1687

Intern. J. Neuroscience, 115:1687–1709, 2005Copyright 2005 Taylor & Francis Inc.ISSN: 0020-7454 / 1543-5245 onlineDOI: 10.1080/00207450590958556

AGE AND SEX DIFFERENCES INNEUROBEHAVIORAL PERFORMANCE:A STUDY OF PORTUGUESE ELEMENTARYSCHOOL CHILDREN

ISABEL PAVÃO MARTINSALEXANDRE CASTRO-CALDAS

Centro de Estudos Egas Moniz, IMMFaculty of Medicine, University of LisbonLisbon, Portugal

BRENDA D. TOWNES

Department of Psychiatry and Behavioral SciencesUniversity of Washington, School of MedicineSeattle, Washington, USA

GORETTY FERREIRAPEDRO RODRIGUESSUSANA MARQUES

School of Dental MedicineUniversity of LisbonLisbon, Portugal

GAIL ROSEBAUM

Department of Psychiatry and Behavioral SciencesUniversity of Washington, School of MedicineSeattle, Washington, USA

Received 1 December 2004.This project has been funded by the National Institute of Dental and Craniofacial Research Coop-

erative Agreement U01 DE11894.Address correspondence to Dr. Isabel Pavão Martins, MD, PhD, Department of Neurology, Centro

de Estudos Egas Moniz, Hospital de Sta Maria 1600 Lisbon, Portugal. E-mail: labling@mail.telepac.pt

1688 I. P. MARTINS ET AL.

TONYA S. BENTON

Department of Dental Public Health SciencesUniversity of Washington, School of DentistrySeattle, Washington, USA

JORGE LEITÃO

School of Dental MedicineUniversity of LisbonLisbon, Portugal

TIMOTHY DEROUEN

Department of Dental Public Health SciencesUniversity of Washington, School of DentistrySeattle, Washington, USA

In this study normative data were obtained on measures of IQ, visual/motor,motor and memory functions among Portuguese elementary school children.Subjects were 228 females and 275 males, 8.0 to 11.9 years of age, in grades 2through 4, who participated in a dental study. Performance on all tests im-proved with increasing age. Females performed better in rote verbal learning,psychomotor speed, and speed of information processing. Males had higherscores on tests of visual learning, visual memory, and fine motor speed andcoordination. Nonverbal IQ had a significant impact on all tests except motorspeed and coordination. Results represent an initial attempt to evaluate Portu-guese children in educational and medical settings.

Keywords age and sex differences, children, normative data

INTRODUCTION

Neuropsychological tests developed primarily in English and for Anglo-Saxonculture are often used in Portuguese- and Spanish-speaking countries (namelyin Latin America) and in Hispanic patients in the USA. However, there are veryfew measures (Mungas et al., 2000; Pontón et al., 1996; Ostrosky-Solís etal., 1999; Reye et al., 1999) with appropriate norms for those specific popu-lations. In practice, tests from these cultures are compared against theoriginal norms, which may induce errors in the interpretation of results. Cul-ture, spoken language, age, educational level and teaching practices, the degree

NEUROBEHAVIORAL PERFORMANCE IN CHILDREN 1689

of acculturation, and socioeconomic class all have an impact on neuropsycho-logical test performance (Lee et al., 2000; Pérez-Arce, 1999; Pontón et al.,1996). These factors may be particularly relevant in the evaluation of childrenbecause language and cultural influences may modulate the speed, pattern, andstyle of cognitive development as well as the likelihood of suffering a develop-mental disorder, like dyslexia (Lindgren et al., 1985; Paulesu et al., 2001). Thebehavioral assessment of developmental disorders is also dependent on thecultural context (Pineda et al., 2000). The comparison of normative data amongdifferent stages of development and cultures may help in the understanding ofthe sociobiological bases of behavior and, eventually, how they change thefunctional organization of the brain (Castro-Caldas et al., 1998).

The cross-cultural comparisons may also help in the understanding ofsex differences in development. Sex-specific differences in the brain havebeen found by noninvasive neuro-imaging studies, namely in the left hemi-sphere language areas in adults and in children (Blanton et al., 2004; Shaywitzet al., 1995). Although these studies corroborate sex differences in perfor-mance on verbal learning and other verbal tasks (Kramer et al., 1997), theydo not unveil underlying factors, because environmental stimulation modifiesthe development of the normal brain, as has been demonstrated in healthyilliterate adults (Castro-Caldas et al., 1998). However, behavioral studies per-formed in different cultural contexts may reveal the roles played by bio-logical and environmental factors in the emergence of sex differences inbehavior and provide an approach for examining the neurobiology of sex andcultural differences.

The specific aims of the study were to obtain normative data amonghealthy Portuguese children on a diverse set of neurobehavioral tests. Thelong-term goal was to obtain normative information to use in clinical studies.

METHODS

Participants

Participants were students of seven primary schools in Lisbon, Portugal, whowere enrolled in 1997 in a longitudinal investigation about the effects ofdental mercury amalgams in children (DeRouen et al., 2002). This is a col-laborative study conducted by the University of Lisbon Faculty of DentalMedicine and the Faculty of Medicine (Department of Neurology), the De-partment of Dental Public Health Sciences at the University of Washingtonand the National Institute of Dental and Craniofacial Research. Selected schools

1690 I. P. MARTINS ET AL.

belong to a public organization of social welfare, founded in the late 18thcentury, to provide free education to children coming from unfavorable so-cioeconomic and/or family environments. Its attendance changed over thelast two centuries, and it now includes children from diverse socioeconomicconditions including those whose parents pay tuition to enroll their children.In Lisbon, it comprises seven normal elementary and secondary schools andtwo schools for the deaf (all with residential and nonresidential pupils). Chil-dren from these seven normal schools, who were in grades 2nd through 4th,were screened to participate in this longitudinal international study.

With Institutional Review Board and parental or guardian approval, 507children, ages 8 to 12, were enrolled in the study. Criteria for inclusion in thestudy were: (a) need for restorative dental treatment with no dental amalgamsin place, as verified by oral examination; (b) normal urinary mercury levels(defined as less than 10 µg/1); (c) blood lead levels less than 15 µg/dl; (d) nohistory of severe medical illness; and (e) IQ equal to or greater than 67 asmeasured by the Comprehensive Test of Nonverbal Intelligence (CTONI)(Hammill et al., 1997). In the present clinical experience scores on the CTONI(and its earlier version) ranged up to one standard deviation below U.S.norms for individuals of similar educational level, when used among non-U.S.-born subjects in cross-cultural contexts (e.g., Egypt and Turkey). Inaddition, it has been shown (Lassiter et al., 2001) that CTONI nonverbal IQunderestimates fluid intelligence, that is, broad reasoning devoid of culturalfactors (Horn & Cattel, 1996), when compared with other IQ measures thatdiscriminate fluid from crystallized intelligence. Because of this test bias, alower IQ boundary of 67 instead of 70 was chosen as the inclusion criteria.This included 11 children with an IQ of 69, 13 with an IQ of 68, and 5 withan IQ of 67. This appeared to be a natural break as there were no childrenwith an IQ of 66 and 34 children with an IQ between 55 and 65.

Five hundred and seven children were included in the study. Participantswere divided into four age groups: (1) 8.0 to 8.9 (n = 73); (2) 9.0 to 9.9 (n =143); (3) 10.0 to 10.9 (n = 203); and (4) 11.0 to 11.9 (n = 84). The foursubjects who were 12 years of age were dropped from this aspect of thestudy, resulting in a total sample of 503 children. Demographic characteris-tics of the participants are shown in Table 1. There were 228 females (45.3%)and 275 males (54.7%), all of whom were native Portuguese speakers. Themajority (69.8%) were Caucasian, 29% were Afro-Portuguese and 1.2% Asian-Portuguese. Most children (93.8%) were right handed. There were no signifi-cant differences between the four age groups in terms of sex, ethnicity, orIQ. Data concerning socioeconomic status (SES) were not collected because

NEUROBEHAVIORAL PERFORMANCE IN CHILDREN 1691

it was felt that asking children about their parents’ occupation might seem tobe too intrusive.

Procedures

Prior to randomization and dental treatment, participants were individuallyadministered a battery of neurobehavioral tests by a psychometrist trained(by GR) in test administration and scoring.

Instruments

The battery included the following tests: CTONI (Hammill et al., 1997); ReyAuditory Verbal Learning test (RAVLT) (Lezak, 1995); Visual Learning (VLT)and Finger Windows subtests from the Wide Range Assessment of Memoryand Learning (Sheslow & Adams, 1990); Digit Span (DSp), Coding (Cod)and Symbol Search (SS) subtests from the Wechsler Intelligence Scale forChildren—III (Wechsler, 1991); Trail Making Test (TMT) parts A and B(Reitan & Davison, 1974); Stroop Color Word Test (Stroop) (Golden, 1978);

Table 1. Participant characteristics by age and sex

Age

8.0–8.9 9.0–9.9 10.0–10.9 11.0–11.9

Males:N 37 79 113 46Caucasian 54% 67% 74% 67%Right hand 92% 92% 96% 84%IQ:

Mean 86.05 86.25 85.52 83.35SD 9.06 10.16 10.06 10.71Range 68–103 68–116 67–108 167–110

Females:N 36 64 90 38Caucasian 72% 70% 72% 71%Right hand 94% 92% 98% 100%IQ:

Mean 84.89 85.16 85.38 82.05SD 9.09 11.33 8.91 9.83Range 68–102 67–118 67–107 67–110

1692 I. P. MARTINS ET AL.

Standard Reaction Time (SRT) (Anger, 1985); Finger Oscillation Test (adaptedfrom Reitan and Davison [1974] by Western Psychological Services) (FOT);Pegboard (Peg), Matching (Match), and Drawing (Draw) subtests from theWide Range Assessment of Visual Motor Abilities (Adams & Sheslow, 1995).Tests are described in the Appendix.

Tests were chosen on the basis of their appropriateness for the age of thechildren, documented sensitivity to the integrity of brain functions, and ap-propriateness for measuring abilities in each of three functional domains andintelligence memory (short and long term, verbal and visual memory), atten-tion/executive functions (brief and sustained attention plus speed of infor-mation processing and freedom from distractibility) and motor/visuomotorfunctions. The Matching test (problem solving), Trail Making B (cognitiveflexibility), and Stroop Color Word (inhibition) comprise a small subset oftests related to executive functions. Linguistic functions were not included(except for the verbal memory tests) because of the difficulty of adaptingthese tests in cross-cultural settings and because the impact of mercury inbrain functions, if any, was expected to be primarily in the areas of attention,memory, and (visual) motor functions. The administration of the entire testbattery took 2 h.

Statistical Analysis

To establish normative information, means and standard deviations for eachtest variable were computed separately for ages 8.0 to 8.9 (n = 73), 9.0 to 9.9(n = 143), 10.0 to 10.9 (n = 203) and 11.0 to 11.9 (n = 84). Two-wayANOVAs were performed on each variable to determine potential differ-ences in age, gender, and age by sex interactions. The significance of groupdifferences was calculated by subsequent Tukey tests.

Two (age) by four (IQ) ANOVAs were computed separately for each offour measured nonverbal IQ groups on the CTONI: IQ1 (ranging from 67–79) (n = 166), IQ2 (80–89) (n = 175), IQ3 (90–99) (n = 116), and IQ4 (equalor greater than 100) (n = 46). The two age groups were younger children(aged 8–9.9 years) (n = 216) and older children (10.0–11.9 years) (n = 287).

RESULTS

A summary of participants’ scores on the neurobehavioral tests by age areshown for the group as a whole (Table 2) and for males and females sepa-rately (Table 3). The number of participants varies slightly from test to test

NEUROBEHAVIORAL PERFORMANCE IN CHILDREN 1693

Tab

le 2

.M

eans

and

sta

ndar

d de

viat

ions

of

neur

obeh

avio

ral

mea

sure

s by

age

Age

8.0

–8.9

9

.0–9

.9

10.

0–10

.9

11.0

–11.

9

n

= 7

3

n =

143

n

= 2

03

n =

84

Dom

ain/

Tes

tM

ean

SD

Mea

nS

DM

ean

SD

Mea

nS

DF

Tuk

ey

Inte

llig

ence

CT

ON

I-1

2.56

1.77

3.29

2.17

3.70

2.38

4.89

3.04

13.9

0***

1, 2

< 2

, 3

< 4

CT

ON

I-2

1.58

1.91

2.40

2.81

2.89

3.00

3.97

3.43

5.90

**1,

2 <

2,

3, 4

CT

ON

I-3

7.99

2.43

8.58

2.52

8.92

2.43

9.29

2.47

4.19

**1,

2 <

2,

3, 4

CT

ON

I-4

10.2

74.

2811

.34

3.98

12.3

24.

0412

.81

3.13

7.37

***

1, 2

< 2

, 3

< 3

, 4

CT

ON

I-5

5.53

3.04

6.90

3.38

8.36

3.32

8.95

3.44

19.7

8***

1 <

2 <

3,

4C

TO

NI-

64.

262.

275.

542.

696.

782.

927.

043.

3918

.79*

**1

< 2

< 3

, 4

Mem

ory

VL

T-L

earn

18.7

37.

8420

.58

8.22

22.2

38.

6122

.74

9.28

4.17

**1,

2 <

2,

3, 4

VL

T-M

emor

y5.

932.

866.

262.

996.

843.

086.

933.

302.

46R

AV

LT

-13.

971.

534.

221.

674.

801.

584.

581.

526.

65**

*1,

2 <

2,

3 <

3,

4R

AV

LT

-58.

932.

589.

382.

7110

.09

2.96

10.3

42.

985.

00**

1, 2

< 2

, 3,

4R

AV

LT

-64.

111.

734.

541.

774.

831.

794.

741.

543.

34*

1, 2

< 2

, 3,

4R

AV

LT

-77.

452.

627.

612.

788.

612.

879.

022.

697.

84**

*1,

2,

< 3

, 4

RA

VL

T-8

7.30

2.71

7.68

3.01

8.62

2.91

8.95

3.01

7.00

***

1, 2

< 2

, 3

< 3

, 4

RA

VL

T-T

ot34

.26

8.96

36.4

29.

6240

.66

9.39

40.9

68.

8313

.00*

**1,

2 <

3,

4

(Tab

le c

ontin

ues

next

pag

e)

1693

1694 I. P. MARTINS ET AL.

Tab

le 2

.M

eans

and

sta

ndar

d de

viat

ions

of

neur

obeh

avio

ral

mea

sure

s by

age

(C

onti

nued

)

Age

8.0

–8.9

9

.0–9

.9

10.

0–10

.9

1

1.0–

11.9

n =

73

n

= 1

43

n =

203

n =

84

Dom

ain/

Tes

tM

ean

SD

Mea

nS

DM

ean

SD

Mea

nS

DF

Tuk

ey

Att

enti

onD

Sp

9.52

2.19

10.2

32.

6610

.78

3.02

11.0

62.

675.

39**

1, 2

< 2

, 3,

4C

od30

.96

7.15

34.6

68.

3240

.18

8.60

41.8

39.

2234

.25*

**1

< 2

< 3

, 4

SS

17.1

04.

3618

.28

4.11

20.6

24.

5020

.44

4.45

27.7

7***

1, 2

< 3

< 4

Fin

win

9.64

2.35

10.8

32.

9611

.46

2.64

11.4

92.

819.

06**

*1

< 2

, 3,

4T

MT

-A34

.32

12.8

131

.46

14.8

225

.88

11.4

620

.99

7.24

21.7

3***

1 >

2 >

3,

4T

MT

-B82

.86

35.3

276

.65

42.7

757

.89

27.9

249

.23

20.3

822

.67*

**1,

2 >

3,

4T

MT

-Aer

r0.

230.

570.

180.

500.

230.

610.

070.

301.

96T

MT

-Ber

r1.

231.

370.

931.

530.

771.

240.

560.

804.

02**

1, 2

, 3

> 3

, 4

Str

oop-

W44

.73

13.4

551

.39

12.3

058

.94

12.7

862

.67

13.5

431

.36*

**1

< 2

< 3

, 4

Str

oop-

C39

.75

5.94

42.2

88.

4146

.37

8.49

48.9

99.

5521

.48*

**1,

2 <

3,

4S

troo

p-C

W20

.04

6.17

20.3

85.

8822

.03

6.03

22.6

17.

653.

88**

1, 2

, 3

< 2

, 3,

4S

RT

0.96

0.23

0.95

0.20

0.87

0.19

0.82

0.20

10.9

6***

1, 2

> 3

, 4

Mot

or/V

isua

l-M

otor

FO

T-D

om32

.82

5.02

35.4

35.

8337

.66

6.10

38.4

55.

8617

.00*

**1

< 2

< 3

, 4

FO

T-N

D28

.53

4.36

30.3

85.

0632

.74

5.39

33.8

64.

8120

.63*

**1

< 2

< 3

, 4

Peg

-Dom

33.3

75.

3735

.10

5.82

37.9

66.

2338

.43

5.83

16.5

0***

1, 2

< 3

, 4

Peg

-ND

30.3

34.

8232

.64

5.50

35.0

35.

4435

.96

4.94

21.0

7***

1 <

2 <

3,

4D

raw

13.2

72.

0413

.90

1.88

14.4

92.

2615

.01

2.22

10.9

0***

1, 2

< 2

, 3

< 3

, 4

Mat

ch28

.41

4.49

29.9

64.

9832

.19

4.60

32.9

64.

3219

.21*

**1,

2 <

3,

4

*p <

.05;

**p

< .0

1; *

**p

< .0

01.

1694

NEUROBEHAVIORAL PERFORMANCE IN CHILDREN 1695

as not all tests could be administered to every participant, due primarily tooccasional equipment failure.

As expected, children’s performances on all of the neurobehavioral testsrevealed significant age differences (note that scores on the Trail Making andSRT tests are time and error scores and, thus, scores decrease with age).Thirty, out of 32, test scores showed a significant change with age in theexpected direction (Table 3).

Males scored better than females on tests of visual learning [VLT-Learn:F(1,501) = 3.77, p = .05], visual memory (VLT-Mem: F(1,501) = 6.54, p <.02], fine motor speed in the dominant [FOT-Dom: F(1,501) = 10.17, p <.01] and nondominant [FOT-ND: F(1,501) = 29.61, p < .001] hands and inmotor coordination in the nondominant hand [PEG-ND: F(1,500) = 7.73, p <.01]. Females scored better than males on tests of psychomotor speed [F(1,501)= 15.68, p < .001], speed of information processing [Stroop-W: F(1,483) =5.63, p < .05; Stroop-C: F(1,483) = 8.90, p < .01; Stroop-CW: F(1,148) =6.03, p < .01] and initial rote verbal learning [RAVLT-1: F(1,501) = 5.04,p < .05]. Females also made fewer errors on a test of sustained attention andcognitive flexibility [TMT-Berr: F(1,501) = 9.38, p < .01].

As seen in Table 3, age differences for males were present for mosttests. Exceptions were a slight decrease for 11-year-olds, compared with 10-year-olds on tests of visual learning (VLT-Learn: X = 22.11 vs. 23.08),visual memory (VLT-Memory: X = 6.80 vs. 7.37) and initial rote verballearning (RAVLT-1: X = 4.37 vs. 4.71). For females, (Table 3) visual learn-ing (VLT-Learn) of the 9-year-olds was inferior to the 8-year-olds (X =18.70 vs. 19.03) and 11-year-olds made a slightly greater number of errorson a test of cognitive flexibility (TMT-Berr) than 10-year-olds (X = 0.50 vs.0.48). Age differences were significant for 7 out of 11 measures for malesand 9 out of 11 measures for females.

The participants’ performance was divided into four groups according tomeasured IQ on the CTONI: (1) 67 to 79; (2) 80 to 89; (3) 90 to 99; and (4)100 to 118. Each of these 4 groups was further subdivided into youngerchildren (ages 8 and 9 years) and older children (ages 10 and 11 years).Table 4 shows means and standard deviations by IQ and age group (youngerand older). ANOVAs were performed to evaluate the significance of groupdifferences in neurobehavioral performance. As seen earlier, increased agewas associated with improved neurobehavioral performance in all domains.None of the IQ by age interactions was significant.

IQ had a significant impact on neurobehavioral performance in two do-mains. As seen in Table 5, there was a consistent and highly significant effect

1696 I. P. MARTINS ET AL.

Table 3. Means and standard deviations on each of the neurobehavioral measures forthe whole group and for males and females separately

Total group Males Females n = 503 n = 275 n = 228

Domain/Test Mean SD Mean SD Mean SD F

IntelligenceCTONI-1 3.62 2.46 3.65 2.48 3.58 2.45 0.09CTONI-2 2.64 2.93 2.79 2.99 2.46 2.86 1.53CTONI-3 8.75 2.49 8.78 2.49 8.71 2.49 0.12CTONI-4 11.83 4.00 11.72 3.88 11.96 4.13 0.44CTONI-5 7.63 3.50 7.77 3.60 7.47 3.37 0.90CTONI-6 6.10 3.01 6.33 3.13 5.84 2.83 3.32

MemoryVLT-Learn 21.34 8.59 22.01 8.85 20.52 8.21 3.77*VLT-Memory 6.56 3.08 6.88 3.17 6.18 2.92 6.54**RAVLT-1 4.48 1.61 4.33 1.64 4.66 1.61 5.04*RAVLT-5 9.76 2.87 9.80 2.97 9.71 2.76 0.12RAVLT-6 4.63 1.75 4.50 1.66 4.79 1.85 3.37RAVLT-7 8.23 2.84 8.16 3.01 8.31 2.61 0.37RAVLT-8 8.22 2.98 8.21 3.12 8.22 2.82 0.00RAVLT-Tot 38.57 9.64 38.47 9.95 38.70 9.26 0.07

AttentionDSp 10.49 2.79 10.45 2.89 10.53 2.67 0.11Cod 37.55 9.23 36.09 9.42 39.32 8.70 15.68***SS 19.75 4.70 19.41 4.91 20.16 4.42 3.23Finwin 11.02 2.79 11.07 2.72 10.97 2.87 0.16TMT-A 27.87 12.90 27.93 13.41 27.81 12.29 0.01TMT-B 65.40 35.01 66.77 34.75 63.75 35.33 0.93TMT-Aerr 0.19 0.54 0.20 0.54 0.18 0.53 0.06TMT-Berr 0.85 1.30 1.01 1.44 0.65 1.09 9.38**Stroop-W 55.57 14.34 54.11 14.25 57.33 14.29 6.03**Stroop-C 44.75 8.88 43.66 8.93 46.60 8.65 8.90**Stroop-CW 21.39 6.37 20.77 6.07 22.14 6.64 5.63*SRT 0.90 0.20 0.89 0.21 0.90 0.19 0.14

Motor/Visual-MotorFOT-Dom 36.46 6.11 37.24 6.17 35.51 5.92 10.17**FOT-ND 31.65 5.35 32.80 5.42 30.26 4.94 29.61***Peg-Dom 36.56 6.20 36.81 6.07 36.26 6.35 0.97Peg-ND 33.82 5.60 34.45 5.56 33.07 5.57 7.73**Match 31.14 4.90 31.28 5.00 30.96 4.77 0.54Draw 14.23 2.18 14.15 2.25 14.34 2.10 0.97

*p < .05; **p < .01; ***p < .001.

NEUROBEHAVIORAL PERFORMANCE IN CHILDREN 1697

Tab

le 4

.S

core

s on

neu

robe

havi

oral

tes

ts b

y se

x an

d ag

e

Age

8.0

–8.9

9

.0–9

.9

10.

0–10

.9

11.

0–11

.9

n

= 3

7

n =

79

n

= 1

13

n =

46

Dom

ain/

Tes

tM

ean

SD

Mea

nS

DM

ean

SD

Mea

nS

DF

Tuk

ey

MA

LE

Mem

ory

VL

T-L

earn

18.4

37.

8722

.10

8.51

23.0

88.

8022

.11

9.79

2.62

VL

T-M

emor

y5.

843.

066.

702.

947.

373.

036.

803.

802.

36R

AV

LT

-13.

761.

714.

051.

724.

711.

524.

371.

584.

41**

1, 2

, 3

< 2

, 3,

4A

tten

tion

Cod

28.4

65.

8533

.08

8.29

39.3

48.

9139

.39

9.73

20.9

0***

1 <

2 <

3,

4T

MT

-Ber

r1.

381.

381.

081.

741.

001.

410.

610.

772.

09S

troo

p-W

43.6

914

.37

49.6

214

.08

57.9

412

.85

59.5

211

.69

15.0

6***

1, 2

< 3

, 4

Str

oop-

C38

.64

6.33

40.7

98.

3745

.81

8.92

46.9

38.

6811

.45*

**1,

2 <

3,

4S

troo

p-C

W19

.15

4.69

19.9

16.

2921

.79

5.92

20.8

66.

632.

40M

otor

/Vis

ual-

Mot

orF

OT

-Dom

33.1

14.

2735

.90

6.30

38.5

85.

9039

.59

4.89

12.0

6***

1, 2

< 2

, 3

< 3

, 4

FO

T-N

D29

.43

4.62

31.3

45.

4934

.21

5.02

35.0

44.

6414

.66*

**1,

2 <

3,

4P

eg-N

D30

.14

4.67

33.1

35.

0635

.88

5.42

36.7

24.

9616

.29*

**1

< 2

< 3

, 4

(Tab

le c

ontin

ues

next

pag

e)

1697

Tab

le 4

.S

core

s on

neu

robe

havi

oral

tes

ts b

y se

x an

d ag

e (C

onti

nued

)

Age

8.0

–8.9

9

.0–9

.9

10.

0–10

.9

11.

0–11

.9

n

= 3

7

n =

79

n

= 1

13

n =

46

Dom

ain/

Tes

tM

ean

SD

Mea

nS

DM

ean

SD

Mea

nS

DF

Tuk

ey

FE

MA

LE

Mem

ory

VL

T-L

earn

19.0

37.

9118

.70

7.48

21.1

68.

2823

.50

8.70

3.40

*1,

2,

3 <

3,

4V

LT

-Mem

ory

6.03

2.69

5.72

2.99

6.18

3.03

7.08

2.61

1.79

RA

VL

T-1

4.19

1.28

4.44

1.59

4.92

1.65

4.84

1.42

2.57

Att

enti

onC

od33

.53

7.52

36.6

27.

9841

.23

8.12

44.7

97.

6816

.68*

**1,

2 <

3,

4T

MT

-Ber

r1.

081.

360.

751.

210.

480.

910.

500.

833.

18*

1, 2

, 3

> 3

, 4

Str

oop-

W45

.78

12.6

053

.57

12.0

360

.20

12.6

468

.32

14.7

217

.96*

**1

< 2

, 3

< 3

, 4

Str

oop-

C40

.82

5.42

44.1

78.

1447

.08

7.91

51.3

710

.06

11.8

1***

1, 2

< 2

, 3

< 4

Str

oop-

CW

20.9

17.

3020

.98

5.30

22.3

36.

1824

.63

8.31

2.87

*1,

2,

3 <

3,

4M

otor

/Vis

ual-

Mot

orF

OT

-Dom

32.5

35.

7434

.86

5.20

36.5

06.

2037

.08

5.61

5.31

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2 <

2,

3, 4

FO

T-N

D27

.61

3.93

29.5

84.

3830

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5.29

32.4

24.

667.

32**

*1,

2 <

2,

3 <

3,

4P

eg-N

D30

.53

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32.0

55.

9933

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5.30

35.0

54.

845.

98**

1, 2

< 2

, 3

< 3

, 4

*p <

.05;

**p

< .0

1; *

**p

< .0

01.

1698

1699

(Tab

le c

ontin

ues

next

pag

e)

Tab

le 5

. M

eans

, st

anda

rd d

evia

tion

s, a

nd F

tes

ts o

n ne

urob

ehav

iora

l m

easu

res

by f

our

IQ g

roup

s an

d ag

e (y

oung

= 8

–9;

old

= 1

0–11

)

Gro

up

IQ

67–

79

80–8

9

90

–99

1

00

Age

Y

oung

Old

You

ng

Old

Y

oung

Old

You

ng

Old

F

N6

8

98

74

1

01

526

4

22

24D

omai

n/T

est

IQ

Age

Mem

ory

VL

T-L

earn

17.8

79.

0320

.22

9.07

19.6

27.

0222

.18

8.32

22.5

28.

2124

.94

8.84

21.4

56.

8625

.17

7.33

97.2

5**

39.3

9***

VL

T-M

emor

y5.

443.

126.

203.

155.

732.

666.

863.

197.

442.

917.

722.

996.

682.

507.

332.

8417

.79*

9.06

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AV

LT

-13.

761.

634.

391.

544.

051.

644.

671.

564.

381.

485.

111.

585.

001.

825.

461.

2210

2.28

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.79*

**R

AV

LT

-58.

472.

569.

493.

118.

962.

589.

912.

6410

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2.61

10.9

23.

1110

.64

2.59

11.9

62.

0517

7.95

***

54.6

9***

RA

VL

T-6

3.90

1.82

4.50

1.70

4.32

1.58

4.70

1.65

4.83

1.79

5.19

1.76

5.14

1.70

5.46

1.77

43.7

3**

16.4

9***

RA

VL

T-7

7.06

2.64

8.05

3.01

6.92

2.56

8.52

2.57

8.21

2.64

9.69

2.59

9.68

2.40

9.83

2.79

11.9

8*13

.66*

RA

VL

T-8

6.72

2.54

7.87

2.96

7.15

2.91

8.52

2.71

8.42

2.80

9.70

2.83

9.45

3.07

10.3

82.

8415

8.30

***

60.6

1***

RA

VL

T-T

ot32

.96

9.30

38.2

68.

7134

.09

9.00

40.0

39.

1438

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8.44

43.5

59.

2542

.32

9.92

46.3

87.

4496

.50*

*89

.38*

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tten

tion

DS

p9.

432.

419.

812.

449.

781.

9410

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2.26

10.7

92.

9312

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3.54

10.5

43.

1412

.25

3.72

11.5

8*14

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Cod

32.3

48.

6238

.60

8.86

32.0

57.

2640

.39

8.23

35.2

18.

1942

.53

9.02

37.0

47.

6945

.29

8.05

17.2

4*13

4.79

***

SS17

.50

3.86

20.4

84.

4217

.40

4.53

21.3

64.

8818

.06

4.17

21.4

54.

4620

.23

3.82

22.2

93.

704.

8562

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inw

in9.

532.

5310

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2.29

10.2

32.

7511

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2.55

11.8

12.

5812

.00

2.68

10.6

43.

3212

.88

3.68

6.09

11.1

8*T

MT

-A35

.18

13.9

526

.81

12.7

332

.55

16.5

424

.81

9.87

31.9

211

.42

22.3

98.

0424

.68

9.50

18.7

97.

2427

.04*

95.5

7***

TM

T-B

88.8

146

.60

65.2

433

.34

79.0

141

.16

54.3

621

.80

78.3

332

.68

46.7

513

.96

59.5

923

.35

42.0

820

.97

48.1

9**

128.

87**

*S

troo

p-W

48.6

113

.75

58.3

215

.39

48.0

613

.63

57.6

311

.53

50.5

513

.66

63.9

711

.45

51.5

014

.07

66.3

89.

104.

9079

.76*

**

1700 I. P. MARTINS ET AL.

1700

Tab

le 5

. M

eans

, st

anda

rd d

evia

tion

s, a

nd F

tes

ts o

n ne

urob

ehav

iora

l m

easu

res

by f

our

IQ g

roup

s an

d ag

e (y

oung

= 8

–9;

old

= 1

0–11

) (C

onti

nued

)

Gro

up

IQ

67–

79

80–8

9

90

–99

1

00

Age

Y

oung

Old

You

ng

Old

Y

oung

Old

You

ng

Old

F

N6

8

98

74

1

01

526

4

22

24D

omai

n/T

est

IQ

A

ge

Str

oop-

C39

.88

7.99

45.0

210

.00

41.2

87.

1646

.91

7.64

41.9

27.

1548

.33

7.70

45.0

09.

4953

.17

9.19

18.0

8*10

0.39

***

Str

oop-

CW

18.4

36.

1821

.23

7.73

20.1

06.

0222

.09

5.83

22.2

44.

8122

.73

4.61

23.4

56.

2025

.04

7.82

24.2

9*22

.99*

**S

RT

1.01

0.21

0.88

0.20

0.95

0.19

0.86

0.20

0.91

0.22

0.84

0.18

0.89

0.21

0.76

0.16

12.8

7*46

.27*

**M

otor

/vis

ual-

mot

orF

OT

-Dom

33.0

95.

5136

.66

5.46

34.2

45.

3737

.60

5.50

35.4

85.

5839

.48

6.33

37.9

18.

1639

.83

8.27

22.2

3*59

.73*

**F

OT

-ND

28.6

04.

3532

.44

4.93

29.6

64.

6932

.34

5.15

30.2

55.

1934

.56

5.52

32.5

05.

5834

.71

5.26

6.98

41.9

5**

Peg

-Dom

33.6

85.

4637

.61

5.92

34.5

55.

2837

.68

6.47

35.6

36.

6238

.56

6.23

34.3

25.

5540

.62

4.27

1.90

42.6

2**

Peg

-ND

31.1

95.

2034

.41

5.14

31.8

14.

8534

.92

5.50

32.3

66.

3235

.95

4.94

32.9

15.

3638

.79

4.72

5.07

57.3

7***

Mat

ch26

.91

4.87

30.0

54.

6228

.96

3.75

32.1

63.

8832

.15

3.81

36.0

23.

4032

.41

5.80

38.2

53.

0829

2.34

***

181.

92**

*D

raw

12.9

11.

6413

.82

1.96

13.7

71.

9214

.65

2.02

14.3

32.

0315

.09

2.36

14.3

22.

0816

.75

2.44

8.59

18.7

4*

*p <

.05

; **

p <

.01

; **

*p <

.00

1.

NEUROBEHAVIORAL PERFORMANCE IN CHILDREN 1701

of IQ on all tests of memory. IQ was also associated with better performanceon tests of attention with the exception of a simple sustained attention task(SS) and a test of brief visual attention (Finwin). IQ was unrelated to measuresof motor speed (FOT), fine motor coordination (Peg), and drawing. The highlysignificant effect of IQ on the Matching Test [F = 292.34 (3,499), p < .001] isrelated to the fact that items on this test progress from simple perceptualmatching to complex visual spatial problem solving. The more difficult itemsare measuring executive functions and, thus, are consistently related to intellec-tual abilities (Arffa et al., 1998; Seidenberg et al., 1983).

DISCUSSION

A battery of tests primarily designed and adapted to North American childrenwas standardized on a sample of 503 healthy Portuguese children aged 8through 11 years. To the authors’ knowledge, this is the first study to de-velop norms for Portuguese children on an extensive battery of neurobehavioraltests, although data for individual tests have been obtained (Marques, 1979;Simões, 2000; Agostini et al., 1998). The results showed marked age and IQeffects, some sex effects, and a general cultural influence.

As expected, there were age differences in proficiency and number oferrors. Older children, in general, performed better than younger children.These age differences were significant in all measures except for visual memoryand the number of errors in Trail Making Test A (TMT-A). With regard toTMT-A errors, the nonsignificant age difference can be explained by a ceil-ing effect because even younger children made few, if any, errors. The timenecessary to complete the TMT-A, however, was significantly reduced inolder children.

Sex differences were in line with those previously reported: girls have abetter performance on tasks of rote verbal learning, speed of informationprocessing, and psychomotor speed, and made fewer errors on a test of cogni-tive flexibility (TMT-B). In contrast, boys performed better than girls on visuo-spatial tasks, motor speed and coordination and visual memory. These findingsare well-documented in other populations for visuo-spatial tasks, language,memory, and some executive functions (Grossi et al., 1979; Halpern, 2000;Hyde & Linn, 1988; Kimura, 1996; Klitenberg et al., 1987; Orsini et al., 1981;Williams et al., 1995). These sex effects, obtained across cultures, may reflecteither neurobiological differences associated with sexual differentiation orsimilar social and educational trends that affect sexual development acrosscultures (Hyde & Linn, 1988; Maccoby & Jacklin, 1974).

1702 I. P. MARTINS ET AL.

Children with higher IQ scores on the CTONI performed better thanchildren with lower IQ scores in all functional domains. These findings wereconsistent with relationships between IQ and executive functions (Arffa etal., 1998), language related skills, memory, some attentional measures, andvisuo-spatial tests (Nielson et al., 1989; Parsons, 1984) found in previousstudies. Although these relationships between IQ and neurobehavioral perfor-mances were replicated, a question remains as to whether performance ofPortuguese school children is the same as that found in the U.S.

Scores obtained in the present investigation were compared to publishedU.S. test norms. Children in this study obtained lower scores on most mea-sures (including nonverbal IQ) than North American children of the sameage group (the only exception being the RAVLT 1, Peg-Dom, Peg-ND, andFOT). Scores were more often between 0.5 and 1 standard deviation belowmean scores for age. Differences in language, culture, and educational prac-tices could make these tests more difficult for Portuguese children (i.e., testbias). The validity of neuropsychological tests and behavioral scales are cul-turally, or context, dependent. The psychometric properties of some tests inthe original language do not translate as well as the items into the new lan-guage (Pontón & Ardila, 1999). Although language was not evaluated, verbalmemory and some attention tests (Digit Span) required the use of language.Digit span tasks depend on the phonological length of the words for digits.Therefore, average digit span ranges from 5.8 in Spanish, to 7 in English andto 9 or 10 in Chinese (Ardila et al., 1994; Dehaene, 1997) and bilingualshave a higher digit span in English than in Spanish (Ardila et al., 2000).Apart from language, culture and teaching strategies may account for someof the differences (Olazaran et al., 1996). Educational practice in Portugalcompared to the U.S., may rely more on rote learning than abstract reason-ing, which could explain the higher score on the RAVLT-1 in Portuguesechildren.

In addition to cultural factors, the low test scores obtained may be theresult of differences in the populations taking part in the current study inPortugal versus normative studies in the U.S. In the current study childrenwere biased toward a socially disadvantaged group. There are at least tworeasons for this. First, children enrolled in participating schools come mostlyfrom lower socioeconomic groups and have a much higher percentage ofethnic minorities (30% in this study) and orphans compared to other urbanpublic elementary schools in Lisbon. Second, requirements for inclusion inthis study were the need for restorative dental treatment but no prior exposure

NEUROBEHAVIORAL PERFORMANCE IN CHILDREN 1703

to dental amalgam. Thus, the sample consists of children who needed, but sofar had not been provided dental care, which again points to a lower socio-economic status than the general population of Portugal. In poor or develop-ing countries, or countries with large social differences, SES may have astrong impact on test performance. It is known that low parental socioeco-nomic status is associated with a lower performance on neuropsychologictests, IQ (Broman et al., 1987), and language tests in particular. Unfortu-nately, due to study policies the present authors were unable to assess poten-tial interactions between SES and neurobehavioral performance in this groupof children.

The impact of language, acculturation, and socioeconomic status on neuro-behavioral abilities was beyond the scope of this investigation. These factorsare of potential relevance when assessing ethnic minorities (Taussig & Ponton,1996). The sample, furthermore, was biased toward lower socioeconomicstatus, those with very low intelligence were excluded and the sample in-cludes few children in the upper IQ range. This bias limits generalization ofneurobehavioral findings to children of superior intelligence and to childrenof a higher socioeconomic status. Although this sample does not representthe whole range of the Portuguese population, it may still be useful and fairlyrepresentative of clinical populations attending public services of neurologyand psychology services.

Despite the recognized limitations, the results of this investigation con-stitute a valuable aid to clinicians who assess Portuguese children with knownor suspected brain dysfunction or learning disabilities. Results cover a widerange of domains across age groups and have norms stratified for age, sex,and IQ. Norms stratified by IQ may prove extremely valuable in the evalua-tion of developmental disorders and children with brain lesions, to isolatetheir specific areas of impairment not explained by a lower general cognitiveperformance. The present results also allow a direct comparison with interna-tional or North American studies in the pattern or profile of cognitive impair-ment of developmental disorders and structural lesions of the brain.

In addition, some of the tests (e.g., RAVLT) can assess qualitative as-pects of memory (e.g., immediate, long term memory, pro- and retroactiveinterference) that, in adults, have been shown to be differentially sensitive toorganic and emotional disturbances (Mungas, 1983). Until now, most of thesemeasures lacked normative data for the Portuguese child population.

Future research is needed to extend the normative study to children ofhigher socioeconomic status in order to elucidate the effects of social class

1704 I. P. MARTINS ET AL.

on test performance. There is a need to validate the test battery by comparingresults with other tests standardized in Portugal or on children with knownneurologic impairments. An investigation of the pattern of cognitive impair-ment of children with known brain lesions on this test battery would demon-strate the sensitivity to lesion localization, lateralization, and severity. Fi-nally, cross-cultural and cross-linguistic studies would provide clinical andscientific knowledge on the modulating effects of language and culture oncognitive development.

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APPENDIX: DESCRIPTION OF NEUROBEHAVIORALTESTS BY DOMAINS

Intelligence: The Comprehensive Test of Nonverbal Intelligence is a languageComprehensive free test of cognitive abilities. A 2 × 2 matrix is presented to theTest of child in which there are two pictures at the top (e.g., a shoe andNonverbal a shoe) and one picture on the bottom (e.g., a boot) plus a blankIntelligence space. From a five-item array at the bottom of the page, the child(CTONI) picks the item that belongs in the empty space. Score is the num-

ber of correct responses out of a possible 25 on each of six subtests:Pictorial Analogies (CTONI-1); Geometric Analogies (CTONI-2);Pictorial Categories (CTONI-3); Geometric Categories (CTONI-4); Pictorial Sequences (CTONI-5); and Geometric Sequences(CTONI-6).

Memory: On the Visual Learning Test, 14 fixed visual designs are presentedVisual Learning in a position on a display board. The child is asked to rememberTest (VLT) which spatial location is associated with each design. Immediate

feedback as to correctness of the child’s responses is provided topromote learning on the first three trials. There is no feedback onthe fourth trial. A delayed recall trial for this test is administeredfollowing a 15-min intervening task. Score is the total number ofcorrect designs learned across the first four trials (VLT-Learn) andremembered at delay (VLT-Memory).

Rey Auditory The Rey Auditory Verbal Learning Test consists of 15 nouns readVerbal Learning aloud for 5 consecutive trials, each trial followed by a free-recallTest (RAVLT) trial. Upon completion of trial 5, an interference list of 15 words

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is presented followed by a free-recall of that list. Recall of thefirst list, without further presentation of those words, is obtainedimmediately following the interference trial (immediate memory)and 20 min later (delayed memory). Scores are the number ofitems recalled on the first (RAVLT-1) and fifth (RAVLT-5) tri-als, the interference trial (RAVLT-6), and the immediate (RAVLT-7) and delayed (RAVLT-8) memory trials, plus the total wordsrecalled on the first five trials (RAVLT-Total).

Attention: The Digit Span Test is a series of orally presented number se-Digit Span quences. The child repeats verbatim a series of digits forward; a(DSp) second series of numbers are repeated in the reverse order. Score

is the total number of sequences correctly recalled.

Coding (Cod) A row of numbers from 1 to 9 is paired with a different symbolfor each number. From this key the child draws the appropriatesymbol under its corresponding number in a randomly presentedarray of numbers. Score is the number of correct symbols drawnin 120 s.

Symbol Search The Symbol Search Test has a series of paired groups of sym-(SS) bols, each pair consisting of a target(s) and a search group. The

child scans the group and indicates whether or not a target sym-bol appears in the search group. Score is the correct number oftargets identified in 120 s.

Finger Windows The child indicates his/her memory of a “rote” visual pattern by(Finwin) manually reproducing a demonstrated spatial sequence. The ex-

aminer points to increasingly longer series of locations found ona card, and the child is asked to reproduce the spatial sequences.Score is the number of correct sequences reproduced (Wechsler,1991).

Trail Making In Part A of the Trail Making Test, the child connects sequen-Test (TMT) tially numbered circles from 1 to 15. In Part B, the child connects

alternately numbered (1–8) and lettered (A–G) circles as quicklyas possible. Score is time in seconds to complete Part A (TMT-A) and Part B (TMT-B) plus errors made on each part (TMT-Aerr and TMT-Berr).

Stroop Color The Stroop Test measures the ease with which the child can shiftWord Test his or her perceptual set to conform to changing demands. The(Stroop) materials consist of three cards. On the first trial the words blue,

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green, and red are printed 100 times in black and white. The childis asked to read as many words as he or she can in 45 s (Stroop-W). On the second trial the child is given a card with 100 Xs inrandom order in the colors blue, green, and red. He or she is askedto name the colors of the Xs for 45 s (Stroop-C). On the thirdtrial the child is given a card with the words blue, green, and redprinted 100 times in random order but in a color of ink that isdifferent from the written word (e.g., the word green is printed inblue ink). The child is asked to name the color he or she seesdisregarding the word (Stroop-CW). Each trial is 45 s and scoreis the number of successful identifications on each trial.

Standard On the reaction time test, the child completes a 6-min trial ofReaction Time hitting a button every time a red light appears on the timer box.(SRT) Score is the mean reaction time of the successful responses out of

60 potential responses.

Motor/Visual The child taps as rapidly as possible with the index finger on anMotor: electronic finger tapper; 5 10-s trials are completed with the dominantFinger Oscillation (FOT-Dom) and non-dominant (FOT-ND) hands. Score is the meanTest (FOT) number of taps in five trials for each hand.

Pegboard The child places pegs in a board first with the dominant (Peg-Dom) and then the non-dominant(Peg-ND) hands. Score is thenumber of pegs placed within 90 s.

Matching Test The Matching Test provides a measure of spatial perception and(Match) problem solving by presenting visual spatial tasks developmen-

tally arranged in order of increasing difficulty. The child markswhich of four options “goes best” with an item standard. A cor-rect choice is dependent on visual spatial skills such as perspec-tive, orientation, rotation, and size discrimination. The child con-tinues until he or she makes six errors within a series of eightconsecutive items. Score is the number of correct items out of apossible 46.

Drawing Test For the Drawing Test, children copy designs developmentally ar-(Draw) ranged in order of increasing difficulty until three consecutive items

are failed. Score is the number of designs correctly drawn out ofa possible 24.