Abbreviations

DCD= Developpemental Coordination Disorder

IM= Ideomotor

VSC = Visuospatial/ or visuoconstructional

MX = mixed subtype

VCI = Verbal Comprehension Index

VSI = Visual Spatial Index

FIQ = Full IQ

NP-MOT = Developmental neuropsychomotor battery

1. Introduction

There is still no consensus in the literature regarding the definition of giftedness but there are different theoretical concepts. The gifted children have been shown to excel in their academic achievements in a supportive environment (social, scholarly) [1-3]. Thus, multiple selection criteria for giftedness screening are used such as standardized tests and other informal sources as teacher’s opinion, parent’s observations, and creativity [4-7]. Certain studies underline an early neurophysiological maturation in gifted children allowing the early emergence of postural, locomotors acquisitions, and visuo-manual coordination as well as language and cognitive processes [8-12]. Authors in the literature have only studied cognitive performances and assume a systematic asynchrony between intellectual and motor performances in gifted children [13-15].

Normal distribution considers a superior IQ from 120 to 129 (6.7% of the general population) according to the Gaussian curve of the Wechsler intelligence scale [16]. Full IQ (FIQ) within that range is qualified as a High Intellectual Quotient (HIQ). Very superior IQ beginning at 130 (2.5%), two standard deviations from the mean, is qualified as High Intellectual Potential (HIP). Therefore, children with HIP are considered gifted children according to the World Health Organization [17].

Moreover, it is common to think that HIQ/HIP children cannot have learning disabilities because there are few studies on this subject [18, 19]. Empirical evidence proves otherwise, but the link has yet to be explored [20-22]. Developmental coordination disorder (DCD) is one of the least studied, while attention deficit-hyperactivity disorder is more investigated [23-26]. DCD can be defined as a non-verbal neuropsychological dysfunction which can give rise to behavioral and learning disabilities [27]. It is not a form of brain injury as in adult apraxia, it is an impairment linked to the maturation process of the central nervous system. The developmental approach explains that children with DCD have never acquired the capacity to perform complex motor actions adapted to age, that is not due to an intellectual disability, nor by visual impairment and nor is it due to neurological brain involvement (e.g., muscular dystrophy, cerebral palsy) [28]. It is a common disorder in school-aged children with an estimated prevalence of 5-6% between 5 and 11 years old [28]. Researchers and clinician practitioners must use DSM criteria as recommended since 1994 by London International consensus [29] and as advised by the European Academy of Childhood Disability [30]. However, the authors have rarely investigated DCD in relation to cognitive functions including IQ level. We do not know the specificity of clinical features in children with HIQ/HIP. Are they different or similar?

Few studies have used clusters analysis to identify distinct subtypes of DCD and not all the authors use the same motor assessments. They used a few cognitive and neuromotor tests (e.g., imitation of gestures, gnosis, neurovisual, and neurological soft signs). Thus, it is not easy to compare studies. Only one subtype is common to all the studies: a group with impairments in global and fine motricity [31-32]. Some studies identified groups with visuospatial DCD or visuo-motor integration disorder [33-39] and only three studies used transitive gestures and motor sequencing to identify ideomotor impairment [31, 39, 40].

Recent studies [31, 34, 36] provided a better understanding of the DCD based on a standardized developmental assessment with quantitative and qualitative measures. They use age-related normative data to identify subtypes of DCD, using multidimensional clinical and statistical approaches. The authors identified two to three pure types of DCD and the specific diagnostic markers: Ideomotor (IM) (8%), visuospatial/ or visuoconstructional (VSC) DCD (52%), and a mixed subtype (MX) (40%). Children with IM-DCD were characterized by significant impairments in digital perception, manual praxis, and imitation of gestures, while the VSC subgroup appeared to have deficiencies in visual motor integration, visual spatial motor structuring, and/or constructional abilities (with difficulties in Lego blocks to follow a model). Finally, the MX group shares common impairments to IM and VSC and exhibited the specific deficits in motor coordination of the lower-upper limbs, poor manual dexterity, neurological soft signs (e.g. synkinesis, adiadochokinesia), and certain comorbidities (e.g., executive functions disorders, auditory-memory deficits, and auditory-attention difficulties).

The aims of the current study were to analyze multivariate associations between DCD subtypes and several neuropsychological, neuropsychomotor, and neurovisual characteristics, in order to refine the specific features of DCD depending on IQ score and define motor profiles according to cognitive abilities and IQ index scores. The first hypothesis suggests a relationship between early psychomotor development and high IQ. The second explores if there are specific DCD clinical features in HIQ versus HIP with DCD compared to typical children also with DCD and examined subtypes of DCD.

2. Material and Methods

2.1 Participants

Data from 38 DCD children (average age: 9 years old, 2.7 SD) based on criteria of Diagnostic and Statistical Manual of Mental Disorders (DSM-5) [28] were collected. Inclusion criteria were strict: Children with sensory deficit, dyslexia, and attention deficit-hyperactivity disorder (based on DSM criteria), psychiatric abnormalities or general medical abnormalities, and traumatic brain injury were not included, nor was any child born premature (<37 weeks), and no physical therapy neither medication.

Children from 6-12 years old were recruited in the outpatient consultation of the child psychiatry department at Necker Hospital in Paris, France. All of them met the criterion A for DCD described in the DSM-5 [28], with acquisition and execution of motor skills which are clearly below the level expected given the subject's chronological age and despite learning and using opportunities of these skills with standardized tests [41-43]. Children who meet inclusion criteria were assigned to the three DCD subtypes validated in a previous study and described above [31, 34].

Two matched groups were studied: 19 typical children with DCD (IQ=90-110) and another group including 19 HIQ-HIP (high intellectual quotient or high intellectual potential) children. Within this last group, we distinguished superior IQ starting at +1.33 SD (HIQ=120-129), and very superior IQ at +2 SD (IQ≥130) who are identified as gifted children (HIP) by the Wechsler intelligence scale [16-17]. The two groups were matched according to sociodemographic data, age, no language disorder, and no ophthalmological abnormalities. Only IQ scores are identified as differentiation criterion. The Institutional ethic committee of Paris Descartes University, Sorbonne Paris city, approved the study (CER-PD 2018-72; CER-PD 2019-49). Participants provided written informed consent before the start of the study, signed by a parent or legal representative and children before enrolment in the study.

2.2 Measures

2.2.1 Neuropsychological assessment: All children recruited in DCD sample had completed a standard measure of intelligence, the Wechsler Intelligence Scale for children according to the age (WISC-IV) [16]. Verbal Comprehension Index (VCI), Visual Spatial Index (VSI), and Full IQ (FIQ) scores were expressed as standardized scores (mean 100, SD=15). We have completed cognitive investigations by visual-motor integration, constructional and visuospatial structuring (Khos’ cubes), and executive functions (Tower of London test and Porteus Labyrinths) assessments [44].

2.2.2 Neuropsychomotor developmental assessment: All children were assessed with a developmental neuropsychomotor battery (NP-MOT) [42] with age-related normative data to evaluate neuropsychomotor physical functions. It is applicable to children from 4 years old. It is a standardized and validated assessment and it has been found to have adequate test-retest reliability and internal consistency. Correlation coefficients of the NP-MOT with the Bruininks-Oseretsky Test Motor Proficiency (BOTMP) [45] range from 0.72 to 0.84, for motor coordination and balance [36]. NP-MOT battery allows physical standardized assessment of passive/active muscular tone of limbs and axial tone, highlighting NSS such as synkinesis, the presence of a pyramidal tract dysfunction (hypertonia), bodily spatial integration, basic motor function, control and regulation in gross motor tasks (gait, balance, coordination), laterality, manual dexterity, manual praxis, digital perception, rhythmic, and auditory attention tasks, completed by imitation of gestures (see [32] for a synopsis of NP-MOT battery tasks).

2.2.3 Neurovisual assessment and other measures: Electro-physiological neurovisual examination including Electroretinogram (ERG) test, with smooth visual pursuits, and Visual Evoked Potential (VEP) test [46] was used to analyze the sensory and visual motor pathways. To detect dysgraphia, we have used Ajuriaguerra standardized scale of handwriting [43], a score of 19 to 25 indicates significantly dysgraphic handwriting. Finally, an anamnesis form was also used to collect data about pregnancy and delivery, psychomotor development (e.g., sitting alone, walking), and any difficulties with constructional play, such as puzzles and Lego blocks following a model relative to developmental markers found in previous study [31]. The child school report book was examined to identify if there are some learning difficulties (such as mathematics, written French).

2.2.4 Statistical analyses: We used R software [47] for statistical treatment. Data were analyzed according to the intention-to-treat principle. We used p-values at 0.05 to indicate statistical significance and p-values at 0.001 if reached. We also applied the Bonferroni method to adjust for multiple comparisons. To analyze the dependence between IQS and all DCD variables (continuous outcomes according to one or more classification factors), parametric Multivariate Analysis of Variance (MANOVA) was used. Two-group comparisons of scale scores were performed using Student T-test (t) and Pearson's chi-square test (χ2) was carried out to analyze dichotomic variables (Two-way cross-classification between qualitative variables). Variables were coded as 0 for success to a test (meaning no disorder) or 1 for failure (indicating a probable disorder) based on regular scoring (standard deviation: 1 < SD or < 20th percentile according to the test). A Pearson’s correlation test (r) for numeric continuous variables and Spearman's ρ test (ρ) for non-parametric correlations were used.

3. Results

3.1 Sample characteristics

Table 1 shows sociodemographic, cognitive, and medical characteristics of 38 children with DCD. Groups were matched according to sociodemographic data; age (t= -0.069, df=18, p=0.94, [95% CI, 95.16 to 124.24]), absence of language disorder χ2 (1)=0.3, p=0.73, [95% CI, 0.72 to 0.74], and absence of ophthalmological abnormalities χ2 (1)=0, p=1, [95% CI, 1 to 1]. Only IQ scores are identified as differentiation criterion of groups (t=12.87, df=18, p<0.0001, [95% CI, 127.36 to 138.01]). In HIQ-HIP children with DCD, we identified high rate of MX, low rate of IM and VSC-DCD compared to typical children with DCD (Figure 1). HIQ compared to HIP, there is no significant difference in MX-DCD frequency (respectively 56% vs 60%). Mathematical difficulties were strongly present in the whole sample, comparing typical DCD children and HIQ-HIP DCD, 100% vs 20% of mathematical difficulties in VSD-DCD χ2 (1)=4.5, p=0.07, [95% CI, 0.067 to 0.077], but in MX-DCD, 100% vs 90.91%. It does not appear in the IM-DCD.

Legend: HIP: High intellectual potential (gifted children); HIQ: High intellectual quotient; SD: standard deviation. FIQ: full intellectual quotient.

Figure 1: IM and VSC-DCD frequency in HIQ-HIP group compared to typical children with DCD.

Table 1: Sample characteristics with sociodemographic, cognitive, and medical data in DCD groups (typical children vs HIP-HIQ).

Legend: HIQ: High Intellectual Quotient (IQ = 120-129)

HIP: High Intellectual Potential (gifted children; IQ ≥130)

IM-DCD: Ideomotor-DCD

VSC-DCD: Visuo-Spatial/ or Constructional-DCD

*: significant difference p ≤ 0.05

3.2 Relationship between IQ and neuropsychomotor development

In HIQ-HIP children, there are negative and significant correlations between main IQ index scores (VCI, VSI, and FIQ) and the developmental milestones to sit, to walk and language. VSI was negatively correlated to age of language acquisition (r= -0.366 [95% CI, -0.587 to 0.135], p=0.024). These correlations show that children with DCD having a high VSI (from 110) developed language and sitting early. Regarding VCI, the earlier a child develops walking, sitting and language, the higher is his VCI. It is correlated with sitting (r= -0.425 [95% CI, -0.651 to -0.167], p=0.008), walking (r= -0.421 [95% CI, -0.626 to -0.147], p=0.009) and language (r= -0.514 [95% CI, -0.701 to -0.319], p=0.001). Finally, FIQ is negatively and significantly correlated with sitting (r= -0.356 [95% CI, -0.626 to -0.008], p=0.028), walking (r= -0.41 [95% CI, -0.621 to -0.122], p=0.01) and language (r= -0.624 [95% CI, -0.766 to -0.462], p<0.0001). Therefore, children whose score is very high on Wechsler test, are more likely to have an early psychomotor development.

3.3 Relationship between IQ index scores and DCD subtypes

Our findings display that IM-DCD had an influence on FIQ [F (1, 36)=4.67, p=0.035] and VSI [F (1, 36)=4.91, p=0.031]. VSC-DCD had an influence on FIQ [F (1, 36)=5.28, p=0.025]. DCDs being present in both groups (HIQ-HIP and Typical children), these results show that an IM and VSC-DCDs are less likely to be found in children with high IQ. Comparing data, results show that children without IM or VSC-DCD scored higher IQ in the tests, which could imply a relationship between DCD subtypes and IQ (Table 2). There is no significant difference between HIP and HIQ. Furthermore, to better understand how IQ influences DCD subtypes, we have analyzed neuropsychomotor and cognitive profiles in the sample. We tested each variable’s dependence on IQ.

Legend: VSI : Visual Spatial Index ; VCI : Verbal Compréhension Index ; FIQ : Full Intellectual Quotient ; SD : Standard Deviation ; DCD subtypes : Developpemental Coordination Disorder subtypes ; IM-DCD : Ideomotor DCD ; VSC-DCD : Visuo-Spatial/ or Constructional DCD.

Table 2: Mean of scores in IQ scale for each DCD subtypes in whole sample.

3.4 Relationship between IQ and neuropsychomotor features

Regarding neuropsychomotor features evaluated by NP-MOT battery, we compared HIQ-HIP DCD children to typical DCD children : 84% vs 47%, respectively, achieved object spatial orientation skill but not significantly, 84% vs 37% of adiadochokinesia χ2 (1)=5.4, p=0.02, [95% CI, 0.033 to 0.041], and 10% vs 87% of bimanual coordination disorder χ2 (1)=9, p=0.003, [95% CI, 0.003 to 0.005] (Table 3). There is no significant difference between HIP and HIQ. Outcomes showed better scores in favor of HIQ-HIP group for the “objects spatial orientation” item, but they had worse scores than typical children with DCD regarding “spatial orientation on others” and “body integration of spatial orientation” item (Table 4). Regarding functional laterality, we found a statistical difference beginning at QI=130, between HIP and typical children χ2 (1)=4.571, p=0.033, [95% CI, 0.052 to 0.061], with 33% of right-handed and 67% of left-handed versus 65% of right-handed and 35% of left-handed respectively. There is no statistical difference in this aspect between HIQ and typical children neither between HIP and HIQ children; HIQ presents 80% of right-handed and 20% of left-handed children (see Table 4).

Legend: HIP: High Intellectual Potential (gifted children); HIQ: High Intellectual Quotient

Table 3: IQ’s influence on neuropsychomotor tasks of NP-MOT battery (Vaivre-Douret, 2006) and neurovisual functions.

Legend: HIP: High Intellectual Potential (gifted children); HIQ: High Intellectual Quotient; IQ: Intellectual Quotient; *: Significant difference p < 0.05; df: Degrees of freedom.

Table 4: IQ’s influence on neuropsychomotor tasks of NP-MOT battery (Vaivre-Douret, 2006) and neurovisual functions.

3.5 Relationship between DCD subtypes and cognitive functions

In whole sample, IM-DCD had a significant, strong and positive correlation with executive functions disorder (FE) (ρ = +0.519 [95% CI, 0.163 to 0.795], p=0.001), and a significant, strong, and negative correlation between Khos cubes test failure and VSC-DCD (ρ= -0.651 [95% CI, -0.899 to -0.406], p=0.006). There is no significant difference between HIP and HIQ.

4.Discussion

This study displayed similar clinical features of DCD in both groups HIQ-HIP and typical children. High IQ DCD children have significantly better executive functions and visio-spatial constructional functioning than typical children with DCD but worse auditory attention and memory, and more neurological soft signs. These outcomes underline better skills of mental representation and evocation through internal language in HIQ-HIP children with DCD allowing them to better plan and control gestures that contribute to less Ideomotor or Constructive pure DCD.

They are in accordance with the literature; on one hand concerning the link between intelligence and executive functions [48]. In HIQ-HIP children, it highlights better activation and connectivity of the frontoparietal lobe and cerebral cortex improving fluid reasoning [49]. On the other hand, VSC-DCD is characterized by specific disorders of "visuo-spatial motor structure", "visuo-motor integration"," visuo-spatial motor construction", associated with ocular pursuit disorders [31, 46]. Two systems are considered in visual perception [50] but the occipital-parietal dorsal pathway (“where”) is focused on localization and action to direct the gesture with vision. This pathway is impaired in the VSC subtype [31, 46] and involves thalamus, basal ganglia, and cerebellum, this last affecting also visual pursuits [32, 46]. Desco’s study [51] shows bilateral activation patterns and increased activation in the parietal and frontal regions of gifted children and demonstrates that these activations are associated with improved skills in visuospatial treatment and logical reasoning. We identified more left-handed in HIP children (IQ ≥ 130) confirming more involvement of the right cortex in HIP group. This may open more in-depth research fields to better understand the neurological impairments involved in DCD in this population.

Higher frequency of MX-DCD can be explained by the fact that fewer primary school children (with high IQ) consult for pure DCD such as VSC or IM subtype because they can easily compensate the disorder by mental strategies and better executive functions. Recent studies [31, 32, 34, 36] showed that MX subgroup shares impairments common to IM and VSC, and is characterized by specific impairments regarding motor coordination of the lower and upper limbs, poor manual dexterity, neurological soft signs suggesting synkinesis and/ or adiadochokinesia, and some comorbidities (e.g., auditory-memory deficits, auditory-attention difficulties...). Based on these findings, our outcomes identified more auditory attention and memory, significant adiadochokinesis deficits and bimanual coordination disorder in HIQ-HIP group, allowing to better explain the high rate of MX subtype in this group. Adiadochokinesia is the difficulty to perform alternative prono-supination movements of the hand and evoke more neurological soft signs in HIQ-HIP children [36, 52], highlighting cerebellum impairment. It is often associated with learning disabilities and our findings confirm higher risks of comorbidity in DCD [22, 25, 53], particularly in MX by that is the common subtype in the main DCD studies [32]. It is important not to neglect comorbidity’s influence on IQ scores for HIQ children as it might lower the FIQ (120-129).

To be gifted does not prevent a neurodevelopmental disorder such as DCD and possible learning disability may lower the FIQ. For example, mathematical difficulties (applying calculation with a handwritten operation, geometry, problem to solve) are strongly present in both groups in our sample with no significant difference. This is in line with literature proving that mathematics skills are particularly affected in DCD [31, 36]. Our finding displayed mainly mathematic difficulties in MX-DCD subtype and very few in VSC-DCD for HIQ-HIP, confirming the better compensation strategies in high IQ children with DCD concerning pure subtype as VSC subtype [34].

Regarding psychomotor development, the finding highlight early milestones in high IQ DCD but the quality of motor skills still deficient and those from early childhood. These are in accordance with category C of the diagnosis criteria of DSM-5 [28]. Motor milestones are not systematically delayed by a DCD as confirmed by previous studies [8, 32], but the acquisition of coordinated motor skills remains below chronological age (criterion A of DSM-5) [28]. It is therefore fundamental to differentiate psychomotor development (acquisition of walking, sitting...) from neuromotor skills (coordination, praxis...) because, despite an early maturation in high IQ children, motor performance of intentional gestures or the ability to perform complex motor actions can be disturbed by a neurological dysfunction [36] as in typical children.

5. Conclusion

In conclusion, the findings of the present study are relevant to attest that HIQ-HIP children DCD have similar clinical features compared to typical children with DCD. They present lower rates of pure VSC and IM-DCD than typical children with DCD because they appear to use mental evocation with visual representation and internal language necessary for better planning. Thus, we can recommend for clinicians to use these strategies in the remediation for cognitive difficulties in typical children, do not overlook that the higher the IQ, the more HIP children can mask learning disabilities [8, 18, 54] with a heterogeneous profile of index level scores between VSI and VCI [8, 55, 56], VSI being more affected by DCD, that the presence of a subtype of DCD decreases the IQ index scales and therefore also FIQ. Thus, it is possible to misdiagnose some HIP in HIQ group. That questions the validity of the IQ cutoff score of the 130 thresholds for the IQ of HIP. Therefore, regarding our findings, it appears essential to evaluate in-depth with multidimensional assessments (neuropsychological and neuropsychomotor batteries) the child presenting some heterogeneous index scores or subtests in his IQ profile. Finally, it underlines also that it is important to take into account multiple selection criteria to define HIP gifted children, such as behavioral, socio-emotional and cognitive skills, informal sources (parents and teachers) [4, 5].

The strengths of the study are in the detailed neuropsychological profile provided on the children, and the history of early development. The results demonstrate important implications for future clinical research, and it is useful for clinical decision-making processes. The limitations are in the small numbers, especially with the division of the samples into DCD subtypes. Future research could replicate the current study with a larger sample and assess in addition to socio-cognitive and psycho-affective components.

Acknowledgments

We are grateful to the children and their families who agreed to participate in this study. This research was supported by the University Institute of France (Institut Universitaire de France, IUF (Grants numbers L17P99, IUF004). The funding sources was not involved in the study design, the collection, analysis, and interpretation of data, the writing of the report, or the decision to submit the article for publication.

Declaration of Interest Statement

The authors declare that they have no conflict of interest.

References

1. Curby TW, Rudasill KM, Rimm-Kaufman, et al. The role of social competence in predicting gifted enrollment. Psychology in the Schools 45 (2008): 729-744.
2. Subotnik RF, Olszewski-Kubilius P, Worrell FC. Rethinking giftedness and gifted education: A proposed direction forward based on psychological science. Psychological science in the public interest 12 (2011): 3-54.
3. Reis SM, Renzulli JS. Is there still a need for gifted education? An examination of current research. Learning and individual differences 20 (2010): 308-317.
4. Moon SM, Rosseli, HC. Developing gifted programs. In: Heller KA, Mönks FJ, Sternberg RJ, Subotnik RF, Oxford. International handbook of giftedness and talent. England: Elsevier (2000): 499-521.
5. Lohman DF, Korb KA, Lakin JM. Identifying academically gifted English-language learners using nonverbal tests : A comparison of the Raven, NNAT, and CogAT. Gifted Child Quarterly 34 (2008): 595-623.
6. Lakin JM, Lohman DF. The predictive accuracy of verbal, quantitative and nonverbal reasoning tests: Consequences for talent identification and program diversity. Journal for the Education of the Gifted 34 (2011): 595-623.
7. Kroesbergen EH, Van Hooijdonk M, Van Viersen S, et al. The psychological well-being of early identified gifted children. Gifted Child Quarterly 60 (2016): 16-30.
8. Vaivre-Douret L. Les caractéristiques développementales d’un échantillon d’enfants tout venant « à hautes potentialités » (surdoués): suivi prophylactique [The developmental characteristics of children's sample with high potentialities (gifted children): preventive follow-up]. Neuropsychiatrie de l’enfance et de l’adolescence 52 (2004): 29-141.
9. Simoes Loureiro I, Lowenthal L, Lefebvre L, et al. Le trouble déficitaire de l’attention chez l’enfant à haut potentiel : étude exploratoire [The ADHD with high potential child: exploratory study]. Approche Neuropsychologique des Apprentissages de l'Enfant 101 (2009): 317-322.
10. Bildiren A. Developmental characteristics of gifted children aged 0–6 years: parental observations. Early Child Development and Care 188 (2018): 997-1011.
11. Gross MUM. Small poppies: Highly gifted children in the early years. Roeper Review 21 (1999): 207-214.
12. Winisdorffer J, Vaivre-Douret L. Dépister l’enfant à « hautes potentialités » : apports d’une étude rétrospective longitudinale de 19 enfants sur 18 années d’exercice en milieu rural [Detection of the child with high potentialities (gifted child) : contributions of a longitudinal retrospective study of 19 children over 18 years of exercise in rural areas]. La revue du praticien 62 (2012): 1205-1211.
13. Terrassier JC. Les enfants intellectuellement précoces [Early intellectually children]. Archives de Pédiatrie 16 (2009): 1603-1606.
14. Lovecky DV. Identity development in gifted children: Moral sensitivity. Roeper Review 20 (1997): 90-94.
15. Guénolé F, Baleyte J. Le paradoxe des enfants surdoués. Revue de neuropsychologie [The paradox of gifted children]. Revue de neuropsychologie 9 (2017): 19-26.
16. Wechsler, D. WISC-IV: Wechsler Intelligence Scale for Children, Fourth edition: Technical and Interpretive Manual. San Antonia, TX: PsychCorp. (2003).
17. Health WEC. on M, Organization WH. Expert Committee on Mental Health: report on the second session, Geneva, 11-16 September 1950. World Health Organisation (1951).
18. Vaivre-Douret L. Les surdoués: ils ont aussi des troubles des apprentissages. [Gifted children: they have also learning disabilities]. Revue du Haut Comité de Santé Publique 26 (1999).
19. Vaivre-Douret L. Le développement de l’enfant aux “aptitudes hautement performantes” (surdoués): importance des fonctions neuro-psychomotrices psychomotrices [Development of the high potentialities child (gifted): The importance of neuropsychomotor functions]. Approche Neuropsychologique Des Apprentissages Chez l’Enfant 14 (2002): 95-110.
20. David HA, Double Label: Learning Disabilities and Emotional Problems among Gifted Children. International Letters of Social and Humanistic Sciences 75 (2017): 22-31.
21. Beckmann E, Minnaert A. Non-cognitive Characteristics of Gifted Students with Learning Disabilities: An In-depth Systematic Review. Frontier in Psychology 20 (2018): 504-504.
22. Brody LE, Mills CJ. Gifted Children with Learning Disabilities: A Review of the Issues. Journal of Learning Disabilities 30 (1997): 282-296.
23. Cordeiro ML, Farias AC, Cunha A, et al. Co-Occurrence of ADHD and high IQ: a case series empirical study. Journal of Attention Disorder 15 (2011): 485-490.
24. Budding D, Chidekel D. ADHD and giftedness: a neurocognitive consideration of twice exceptionality. Applied Neuropsychology Child 1 (2012): 145-151.
25. Hartnett DN, Nelson JM, Rinn AN. Gifted or ADHD: the possibilities of misdiagnosis. Roeper Review 26 (2004): 26:73-76.
26. Tordjman S, Guignard JH, Seligmann C, et al. Diagnosis of hyperactivity disorder in gifted children depends on observational sources. Gifted and Talented International 22 (2007): 62-67.
27. Vaivre-Douret L. Troubles d’apprentissage nonverbal: les dyspraxies développementales [Non-verbal learning disabilities: developmental dyspraxia]. Archives de Pédiatrie 14 (2007): 1341-1349.
28. American Psychiatric Association. Diagnostic and Statistical Manual of Mental disorders: DSM-5. 5th edn. Washington, DC: American Psychiatric Publishing (2013).
29. Polatajko H, Fox M, Missiuna C. An International Consensus on Children with Developmental Coordination Disorder. Canadian Journal of Occupational Therapy 62 (1995): 3-6.
30. Blank R, Smits?Engelsman B, Polatajko H, et al. European Academy for Childhood Disability (EACD): Recommendations on the definition, diagnosis and intervention of developmental coordination disorder (long version*. Developmental Medicine and Child Neurology 54 (2012): 54-93.
31. Vaivre-Douret L, Lalanne C, Ingster-Moati I, et al. Subtypes of Developmental Coordination Disorder: Research on Their Nature and Etiology. Developmental Neuropsychology 36 (2011): 614-643.
32. Vaivre-Douret L, Lalanne C. Specific impairments and predictive markers for Developmental Coordination Disorder subtypes in children: the importance of multidimensional developmental assessments in cluster analysis. Journal of Translational Science 5 (2019): 1-13.
33. Vaivre-Douret L, Lalanne C, Cabrol D, et al. Identification de critères diagnostiques des sous-types de troubles de l’acquisition de la coordination (TAC) ou dyspraxie développementale. Neuropsychiatrie de l’Enfance et de l’Adolescence 59 (2011): 443-453.
34. Lalanne C, Falissard B, Golse B, et al. Refining developmental coordination disorder subtyping with multivariate statistical methods. BMC Medical Research Methodology 12 (2012): 107-107.
35. Lyytinen H, Ahonen T. Developmental motor problems in children: a six-year longitudinal study. Journal of Clinical and Experimental Neurpsychology 10 (1988): 57-57.
36. Vaivre-Douret L, Lalanne C, Golse B. Developmental Coordination Disorder, An Umbrella Term for Motor Impairments in Children: Nature and Co-Morbid Disorders. Frontier in Psychology 7 (2016).
37. Hoare D. Subtypes of Developmental Coordination Disorder. Adapted Physical Activity Quarterly 11 (1994): 158-169.
38. Macnab JJ, Miller LT, Polatajko H. The search for subtypes of DCD: Is cluster analysis the answer? Human Movement Sciences 20 (2001): 49-72.
39. Green D, Chambers ME, Sugden DA. Does subtype of developmental coordination disorder count: is there a differential effect on outcome following intervention? Human Movement Science 27 (2008): 363-382.
40. Dewey D, Kaplan BJ. Subtyping of developmental motor deficits. Developmental Neuropsychology 10 (1994): 265-284.
41. Vaivre-Douret L, Burnod Y. Development of a global motor rating scale for young children (0-4 years), including eye-hand grip coordination. Child: Care, health and Development 27 (2001): 515-534.
42. Vaivre-Douret, L. Batterie d’évaluation des fonctions neuro-psychomotrices (NP-MOT) [Tests battery of developmental neuropsychomotor functions in children (NP-MOT)]. Paris: Centre de Psychologie Appliquée-Pearson (2006).
43. Ajuriaguerra de J. L’écriture de l’enfant: l’évolution de l’écriture et ses difficultés [The handwriting of the child: the evolution of handwriting and its difficulties]. 4th ed. Vol. 1. Paris: Delachaux et Niestlé (1989).
44. Korkman M, Kirk U, Kemp S. Developmental neuropsychological assessment manual. Paris: Centre de Psychologie Appliquée-Pearson (2003).
45. Bruininks O. Buininks-Oseretsky Test of Motor Profiency. Circle Pines, MN: American Guidance Service (1978).
46. Robert MP, Ingster-Moati I, Albuisson E, et al. Vertical and horizontal smooth pursuit eye movements in children with developmental coordination disorder. Dev Med Child Neurol 56 (2014): 595-600.
47. R Core Team R. A language and environment for statistical computing. R Fundation for Statistical Computing (2015).
48. Arffa S. The relationship of intelligence to executive function and non-executive function measures in a sample of average, above average, and gifted youth. Arch Clin Neuropsychol 22 (2007): 969-978.
49. Nusbaum F, Hannoun S, Kocevar G, et al. Hemispheric Differences in White Matter Microstructure between Two Profiles of Children with High Intelligence Quotient vs. Controls: A Tract-Based Spatial Statistics Study. Frontier in Neuroscience 11 (2017): 173.
50. Milner AD, Goodale MA. Two visual systems re-viewed. Neuropsychologia 46 (2008): 774-785.
51. Desco M, Navas-Sanchez FJ, Sanchez-González J, et al. Mathematically gifted adolescents use more extensive and more bilateral areas of the fronto-parietal network than controls during executive functioning and fluid reasoning tasks. NeuroImage 57 (2011): 281-292.
52. Lopez C, Hemimou C, Vaivre-Douret L. Handwriting disorders in children with developmental coordination disorder (DCD): Exploratory study. European Psychiatry 41 (2017): S456.
53. Antshel KM, Faraone SV, Stallone K, et al. Is attention deficit hyperactivity disorder a valid diagnosis in the presence of high IQ? Results from the MGH Longitudinal Family Studies of ADHD. Journal of Child Psychology and Psychiatry 48 (2007): 687-694.
54. Siegle D. Understanding underachievement. In S.I. Pfeiffer (ed), Handbook of Giftedness in children. United Kingdom: Springer Nature (2018): 285-297.
55. Tordjman S, Vaivre-Douret L, Chokron S, et al. Les enfants à haut potentiel en difficulté : Apports de la recherche Clinique [Children in difficulty with high potential: contribution of research]. L’Encéphale 44 (2018): 446-456.
56. Vaivre-Douret L. Caractéristiques développementales de l’enfant à « hautes potentialités » et compréhension de trajectoires vers la dépression à l’âge scolaire en primaire et au collège [Developmental characteristics of the child with high-level potentialities and understanding of trajectories to depression at school age in elementary and in hight school]. Neuropsychatrie de l’Enfance et de l’Adolescence 67 (2019): 140-151.