Papathanasopoulu, K. P. (1992). Effects of progressive exercise onattentional focus. Perceptual and Motor Skills, 75, 351–354.
Cumming, D. C., & Wall, S. R. (1985). Non-sex hormone binding globulin and boundtestosterone as a marker for hypogonadism. Journal of Clinical Endocrinology andMetabolism, 61, 873–876.
Dawson, J. L. (1972). Effects of sex hormones on cognitive style in rats and men. Behav-ioral Genetics, 2, 21–42.
Daughaday, E., & Rotwein, P. (1989). Insulin like growth factors I and II. Peptide, mes-senger ribonucleic acid and gene structures, serum and tissue concentrations. Endo-crine Reviews, 10, 68–91.
Donchin, E., & Coles, M. G. H. (1988). Is the P300 component a manifestation of contextupdating? Behavioral and Brain Sciences, 11, 357–374.
Dustman, R. E., Emmerson, R., & Shearer, D. (1994). Physical activity, age, and cognitiveneuropsychological function. Journal of Aging and Physical Activity, 2, 143–181.
Dustman, R. E., Emmerson, R. Y., & Shearer, D. E. (1990). Electrophysiology and aging:Slowing inhibition, and aerobic fitness. In M. L. Howe, M. J. Stones, & C. J. Brainerd(Eds.), Cognitive and behavioral performance factors in atypical aging (pp. 103–149).New York: Springer-Verlag.
Dustman, R. E., Ruhling, R., Russell, E., Shearer, D. E., Bonekat, H., Shigeoka, J., Wood,J., & Bradford, D. (1984). Aerobic exercise training and improved neuropsychologicalfunction of older individuals. Neurobiology of Aging, 5, 35–42.
Galatzer, A., Beth-Halachimi, N., Kauli, R., & Lazon, Z. (1984). Intellectual function ofgirls with precocious puberty. Pediatrics, 74, 246–249.
Gouchie, C., & Kimura, D. (1991). The relationship between testosterone levels and cog-nitive ability patterns. Psychoneuroendocrinology, 16, 323–334.
Halpern, D. F. (2000). In sex differences in cognitive abilities. Mahwah, New Jersey; Lon-don: Lawrence Association Publishers.
Hawkins, H. L., Kramer, A. F., & Capaldi, D. (1992). Aging, exercise, and attention. Psy-chology and Aging, 7, 643–653.
Herzog, A. G. (1988). Testosterone, free testosterone, and non-sex hormone-binding globulin-bound testosterone, and free androgen index: Which testosterone measurement is mostrelevant to reproductive and sexual function in men with epilepsy. Archive of Neurol-ogy, 49, 133–134.
Hier, D. B., & Crowley, W. F. (1982). Spatial ability in androgen-deficit men. New En-gland Journal of Medicine, 306, 1202–1205.
Howley, E. T., Bassett, D. R. J., & Welch, H. G. (1995). Criteria for maximal oxygenuptake: Review and commentary. Medicine and Science in Sports and Exercise, 27,1292–1301.
Joseph, R., Hess, E., & Birecree, S. (1978). Effects of hormone manipulations and explo-ration on sex differences in maze learning. Behavioral Biology, 24, 364–377.
Janowsky, J. S., Oviatt, S. K., & Orwoll, E. S. (1994). Testosterone influences spatialcognition in older men. Behavioral Neuroscience, 108, 325–332.
Kutlu, N., Ekerbiçer, N., Ari, Z., Uyanik, B. S., Zeren, T., & Tan, U. (2001). Testosteroneand nonverbal intelligence in right-handed men with successful and unsuccessful edu-cational levels. International Journal of Neuroscience, 111, 1–9.
Moffat, S., & Hampson, E. (1996). A curvilinear relationship between testosterone and
Int J
Neu
rosc
i Dow
nloa
ded
from
info
rmah
ealth
care
.com
by
Uni
vers
ity o
f M
elbo
urne
on
10/2
9/14
For
pers
onal
use
onl
y.
T, GH, IGF-I, Mental Reaction Time 637
spatial cognition in humans: possible influence of hand preference. Psychoneuroendo-crinology, 21, 323–337.
Money, J., & Meredith, T. (1967). Elevated verbal IQ and idiopathic precocious sexualmaturation. Pediatric Research, 1, 59–65
Mucci, P., Anselme-Poujol, F., Couert, I., Rossi, M., & Prefaut, C. (1999). Basophil re-leasability in young highly trained and older athletes. Medicine and Science in Sportsand Exercise, 31(4), 507–513.
National Committee for Clinical Laboratory Standards (1991). Procedures for the collectionof diagnostic blood specimens by venipuncture, 3rd ed., NCCLS Document, H3–A3.
Nyborg, H. (1983). Spatial ability in men and women: Review and new theory. Advancesin Behavior Research and Therapy, 5, 89–140.
Petersen, A. C. (1976). Physical androgeny and cognitive functioning in adolescence. Develop-mental Psychology, 12, 524–533.
Polich, J., & Kok, A. (1995). Cognitive and biological determinants of P300: An integra-tive review. Biological Psychology, 41, 103–146.
Rollero, A., Murialdo, G., Fonzi, S., & Simone, G. (1998). Relation between cognitivefunction, growth hormone and insulin-like growth hormone and insulin-like growthfactor I plasma levels in aged subjects. Neuropsychobiology, 38(2), 73–79.
Roof, R. L., & Havens, M. D. (1992). Testosterone improves maze performance and in-duces development of a male hippocampus in females. Brain Research, 572, 310–313.
Schute, V. J., Pellegrino, J. W., Hubert, L., & Reynolds, R. W. (1983). The relationshipbetween androgen levels and human spatial abilities. Bulletin of the Psychonomic So-ciety, 21, 465–468.
Sodergard, R., Backstrom, T., Shanbhag, V., & Carstensen, H. (1982). Calculation of freeand bound fractions of testosterone and estradiol-17 beta to plasma proteins at bodytemperature. Journal of Steroid Biochemistry and Molecular Biology, 16, 801–810.
Spirduso, W. W. (1980). Physical fitness, aging and psychomotor speed: A review. Jour-nal of Gerontology, 35, 850–865.
Stewart, J, Skvarenina, A., & Pottier, J. (1975). Effects of neonatal androgens open-fieldbehavior and maze learning in the prepubescent and adult rat. Physiology and Behav-ior, 14, 291–295.
Stones, M. J., & Kozma, A. (1988). Physical activity, age, and cognitive motor perfor-mance. In M. L. Howe & C. J. Brainerd (Eds.), Cognitive development in adulthood:Progress in cognitive development research (pp. 273–321). New York: Springer Verlag.
Struder, H. K., Hollmann, W., Platen, P., Rost, R., Weicker, H., Kirchhof, O., & Weber,K. (1999). Neuroendocrine system and mental function in sedentary and endurance-trained elderly males. International Journal of Sports Medicine, 20(3), 159–166.
Tan, U. (1990a). Testosterone and nonverbal intelligence in right handed men and women.International Journal of Neuroscience, 54, 277–282.
Tan, U. (1990b). Relationship of testosterone and nonverbal intelligence to hand prefer-ence and hand skills in right handed young adults. International Journal of Neuro-science, 54, 283–290.
Tan, U., & Akgun, A. (1992). There is a direct relationship between nonverbal intelli-gence and serum testosterone level in young men. International Journal of Neuroscience,64, 213–216.
Tan, U., Akgun, A., & Telatar, M. (1993). Relationships among nonverbal intelligence,hand speed and serum testosterone level in left-handed male subjects. InternationalJournal of Neuroscience, 71, 21–28.
Tan, U., & Tan, M. (1998). Curvelinear correlations between total testosterone levels and fluidintelligence in men and women. International Journal of Neuroscience, 95, 77–83.
Uyanik, B. S., Ari, Z., Gümüs, B., Yigitoglu, M. R., & Arslan, T. (1997). Beneficial ef-fects of testosterone undecanoate on the lipoprotein profiles in healthy elderly men: Aplacebo controlled study. Japanese Heart Journal, 38, 73–82.
Van Dam, P. S., Aleman, A., de Vries, W. R., Deijen, J. B., van der Veen, E. A., de Haan,E. H., & Koppeschaar, H. P. (2000). Growth hormone, insulin-like growth factor I andcognitive function in adults. Growth Hormone & IGF Research, 10 (Supp. B), 69–78.
Int J
Neu
rosc
i Dow
nloa
ded
from
info
rmah
ealth
care
.com
by
Uni
vers
ity o
f M
elbo
urne
on
10/2
9/14
For
pers
onal
use
onl
y.