- Email: [email protected]
Motor impairments screened by the Movement Assessment Battery for Children-2 are related to the visual-perceptual deficits in children with Developmental Coordination Disorder
Research in Developmental Disabilities 35 (2014) 2172–2179
Contents lists available at ScienceDirect
Research in Developmental Disabilities
Motor impairments screened by the Movement Assessment Battery for Children-2 are related to the visual-perceptual deficits in children with Developmental Coordination Disorder Chih-Hsiu Cheng a,1, Yan-Ying Ju b, Hsin-Wen Chang c, Chia-Ling Chen c, Yu-Cheng Pei d, Kevin C. Tseng e, Hsin-Yi Kathy Cheng c,* a
Department of Physical Therapy and Graduate Institute of Rehabilitation Science, College of Medicine, Chang Gung University, Tao-Yuan 333, Taiwan b Department of Adapted Physical Education, National Taiwan Sport University, 250 Wen-Hua 1st Road, Kwei-Shan, Tao-Yuan 333, Taiwan c Graduate Institute of Early Intervention, College of Medicine, Chang Gung University, 259 Wen-Hua 1st Road, Kwei-Shan, Tao-Yuan 333, Taiwan d Department of Physical Medicine and Rehabilitation, Chang Gung Memorial Hospital, Tao-Yuan, Taiwan e Department of Industrial Design, College of Management, Chang Gung University, 259 Wenhua 1st Road, Guishan, Tao-Yuan 33302, Taiwan
A R T I C L E I N F O
A B S T R A C T
Article history: Received 11 March 2014 Received in revised form 8 May 2014 Accepted 16 May 2014 Available online
This study was to examine to what extent the motor deficits of children with Developmental Coordination Disorder (DCD) verified by the Movement Assessment Battery for Children-2 (MABC-2) are linked to their visual-perceptual abilities. Seventeen children with DCD and seventeen typically developing children (TD) aged 5–10 years screened from a total of 250 children were recruited. The assessments included MABC-2, traditional test of visual perceptual skills (TVPS-R), and computerized test for sequential coupling of eye and hand as well as motion coherence. The results indicated that children with DCD scored lower than TD in MABC-2, and their total scores were highly correlated with manual dexterity component scores. DCD group also showed poor visual-perceptual abilities in various aspects. The visual discrimination and visual sequential memory from the TVPS-R, the sequential coupling of eye and hand, and the motion coherence demonstrated a moderate or strong correlation with the MABC-2 in the DCD rather than the TD group. It was concluded that the motor problems screened by MABC-2 were significantly related to the visual-perceptual deficits of children with DCD. MABC-2 is suggested to be a prescreening tool to identify the visual-perceptual related motor deficits. ß 2014 Elsevier Ltd. All rights reserved.
Keywords: Developmental Coordination Disorder Perception Movement Manual dexterity Balance
* Corresponding author. Tel.: +886 3 211 8800x3667; fax: +886 3 211 8700. E-mail addresses: [email protected] (C.-H. Cheng), [email protected] (Y.-Y. Ju), [email protected] (H.-W. Chang), [email protected] (C.-L. Chen), [email protected] (Y.-C. Pei), [email protected] (K.C. Tseng), [email protected], [email protected] (H.-Y. Cheng). 1 Tel.: +886 3 211 8800x3714. http://dx.doi.org/10.1016/j.ridd.2014.05.009 0891-4222/ß 2014 Elsevier Ltd. All rights reserved.
C.-H. Cheng et al. / Research in Developmental Disabilities 35 (2014) 2172–2179
2173
1. Introduction Developmental Coordination Disorder (also known as Dyspraxia), is the term used to describe a range of difficulties that children experience with posture, movement and coordination, without any specific medical reason for these difficulties (American Psychological Association, 2013). The most commonly reported prevalence of DCD is 5–6% (Zwicker, Missiuna, Harris, & Boyd, 2012). These children typically have difficulties with fine and/or gross motor skills, and demonstrated a slower, less accurate and variable motor performance, and tend to withdraw from physical play with other children (Piek & Dyck, 2004). Despite a generalized impairment in nearly all areas of motor performances, the children with DCD show considerable variation in the degree and pattern of perceptual-motor deficits (Tsai, Wilson, & Wu, 2008). Some studies suggested to consider subtypes of DCD based on visual dysfunctions (Hoare, 1994; Macnab, Miller, & Polatajko, 2001), such as deficits in visual-motor integration (Bonifacci, 2004; Van Waelvelde, De Weerdt, De Cock, & Smits-Engelsman, 2004; Wilson & McKenzie, 1998), impaired visual sensitivity (Sigmundsson, Hansen, & Talcott, 2003), or visual-spatial processing (Wilson & McKenzie, 1998). Visual perception concerns both object identity and localization in space, and is intimately connected with action systems. Any deficit in this processing network leads to problems in movement planning, on-line movement correction, and feedback control (Wilson & McKenzie, 1998). However, in terms of motor-free visual-perceptual ability, some studies have found conflicting results. Sigmundsson et al. (2003) found that children with DCD showed impaired visual sensitivity, but Bonifacci (2004) did not. Sigmundsson et al. tested children with developmental ‘‘clumsiness’’ on a series of visual coherence threshold tasks comprising a measure of global motion processing, a measure of static global form processing with a randomized target position and a measure of static global form processing where the target position was fixed. They found that the children with DCD performed poorer than the control on both dorsal and ventral stream function tests (Sigmundsson et al., 2003). Bonifacci evaluated the children at risk for DCD and found these children demonstrated lower visual-motor integration ability but unaffected perceptual skills (Bonifacci, 2004). Therefore it is important to identify the connection between the visual-perceptual ability and the motor function in children with DCD. Tsai et al. have examined TVPS-R of a group of children with DCD and found that these children scored significantly lower than typically developing children (Tsai et al., 2008). They also found while the group differences in visual-perceptual abilities between DCD and typically developing children were statistically significant, some of the children with DCD did not have general visual-perceptual dysfunction. Although their results have identified the connection between some of the static visual-perceptual ability (via TVPS-R) and the motor function in children with DCD, the visual response to dynamic stimulation was not evaluated. The commonly used motor test for the DCD identification is the Movement Assessment Battery for Children-2 (MABC-2) (Venetsanou et al., 2011). It is a product oriented and norm referenced test designed for identifying children aged 3–12 years with motor difficulties (Henderson & Sugden, 1992, 2007). This test consists of eight items grouped into three sections – manual dexterity (MD), aiming and catching (A&C), and balance (Bal) – and the item content differentiates according to the examinee’s age. This test is popular since it is well organized with few items to facilitate large sample screening over a short period, as well as its administration guidelines have been translated into numerous languages (Tsai et al., 2008). However, the MABC-2 is not yet a ‘‘gold standard’’ for the assessment of children with DCD since it does not identify all subtypes of DCD (Niemeijer, Smits-Engelsman, & Schoemaker, 2007; Venetsanou et al., 2011). To date, MABC-2 was mainly used to examine the motor performance rather than the visual-perceptual function of the children (Venetsanou et al., 2011). To better assess children’s visual-perceptual skills, supplementary tools should be included. There are two different neural pathways which process two different types of visual function. Ventral stream structures are involved more in providing information about the surface properties of objects such as their shape and color, whereas dorsal stream structures generally convey information about the spatial relations between objects and about their motion (Merigan & Maunsell, 1993). To differentiate children with DCD from the others, the Test of Visual Perceptual Skills-Revised (TVPS-R, Gardner, 1996) was often used for evaluating visual-perceptual function. Among its subtests, visual closure or visual discrimination could be linked to the ventral-visual stream, whereas visual–spatial relationships are more likely to be linked to the dorsal-visual stream (Tsai et al., 2008). In addition, the shift of gaze (Wilmut, Wann, & Brown, 2006), test for eye-hand coordination, and the motion coherence thresholds measurements were used for testing dorsal stream function. Nevertheless, since the children with DCD demonstrate problems in both ventral and dorsal visual streams, result from one single test does not represent the particular children is at risk. But screening children with multiple tests is neither timely nor efficient. The purpose of this study was to examine to what extent the test of the MABC-2 is linked to the visual-perceptual abilities of children with DCD. Static as well as dynamic aspects of visual-perceptual abilities, including the visual discrimination, visual form-constancy, visual sequential-memory, visual closure, sequential coupling of eye and hand, and motion coherence, were evaluated. The results of this study will facilitate the MABC-2 as a prescreening tool to verify if the motor deficits of the children with DCD are related to the visual-perception problems. 2. Method 2.1. Participants The authors screened a total of 250 children between 5 and 10 years via convenience sampling from the local school/ preschool and community center. Children were included in the DCD group if they were right handed, scored below the 15th percentile on the MABC-2, without any neurological or physical pathology as examined by a rehabilitation doctor. The 15
2174
C.-H. Cheng et al. / Research in Developmental Disabilities 35 (2014) 2172–2179
percentile instead of the 5th was used because we would like to include those children with a borderline and a deviant performance, and this approach was common in the reported research literature (Geuze, Jongmans, Schoemaker, & SmitsEngelsman, 2001; Johnson & Wade, 2009). The exclusion criteria were any obvious deficits in attention such as having attention deficit hyperactivity disorder, experience in switching dominant hand, and visual deficits which cannot be corrected by surgical procedure or glasses. Exclusion Criteria were assessed by way of parental questionnaires in conjunction with a neuro-developmental examination given by a physician. The typically developing (TD) group included age-matched children who scored above 25th percentile on the MABC-2, right handed and never switched hand dominancy. The Institutional Review Board for Human Studies of Chang Gung Memorial Hospital approved this protocol. Written informed consents were obtained from all participants and their legal guardians. 2.2. Assessments The comprehensive assessment included the paper test (test 1) and the computerized test (tests 2 and 3). LabView 2010 (National Instruments, Austin, TX, USA) was used to develop the visualized program. The computerized test was executed using a 14.1-in. laptop with 60 Hz vertical scan frequency. 2.2.1. Test 1: TVPS-R TVPS-R measures the ability of the brain to make sense of what the eyes see. Among its seven subtests, the visual discrimination, visual form-constancy, visual sequential-memory, and visual closure were chosen since they are sensitive to expose the visual-perceptual deficits in the children with DCD (Niemeijer, Smits-Engelsman, & Schoemaker, 2007; Schoemaker et al., 2001). The subjects would be asked to identify the designated item in the figures according to the different objectives of the four subtests. The numbers of the correct answers would be recorded. 2.2.2. Test 2: Sequential coupling of eye and hand This test was designed to test the ability to shift between the feed-forward and feedback control system of the children with DCD, since evidence suggests that they may have problems with both systems (Wilmut et al., 2006). Three conditions with two sides (left or right) were measured: single (one target), double (two targets) and double-off (two targets appeared, then disappeared) (abbreviated as SL, SR, DL, DR, OL, and OR, respectively). A yellow cue and three possible target circles with the same diameter of 10 mm were presented on the screen at the left and right side of the midline separately, and the yellow cue was at the far left and far right locations (Fig. 1). The subjects were instructed to locate the target and any subsequent target by pressing the corresponding keys on the traditional keyboard as soon as possible (right keys were operated by the right hand and left keys by the left hand). When the trial started, the yellow cue acted as a precursor indicating the subsequent red circles would light up on the same side. Soon the yellow cue disappeared and the target in red appeared immediately at each of the three target locations. In the double and double-off conditions, a second red target appeared 200 ms later at the location opposite to the side of cue. In the double condition, the two red targets would show until being reset. In the double-off condition, both targets disappeared 250 ms after onset. The order of condition was fixed for all children to make it easier for them to understand the tasks (Wilmut et al., 2006). A randomized order risks the possibility that
[(Fig._1)TD$IG]
Fig. 1. Illustration of the target locations in the ‘‘sequential coupling of eye and hand’’ test.
C.-H. Cheng et al. / Research in Developmental Disabilities 35 (2014) 2172–2179
2175
a child does poorly on the most difficult task (e.g. double-off) because it was presented first, or that they only did well on the single-target task because of the practice that proceeded. The reaction time was defined as the time when the cue showed to that the correct key being pressed down. Three complete trials were recorded for each task. 2.2.3. Test 3: Motion coherence Dynamic random dot kinematogram was used to test subject’s global motion processing. The test consisted of identifying two kinds of patches: one is the target with a constant moving velocity and direction (8.78/s toward the left or right side of the screen), and the other is the interfering point moving in a Brownian manner. The threshold is defined as the ratio of number of the targets to that of the interfering points. The higher threshold the subject get, the poorer the sensitivity of the motion perception for the subject is. The test began with 100% threshold, i.e. all the patches moving in the same velocity and direction. If the subject correctly recognized the moving direction of the targets, the threshold would be decreased by 1 dB in the following repetition, otherwise increased by 3 dB. The whole procedure was repeated eight times. The thresholds of the last six times were averaged. Two rounds were executed, and the thresholds from two rounds were recorded. 2.2.4. Test–retest reliability To ensure the visual-perception tests used in current study are reliable, twenty typically developing children were recruited for the test–retest reliability, separated by a week interval. The results showed moderate to high reliability for all three tests (rtest1 = 0.461, ptest1 = 0.041; rtest2 = 0.704, ptest2 = 0.001; rtest3 = 0.858, ptest3 < 0.001). 2.3. Design and procedure A total of 250 children was identified and categorized into two groups (DCD and TD) via the MABC-2 test. After the grouping was done, an occupational therapist who was blind to the group membership of these children then individually administered the test 1 using standard procedures. For the computer tests (tests 2 and 3), the subjects were asked to sit 0.5 m in front of the monitor with eye level in the height of the center of the screen when taking the computerized tests. The height of the armrest was adjusted to a comfortable position, and both feet were on the level ground. Five practice trials were allowed. There were 3–5 min resting intervals among the tests. The data would be excluded when the subjects could not concentrate or complete the tests. 2.4. Data analysis The t-test was used to examine the differences between the children with DCD and TD for the MABC-2 test, visualperception test 1 and 3. Three-way ANOVA with repeated measures on groups (DCD/TD), conditions (single/double/double off), and sides (left/right) was used for the test 2. The Pearson correlation analysis was also applied to reveal the correlation between the MABC-2 and each of the visual-perceptual tests. The significance level was set at 0.05. 3. Results From a total of 250 children, seventeen DCD (7.25 0.28 years) and seventeen TD (7.09 0.34 years) were recruited. The ratio of males to females in the DCD group (12:5) was higher than that in the TD group (8:9). The age difference in two groups was not significant (p = 0.139). For the MABC-2 score, significant differences were found between the two groups (total: 54.9 10.5 and 84.2 6.9; MD: 19.1 6.7 and 32.9 5.1; A&C: 14.4 3.8 and 19.8 4.4; Bal: 21.5 4.9 and 31.4 3.7 for the DCD and TD group respectively, all p < 0.001). As for the DCD group, the total score was highly correlated with the score for MD (r = 0.746), moderately correlated with the score for A&C (r = 0.561), and moderately correlated with the score for Bal (r = 0.669). As for TD, the total score was only moderately correlated with the score for A&C (r = 0.557) and Bal (r = 0.639), respectively (Table 1).
Table 1 Pearson correlation (with p value in the parenthesis) between the component scores and total scores of the M-ABC 2 in children with DCD and in typically developing (TD) children. DCD
Total MD A&C Bal
TD
Total
MD
A&C
Bal
Total
MD
A&C
Bal
1 .746** (.001) .561* (.019) 669** (.003)
– 1 .072 (.785) .152 (.561)
– – 1 .308 (.229)
– – – 1
1 .398 (.114) .557* (.020) .639** (.006)
– 1 .383 (.129) .191 (.464)
– – 1 .373 (.140)
– – – 1
Total: the total score of M-ABC-2; MD: manual dexterity; A&C: aiming and catching; Bal: balance. ** p < .01. * p < .05.
C.-H. Cheng et al. / Research in Developmental Disabilities 35 (2014) 2172–2179
2176
Table 2 Pearson correlation (with p value in the parenthesis) between each subtest in test 1 (TVPS-R) and each component score of M-ABC-2 in children with DCD and in typically developing (TD) children. DCD
TD
DIS Total MD A&C Bal
CON
.329 (.184) .093 (.723) .638** (.006) .085 (.744)
SEQ
.044 .175 .152 .033
(.866) (.500) (.561) (.900)
FGR
.379 (.133) .651** (.005) .015 (.953) .092 (.726)
DIS
.167 .313 .123 .039
(.521) (.221) (.638) (.882)
CON
.000 .470 .345 .252
(.999) (.057) (.176) (.329)
SEQ
.101 .119 .623 .049
(.699) (.648) (.929) (.852)
.203 .305 .209 .200
FGR (.434) (.234) (.421) (.441)
.039 .008 .670 .150
(.881) (.977) (.784) (.566)
Total: the total score of M-ABC-2; MD: manual dexterity; A&C: aiming and catching; Bal: balance; DIS: visual discrimination; CON: form constancy; SEQ: sequential memory; FGR: figure ground. ** p < .01. Table 3 Descriptive and inferential statistics for each subtest in test 2 (sequential coupling of eye and hand) in children with DCD and in typically developing (TD) children. Left
DCD TD Side mean
Right
Group mean
SL
DL
OL
SR
DR
OR
0.57 (.28) 0.42 (.26)
0.70 (.47) 0.43 (.27) 0.51 (.30)§
0.57* (.30) 0.38 (.22)
0.74 (.33) 0.47 (.28)
0.74 (.47) 0.51 (.36) .61 (.37)
0.71* (.46) 0.48 (.30)
0.67*(.39) 0.45 (.28)
Mean (SD): in s. * Significant difference between the DCD and TD group. § Significant difference between the two sides.
3.1. Test 1 For group comparisons between the DCD and TD, significant differences were found in all the subtests including visual discrimination (8.9 3.3 and 11.5 3.8, p = 0.049), form consistency (9.1 3.3 and 11.6 3.6, p = 0.039), sequential memory (12.0 3.2 and 14.2 2.2, p = 0.048) and figure-ground (9.6 2.2 and 12.0 3.2, p = 0.009). Children with DCD scored lower than TD. Correlation tests for the group of DCD revealed a moderate correlation between the visual discrimination and the A&C (r = 0.638). A moderate correlation was also found between the visual sequential memory and the MD (r = 0.651). No other statistical significance was found between other measurements. All these measurements demonstrated no significant correlation in TD (Table 2). 3.2. Test 2 There were significant differences in the main effect of the group (p = 0.043) and side (p < 0.001). Significant differences were found between OL (p = 0.023)/OR (p = 0.048). No statistical significance was found in other subtests or interactions (Table 3). As to the correlation between each subtest and the measurements of MABC-2, the analyses revealed moderate correlation between SL/OR and the total score of MABC-2 (r = 0.554/ 0.486), and between DL/DR/OR and A&C score (r = 0.482/ 0.488/ 0.599). None of the subtests correlated significantly with the MABC-2 scores in TD (Table 4). 3.3. Test 3 The threshold of the motion coherence test was significantly greater in DCD (0.60 0.14) than in TD (0.47 0.14) (p < 0.016). Correlation tests revealed that the threshold was moderately correlated with the total score of MABC-2 (r = 0.670), MD (r = 0.489), and Bal (r = 0.554). No significant correlation was found in TD (Table 5).
Table 4 Pearson correlation (with p value in the parenthesis) between each subtest in test 2 (sequential coupling of eye and hand) and each component score of MABC-2 in children with DCD and in typically developing (TD) children. DCD SL Total MD A&C Bal
.554* (.021) .338 (.184) .459 (.064) .345 (.175)
TD DL .202 (.438) .123 (.637) .482* (.050) .204 (.433)
OL .329 .142 .373 .203
SR (.198) (.586) (.140) (.435)
.371 .131 .401 .286
DR (.142) (.617) (.111) (.266)
.117 (.654) .163 (.533) .488* (.047) .066 (.801)
OR .486* (.048) .242 (.350) .599* (.011) .212 (.414)
SL .243 .081 .340 .158
DL (.348) (.756) (.182) (.545)
.184 .026 .112 .169
OL (.480) (.921) (.668) (.518)
.358 .043 .490 .023
SR (.158) (.871) (.056) (.930)
.361 .056 .328 .201
DR (.154) (.832) (.199) (.440)
.168 .048 .185 .024
OR (.519) (.854) (.478) (.928)
.148 .000 .089 .166
(.571) (.999) (.734) (.525)
Total: the total score of M-ABC-2; MD: manual dexterity; A&C: aiming and catching; Bal: balance; SL: single left; SR: single right; DL: double left; DR: double right; OL: double-off left; OR: double-off right. * p < .05.
C.-H. Cheng et al. / Research in Developmental Disabilities 35 (2014) 2172–2179
2177
Table 5 Pearson correlation (with p value in the parenthesis) between the test 3 (motion coherence) and each component score of M-ABC-2 in children with DCD and in typically developing (TD) children. DCD Total MD A&C Bal
.670** (.003) .489* (.046) .275 (.286) .554* (.021)
TD .052 .172 .034 .175
(.844) (.509) (.897) (.501)
Total: the total score of M-ABC-2; MD: manual dexterity; A&C: aiming and catching; Bal: balance. ** p < .01. * p < .05.
4. Discussion This study was to examine the multiple aspects of the visual-perceptual abilities of the children with DCD, as well as their links to the motor deficits. The major findings were that children with DCD showed significantly poorer performance compared to TD on the visual-perceptual test. The visual discrimination, visual sequential memory, sequential coupling of eye and hand, and motion coherence demonstrated a moderate or strong correlation with the MABC-2. For everyday tasks and assessment batteries such as the MABC, a smooth transition between sequential movements is required (Wilmut et al., 2006). These indicated that the poor performance within DCD in the tasks like static visual discrimination, visual sequential memory and sequential coupling of eye and hand would inevitably lead to slowness in the completion of MABC-2 or everyday tasks. Unlike children with DCD, visual-perceptual abilities of the TD were not correlated with their motor performance as evaluated with MABC-2. Based on those results, the children with DCD could have problem in coordinating the visual signals to perform motor tasks, thus the visual-perceptual ability of the children with DCD should be carefully assessed when checking their motor functions. The sex ratio of male to female in the DCD group was around 2:1, which corresponds to the gender distribution of DCD population (Cermak & Larkin, 2002). Motor function assessments via the MABC-2, including the total score as well as the scores of its corresponding components, were all significantly different between the two groups. For the children with DCD, the total score of MABC-2 showed moderate to high correlation to its component scores, especially in the MD component compared to the TD group. Based on the user manual of MABC-2, the MD component measures the speed and accuracy of hand movement, bimanual coordination, and eye-hand coordination (Henderson & Sugden, 1992, 2007). These indicated that children with DCD demonstrated the soft neurological signs, suggesting the presence of cerebellar dysfunction (Cantin, Polatajko, Thach, & Jaglal, 2007). In test 1, the children with DCD showed significantly poorer accuracy of the visual-perceptual performance than the TD in all subtests. While comparing the test 1 to MABC-2, significant correlations were found between the visual discrimination and the A&C, and between the visual sequential-memory and the MD, in the children with DCD. No significant correlation among these variables was noted in the TD group (Table 2). The visual discrimination subtest is to find the correct design from a group of similar ones, which relies heavily on the process of the visual-perception codes. Previous study has shown that the children with DCD have difficulty in translating the signal from the visual-perception codes into the motor plan (Wilson & McKenzie, 1998). Aiming and catching, a dynamic task requiring the child to accurately perceive the trajectory and speed of an approaching object, is more susceptible to other factors such as motor planning of other effectors compared to a pure reaching to a static target (Lee, Poizner, Corcos, & Henriques, 2014). A poor performance on visual discrimination indicated more time is needed to discriminate and process the location of a moving object, therefore led to poorer performance on A&C. Thus the inferior ability of the A&C in the DCD group compared to the TD group in this study could attribute to the processing fault in the path from visual-perception to movement response. In regards to the visual sequential memory, it is the ability to examine a series of various designs and then identify that particular series from four others. Deficits in this ability reflect problems in signal processing, or in coping with complex signals and therefore causing motor clumsiness. As for test 2, children with DCD showed significantly longer reaction time than TD. There were also moderate correlations between most of the subtests and the total score of MABC-2. The findings indicated that the motor performance of children with DCD, especially during the A&C, was related to the sequential coupling process of eye and hand. In this study, the double-off condition, where two movements were made but both targets to which movements were generated disappeared prior to initiation of a hand movement, might lead to greater errors in children with DCD. In this condition, movements had to be completed purely on the basis of initial visual coding of target location rather than feedback information. Previous research indicated that, while executing simple or single-step goal-oriented visual motor tasks, the performance of children with DCD and was similar to that of TD. However during complex or multi-steps goal-oriented movements, children with DCD made more errors and took more time to focus on the target prior to the initiation of a hand movement (Wilmut et al., 2006). Regarding the motor control mechanism, these results indicated that children with DCD relied on feedback control to correct and coordinate their movements, which meant that they could not predict the upcoming event and plan their actions
2178
C.-H. Cheng et al. / Research in Developmental Disabilities 35 (2014) 2172–2179
in a feed-forward manner (Gheysen, Waelvelde, & Fias, 2011; Smits-Engelsman, Wilson, Westenberg, & Duysens, 2003; Wilmut & Wann, 2008; Wilson, Thamas, & Maruff, 2002). These facts led to a longer period in predicting signal directions and decision making and therefore poor aiming and catching ability. In regards to test 3, children with DCD demonstrated significantly higher threshold than TD, which meant that children with DCD were less sensitive to this dynamic random dot motion coherence test. The result was similar to those found by Sigmundsson et al. (2003). They found that the clumsy children, who were diagnosed solely on the basis of their motor difficulties, were significantly less sensitive than the control group on visual sensitivity tasks. Further correlation analyses found the average threshold in test 3 was moderately correlated with the total score of MABC-2, and the MD and the Bal component scores of MABC-2 in children with DCD. However such correlation was not found in TD group (Table 3). Test 3 measured global motion processing using a dynamic random dot kinematogram with embedded noise. Direct visual attention is therefore needed to justify the direction of those moving dots. According to Cherng et al., attention constitutes a mental resource that supports mental information processing of the mind (Cherng, Liang, Chen, & Chen, 2009). Various pools are involved in this mental resource, such as the stage of processing (perceptual, central or response), the codes of processing (verbal or spatial), and the modalities of input (visual or auditory) and response (manual or vocal). If two simultaneous tasks compete for the same pool of attention resource, they would interfere with each other and there will not be enough resource for both. The motor performance will be affected as a result. In addition, when a motor task is less automatic, it requires greater attention control and is more affected by a concurrently performed task (Tsai et al., 2008). Since children with DCD rely more on visual information during balance tasks, this explained why the coherence threshold is highly correlated with the Bal component in MABC-2. Limitations of the present study were that the comorbidities such as dyslexia or sensory processing disorders were not screened during subject recruitment. The exclusion criteria were any obvious deficits in attention such as having attention deficit hyperactivity disorder, experience in switching dominant hand, and visual deficits which cannot be corrected by surgical procedure or glasses. Since these co-existing disorders might also affect subject’s visual-perceptual function, it would be a plus if we consider the heterogeneous characteristics of children with DCD in future studies. 5. Conclusion In conclusion, this study showed that the motor problems screened by the tests of MABC-2 were significantly related to the visual-perceptual deficits of children with DCD. The correlation between the motor deficits and the visual-perceptual problems could be due to the fault of the input/output processing in the brain. MABC-2 is suggested to be a prescreening tool for verifying whether their motor deficits are linked to the visual-perceptual problems, therefore reducing the time needed for multiple clinical assessments. Findings could also be further used to develop integrated visual-motor examination tools or specific educational interventions for children with DCD. Conflict of interest The authors did not have any financial and personal relationship with other people or organization that could inappropriately influence this work. Acknowledgements The authors would like to thank for the participation of all children, parents, school teachers and staff in this study. This work was supported by the Ministry of Science and Technology (101-2221-E-182-020-MY3), and the Chang Gung Medical Research Program (CMRP), Taiwan (Grant no. CMRPD 1A0691 and 1A0692 ). References American Psychological Association (2013). Diagnostic and statistical manual of mental disorders: DSM-V. Washington, DC: American Psychological Association. Bonifacci, P. (2004). Children with low motor ability have lower visual-motor integration ability but unaffected perceptual skills. Human Movement Science, 23(2), 157–168. Cantin, N., Polatajko, H. J., Thach, W. T., & Jaglal, S. (2007). Developmental coordination disorder: Exploration of a cerebellar hypothesis. Human Movement Science, 26(3), 491–509. Cermak, S. A., & Larkin, D. (2002). Developmental coordination disorder. Canada: Thomson Learning. Cherng, R. J., Liang, L. Y., Chen, Y. J., & Chen, J. Y. (2009). The effects of a motor and a cognitive concurrent task on walking in children with developmental coordination disorder. Gait & Posture, 29(2), 204–207. Gardner, M. F. (1996). Test of visual perceptual skills (non-motor)-revised. Hydesville, CA: Psychological and Educatonal Publications -revised. Geuze, R. H., Jongmans, M. J., Schoemaker, M. M., & Smits-Engelsman, B. C. M. (2001). Clinical and research diagnostic criteria for developmental coordination disorder: A review and discussion. Human Movement Science, 20, 7–47. Gheysen, F., Waelvelde, H. V., & Fias, W. (2011). Impaired visuo-motor sequence learning in DCD. Research in Developmental Disabilities, 32, 749–756. Henderson, S. E., & Sugden, D. A. (1992). Movement assessment battery for children. London, UK: The Psychological Corporation. Henderson, S. E., & Sugden, D. A. (2007). Movement assessment battery for children (2nd ed.). London, UK: The Psychological Corporation. Hoare, D. (1994). Subtypes of developmental coordination disorder. Adapted Physical Activity Quarterly, 11(2), 158–169. Johnson, D. C., & Wade, M. G. (2009). Children at risk for developmental coordination disorder: Judgement of changes in action capabilities. Developmental Medicine and Child Neurology, 51(5), 397–403. Lee, D., Poizner, H., Corcos, D. M., & Henriques, D. Y. (2014). Unconstrained reaching modulates eye-hand coupling. Experimental Brain Research, 232(1), 211–223.
C.-H. Cheng et al. / Research in Developmental Disabilities 35 (2014) 2172–2179
2179
Macnab, J. J., Miller, L. T., & Polatajko, H. J. (2001). The search for subtypes of DCD: Is cluster analysis the answer? Human Movement Science, 20(1–2), 49–72. Merigan, W. H., & Maunsell, J. H. R. (1993). How parallel are the primate visual pathways? Annual Review of Neuroscience, 16, 369–402. Niemeijer, A. S., Smits-Engelsman, B. C. M., & Schoemaker, M. M. (2007). Neuromotor task training for children with developmental coordination disorder: A controlled trial. Developmental Medicine and Child Neurology, 49(6), 406–411. Piek, J. P., & Dyck, M. J. (2004). Sensory-motor deficits in children with developmental coordination disorder, attention deficit hyperactivity disorder and autistic disorder. Human Movement Science, 23(3–4), 475–488. Schoemaker, M. M., Wees, M., Flapper, v. d. B., Verheij-Jansen, N., Scholten-Jaegers, S., & Geuze, R. H. (2001). Perception skill of children with developmental coordination disorder. Human Movement Science, 20, 111–133. Sigmundsson, H., Hansen, P. C., & Talcott, J. B. (2003). Do ‘clumsy’ children have visual deficits. Behavioural Brain Research, 139(1–2), 123–129. Smits-Engelsman, B. C. M., Wilson, P. H., Westenberg, Y., & Duysens, J. (2003). Fine motor deficiencies in children with developmental coordination disorder and learning disabilities: An underlying open-loop control deficit. Human Movement Science, 22, 459–513. Tsai, C. L., Wilson, P. H., & Wu, S. K. (2008). Role of visual-perceptual skills (non-motor) in children with developmental coordination disorder. Human Movement Science, 27(4), 649–664. Van Waelvelde, H., De Weerdt, W., De Cock, P., & Smits-Engelsman, B. C. M. (2004). Aspects of the validity of the Movement Assessment Battery for Children. Human Movement Science, 23(1), 49–60. Venetsanou, F., Kambas, A., Ellinoudis, T., Fatouros, I., Giannakidou, D., & Kourtessis, T. (2011). Can the Movement Assessment Battery for Children-Test be the ‘‘gold standard’’ for the motor assessment of children with Developmental Coordination Disorder? Research in Developmental Disabilities, 32(1), 1–10. Wilmut, K., & Wann, J. (2008). The use of predictive information is impaired in the actions of children and young adults with Developmental Coordination Disorder. Experimental Brain Research, 191, 403–418. Wilmut, K., Wann, J. P., & Brown, J. H. (2006). Problems in the coupling of eye and hand in the sequential movements of children with Developmental Coordination Disorder. Child: Care, Health and Development, 32(6), 665–678. Wilson, P. H., & McKenzie, B. E. (1998). Information processing deficits associated with developmental coordination disorder: A meta-analysis of research findings. Journal of Child Psychology and Psychiatry, 39(6), 829–840. Wilson, P. H., Thamas, P. R., & Maruff, P. (2002). Motor imagery training ameliorates motor clumsiness in children. Journal of Child Neurology, 17(7), 491–498. Zwicker, J. G., Missiuna, C., Harris, S. R., & Boyd, L. A. (2012). Developmental coordination disorder: A review and update. European Journal of Paediatric Neurology, 16(6), 573–581.
Contents lists available at ScienceDirect
Research in Developmental Disabilities
Motor impairments screened by the Movement Assessment Battery for Children-2 are related to the visual-perceptual deficits in children with Developmental Coordination Disorder Chih-Hsiu Cheng a,1, Yan-Ying Ju b, Hsin-Wen Chang c, Chia-Ling Chen c, Yu-Cheng Pei d, Kevin C. Tseng e, Hsin-Yi Kathy Cheng c,* a
Department of Physical Therapy and Graduate Institute of Rehabilitation Science, College of Medicine, Chang Gung University, Tao-Yuan 333, Taiwan b Department of Adapted Physical Education, National Taiwan Sport University, 250 Wen-Hua 1st Road, Kwei-Shan, Tao-Yuan 333, Taiwan c Graduate Institute of Early Intervention, College of Medicine, Chang Gung University, 259 Wen-Hua 1st Road, Kwei-Shan, Tao-Yuan 333, Taiwan d Department of Physical Medicine and Rehabilitation, Chang Gung Memorial Hospital, Tao-Yuan, Taiwan e Department of Industrial Design, College of Management, Chang Gung University, 259 Wenhua 1st Road, Guishan, Tao-Yuan 33302, Taiwan
A R T I C L E I N F O
A B S T R A C T
Article history: Received 11 March 2014 Received in revised form 8 May 2014 Accepted 16 May 2014 Available online
This study was to examine to what extent the motor deficits of children with Developmental Coordination Disorder (DCD) verified by the Movement Assessment Battery for Children-2 (MABC-2) are linked to their visual-perceptual abilities. Seventeen children with DCD and seventeen typically developing children (TD) aged 5–10 years screened from a total of 250 children were recruited. The assessments included MABC-2, traditional test of visual perceptual skills (TVPS-R), and computerized test for sequential coupling of eye and hand as well as motion coherence. The results indicated that children with DCD scored lower than TD in MABC-2, and their total scores were highly correlated with manual dexterity component scores. DCD group also showed poor visual-perceptual abilities in various aspects. The visual discrimination and visual sequential memory from the TVPS-R, the sequential coupling of eye and hand, and the motion coherence demonstrated a moderate or strong correlation with the MABC-2 in the DCD rather than the TD group. It was concluded that the motor problems screened by MABC-2 were significantly related to the visual-perceptual deficits of children with DCD. MABC-2 is suggested to be a prescreening tool to identify the visual-perceptual related motor deficits. ß 2014 Elsevier Ltd. All rights reserved.
Keywords: Developmental Coordination Disorder Perception Movement Manual dexterity Balance
* Corresponding author. Tel.: +886 3 211 8800x3667; fax: +886 3 211 8700. E-mail addresses: [email protected] (C.-H. Cheng), [email protected] (Y.-Y. Ju), [email protected] (H.-W. Chang), [email protected] (C.-L. Chen), [email protected] (Y.-C. Pei), [email protected] (K.C. Tseng), [email protected], [email protected] (H.-Y. Cheng). 1 Tel.: +886 3 211 8800x3714. http://dx.doi.org/10.1016/j.ridd.2014.05.009 0891-4222/ß 2014 Elsevier Ltd. All rights reserved.
C.-H. Cheng et al. / Research in Developmental Disabilities 35 (2014) 2172–2179
2173
1. Introduction Developmental Coordination Disorder (also known as Dyspraxia), is the term used to describe a range of difficulties that children experience with posture, movement and coordination, without any specific medical reason for these difficulties (American Psychological Association, 2013). The most commonly reported prevalence of DCD is 5–6% (Zwicker, Missiuna, Harris, & Boyd, 2012). These children typically have difficulties with fine and/or gross motor skills, and demonstrated a slower, less accurate and variable motor performance, and tend to withdraw from physical play with other children (Piek & Dyck, 2004). Despite a generalized impairment in nearly all areas of motor performances, the children with DCD show considerable variation in the degree and pattern of perceptual-motor deficits (Tsai, Wilson, & Wu, 2008). Some studies suggested to consider subtypes of DCD based on visual dysfunctions (Hoare, 1994; Macnab, Miller, & Polatajko, 2001), such as deficits in visual-motor integration (Bonifacci, 2004; Van Waelvelde, De Weerdt, De Cock, & Smits-Engelsman, 2004; Wilson & McKenzie, 1998), impaired visual sensitivity (Sigmundsson, Hansen, & Talcott, 2003), or visual-spatial processing (Wilson & McKenzie, 1998). Visual perception concerns both object identity and localization in space, and is intimately connected with action systems. Any deficit in this processing network leads to problems in movement planning, on-line movement correction, and feedback control (Wilson & McKenzie, 1998). However, in terms of motor-free visual-perceptual ability, some studies have found conflicting results. Sigmundsson et al. (2003) found that children with DCD showed impaired visual sensitivity, but Bonifacci (2004) did not. Sigmundsson et al. tested children with developmental ‘‘clumsiness’’ on a series of visual coherence threshold tasks comprising a measure of global motion processing, a measure of static global form processing with a randomized target position and a measure of static global form processing where the target position was fixed. They found that the children with DCD performed poorer than the control on both dorsal and ventral stream function tests (Sigmundsson et al., 2003). Bonifacci evaluated the children at risk for DCD and found these children demonstrated lower visual-motor integration ability but unaffected perceptual skills (Bonifacci, 2004). Therefore it is important to identify the connection between the visual-perceptual ability and the motor function in children with DCD. Tsai et al. have examined TVPS-R of a group of children with DCD and found that these children scored significantly lower than typically developing children (Tsai et al., 2008). They also found while the group differences in visual-perceptual abilities between DCD and typically developing children were statistically significant, some of the children with DCD did not have general visual-perceptual dysfunction. Although their results have identified the connection between some of the static visual-perceptual ability (via TVPS-R) and the motor function in children with DCD, the visual response to dynamic stimulation was not evaluated. The commonly used motor test for the DCD identification is the Movement Assessment Battery for Children-2 (MABC-2) (Venetsanou et al., 2011). It is a product oriented and norm referenced test designed for identifying children aged 3–12 years with motor difficulties (Henderson & Sugden, 1992, 2007). This test consists of eight items grouped into three sections – manual dexterity (MD), aiming and catching (A&C), and balance (Bal) – and the item content differentiates according to the examinee’s age. This test is popular since it is well organized with few items to facilitate large sample screening over a short period, as well as its administration guidelines have been translated into numerous languages (Tsai et al., 2008). However, the MABC-2 is not yet a ‘‘gold standard’’ for the assessment of children with DCD since it does not identify all subtypes of DCD (Niemeijer, Smits-Engelsman, & Schoemaker, 2007; Venetsanou et al., 2011). To date, MABC-2 was mainly used to examine the motor performance rather than the visual-perceptual function of the children (Venetsanou et al., 2011). To better assess children’s visual-perceptual skills, supplementary tools should be included. There are two different neural pathways which process two different types of visual function. Ventral stream structures are involved more in providing information about the surface properties of objects such as their shape and color, whereas dorsal stream structures generally convey information about the spatial relations between objects and about their motion (Merigan & Maunsell, 1993). To differentiate children with DCD from the others, the Test of Visual Perceptual Skills-Revised (TVPS-R, Gardner, 1996) was often used for evaluating visual-perceptual function. Among its subtests, visual closure or visual discrimination could be linked to the ventral-visual stream, whereas visual–spatial relationships are more likely to be linked to the dorsal-visual stream (Tsai et al., 2008). In addition, the shift of gaze (Wilmut, Wann, & Brown, 2006), test for eye-hand coordination, and the motion coherence thresholds measurements were used for testing dorsal stream function. Nevertheless, since the children with DCD demonstrate problems in both ventral and dorsal visual streams, result from one single test does not represent the particular children is at risk. But screening children with multiple tests is neither timely nor efficient. The purpose of this study was to examine to what extent the test of the MABC-2 is linked to the visual-perceptual abilities of children with DCD. Static as well as dynamic aspects of visual-perceptual abilities, including the visual discrimination, visual form-constancy, visual sequential-memory, visual closure, sequential coupling of eye and hand, and motion coherence, were evaluated. The results of this study will facilitate the MABC-2 as a prescreening tool to verify if the motor deficits of the children with DCD are related to the visual-perception problems. 2. Method 2.1. Participants The authors screened a total of 250 children between 5 and 10 years via convenience sampling from the local school/ preschool and community center. Children were included in the DCD group if they were right handed, scored below the 15th percentile on the MABC-2, without any neurological or physical pathology as examined by a rehabilitation doctor. The 15
2174
C.-H. Cheng et al. / Research in Developmental Disabilities 35 (2014) 2172–2179
percentile instead of the 5th was used because we would like to include those children with a borderline and a deviant performance, and this approach was common in the reported research literature (Geuze, Jongmans, Schoemaker, & SmitsEngelsman, 2001; Johnson & Wade, 2009). The exclusion criteria were any obvious deficits in attention such as having attention deficit hyperactivity disorder, experience in switching dominant hand, and visual deficits which cannot be corrected by surgical procedure or glasses. Exclusion Criteria were assessed by way of parental questionnaires in conjunction with a neuro-developmental examination given by a physician. The typically developing (TD) group included age-matched children who scored above 25th percentile on the MABC-2, right handed and never switched hand dominancy. The Institutional Review Board for Human Studies of Chang Gung Memorial Hospital approved this protocol. Written informed consents were obtained from all participants and their legal guardians. 2.2. Assessments The comprehensive assessment included the paper test (test 1) and the computerized test (tests 2 and 3). LabView 2010 (National Instruments, Austin, TX, USA) was used to develop the visualized program. The computerized test was executed using a 14.1-in. laptop with 60 Hz vertical scan frequency. 2.2.1. Test 1: TVPS-R TVPS-R measures the ability of the brain to make sense of what the eyes see. Among its seven subtests, the visual discrimination, visual form-constancy, visual sequential-memory, and visual closure were chosen since they are sensitive to expose the visual-perceptual deficits in the children with DCD (Niemeijer, Smits-Engelsman, & Schoemaker, 2007; Schoemaker et al., 2001). The subjects would be asked to identify the designated item in the figures according to the different objectives of the four subtests. The numbers of the correct answers would be recorded. 2.2.2. Test 2: Sequential coupling of eye and hand This test was designed to test the ability to shift between the feed-forward and feedback control system of the children with DCD, since evidence suggests that they may have problems with both systems (Wilmut et al., 2006). Three conditions with two sides (left or right) were measured: single (one target), double (two targets) and double-off (two targets appeared, then disappeared) (abbreviated as SL, SR, DL, DR, OL, and OR, respectively). A yellow cue and three possible target circles with the same diameter of 10 mm were presented on the screen at the left and right side of the midline separately, and the yellow cue was at the far left and far right locations (Fig. 1). The subjects were instructed to locate the target and any subsequent target by pressing the corresponding keys on the traditional keyboard as soon as possible (right keys were operated by the right hand and left keys by the left hand). When the trial started, the yellow cue acted as a precursor indicating the subsequent red circles would light up on the same side. Soon the yellow cue disappeared and the target in red appeared immediately at each of the three target locations. In the double and double-off conditions, a second red target appeared 200 ms later at the location opposite to the side of cue. In the double condition, the two red targets would show until being reset. In the double-off condition, both targets disappeared 250 ms after onset. The order of condition was fixed for all children to make it easier for them to understand the tasks (Wilmut et al., 2006). A randomized order risks the possibility that
[(Fig._1)TD$IG]
Fig. 1. Illustration of the target locations in the ‘‘sequential coupling of eye and hand’’ test.
C.-H. Cheng et al. / Research in Developmental Disabilities 35 (2014) 2172–2179
2175
a child does poorly on the most difficult task (e.g. double-off) because it was presented first, or that they only did well on the single-target task because of the practice that proceeded. The reaction time was defined as the time when the cue showed to that the correct key being pressed down. Three complete trials were recorded for each task. 2.2.3. Test 3: Motion coherence Dynamic random dot kinematogram was used to test subject’s global motion processing. The test consisted of identifying two kinds of patches: one is the target with a constant moving velocity and direction (8.78/s toward the left or right side of the screen), and the other is the interfering point moving in a Brownian manner. The threshold is defined as the ratio of number of the targets to that of the interfering points. The higher threshold the subject get, the poorer the sensitivity of the motion perception for the subject is. The test began with 100% threshold, i.e. all the patches moving in the same velocity and direction. If the subject correctly recognized the moving direction of the targets, the threshold would be decreased by 1 dB in the following repetition, otherwise increased by 3 dB. The whole procedure was repeated eight times. The thresholds of the last six times were averaged. Two rounds were executed, and the thresholds from two rounds were recorded. 2.2.4. Test–retest reliability To ensure the visual-perception tests used in current study are reliable, twenty typically developing children were recruited for the test–retest reliability, separated by a week interval. The results showed moderate to high reliability for all three tests (rtest1 = 0.461, ptest1 = 0.041; rtest2 = 0.704, ptest2 = 0.001; rtest3 = 0.858, ptest3 < 0.001). 2.3. Design and procedure A total of 250 children was identified and categorized into two groups (DCD and TD) via the MABC-2 test. After the grouping was done, an occupational therapist who was blind to the group membership of these children then individually administered the test 1 using standard procedures. For the computer tests (tests 2 and 3), the subjects were asked to sit 0.5 m in front of the monitor with eye level in the height of the center of the screen when taking the computerized tests. The height of the armrest was adjusted to a comfortable position, and both feet were on the level ground. Five practice trials were allowed. There were 3–5 min resting intervals among the tests. The data would be excluded when the subjects could not concentrate or complete the tests. 2.4. Data analysis The t-test was used to examine the differences between the children with DCD and TD for the MABC-2 test, visualperception test 1 and 3. Three-way ANOVA with repeated measures on groups (DCD/TD), conditions (single/double/double off), and sides (left/right) was used for the test 2. The Pearson correlation analysis was also applied to reveal the correlation between the MABC-2 and each of the visual-perceptual tests. The significance level was set at 0.05. 3. Results From a total of 250 children, seventeen DCD (7.25 0.28 years) and seventeen TD (7.09 0.34 years) were recruited. The ratio of males to females in the DCD group (12:5) was higher than that in the TD group (8:9). The age difference in two groups was not significant (p = 0.139). For the MABC-2 score, significant differences were found between the two groups (total: 54.9 10.5 and 84.2 6.9; MD: 19.1 6.7 and 32.9 5.1; A&C: 14.4 3.8 and 19.8 4.4; Bal: 21.5 4.9 and 31.4 3.7 for the DCD and TD group respectively, all p < 0.001). As for the DCD group, the total score was highly correlated with the score for MD (r = 0.746), moderately correlated with the score for A&C (r = 0.561), and moderately correlated with the score for Bal (r = 0.669). As for TD, the total score was only moderately correlated with the score for A&C (r = 0.557) and Bal (r = 0.639), respectively (Table 1).
Table 1 Pearson correlation (with p value in the parenthesis) between the component scores and total scores of the M-ABC 2 in children with DCD and in typically developing (TD) children. DCD
Total MD A&C Bal
TD
Total
MD
A&C
Bal
Total
MD
A&C
Bal
1 .746** (.001) .561* (.019) 669** (.003)
– 1 .072 (.785) .152 (.561)
– – 1 .308 (.229)
– – – 1
1 .398 (.114) .557* (.020) .639** (.006)
– 1 .383 (.129) .191 (.464)
– – 1 .373 (.140)
– – – 1
Total: the total score of M-ABC-2; MD: manual dexterity; A&C: aiming and catching; Bal: balance. ** p < .01. * p < .05.
C.-H. Cheng et al. / Research in Developmental Disabilities 35 (2014) 2172–2179
2176
Table 2 Pearson correlation (with p value in the parenthesis) between each subtest in test 1 (TVPS-R) and each component score of M-ABC-2 in children with DCD and in typically developing (TD) children. DCD
TD
DIS Total MD A&C Bal
CON
.329 (.184) .093 (.723) .638** (.006) .085 (.744)
SEQ
.044 .175 .152 .033
(.866) (.500) (.561) (.900)
FGR
.379 (.133) .651** (.005) .015 (.953) .092 (.726)
DIS
.167 .313 .123 .039
(.521) (.221) (.638) (.882)
CON
.000 .470 .345 .252
(.999) (.057) (.176) (.329)
SEQ
.101 .119 .623 .049
(.699) (.648) (.929) (.852)
.203 .305 .209 .200
FGR (.434) (.234) (.421) (.441)
.039 .008 .670 .150
(.881) (.977) (.784) (.566)
Total: the total score of M-ABC-2; MD: manual dexterity; A&C: aiming and catching; Bal: balance; DIS: visual discrimination; CON: form constancy; SEQ: sequential memory; FGR: figure ground. ** p < .01. Table 3 Descriptive and inferential statistics for each subtest in test 2 (sequential coupling of eye and hand) in children with DCD and in typically developing (TD) children. Left
DCD TD Side mean
Right
Group mean
SL
DL
OL
SR
DR
OR
0.57 (.28) 0.42 (.26)
0.70 (.47) 0.43 (.27) 0.51 (.30)§
0.57* (.30) 0.38 (.22)
0.74 (.33) 0.47 (.28)
0.74 (.47) 0.51 (.36) .61 (.37)
0.71* (.46) 0.48 (.30)
0.67*(.39) 0.45 (.28)
Mean (SD): in s. * Significant difference between the DCD and TD group. § Significant difference between the two sides.
3.1. Test 1 For group comparisons between the DCD and TD, significant differences were found in all the subtests including visual discrimination (8.9 3.3 and 11.5 3.8, p = 0.049), form consistency (9.1 3.3 and 11.6 3.6, p = 0.039), sequential memory (12.0 3.2 and 14.2 2.2, p = 0.048) and figure-ground (9.6 2.2 and 12.0 3.2, p = 0.009). Children with DCD scored lower than TD. Correlation tests for the group of DCD revealed a moderate correlation between the visual discrimination and the A&C (r = 0.638). A moderate correlation was also found between the visual sequential memory and the MD (r = 0.651). No other statistical significance was found between other measurements. All these measurements demonstrated no significant correlation in TD (Table 2). 3.2. Test 2 There were significant differences in the main effect of the group (p = 0.043) and side (p < 0.001). Significant differences were found between OL (p = 0.023)/OR (p = 0.048). No statistical significance was found in other subtests or interactions (Table 3). As to the correlation between each subtest and the measurements of MABC-2, the analyses revealed moderate correlation between SL/OR and the total score of MABC-2 (r = 0.554/ 0.486), and between DL/DR/OR and A&C score (r = 0.482/ 0.488/ 0.599). None of the subtests correlated significantly with the MABC-2 scores in TD (Table 4). 3.3. Test 3 The threshold of the motion coherence test was significantly greater in DCD (0.60 0.14) than in TD (0.47 0.14) (p < 0.016). Correlation tests revealed that the threshold was moderately correlated with the total score of MABC-2 (r = 0.670), MD (r = 0.489), and Bal (r = 0.554). No significant correlation was found in TD (Table 5).
Table 4 Pearson correlation (with p value in the parenthesis) between each subtest in test 2 (sequential coupling of eye and hand) and each component score of MABC-2 in children with DCD and in typically developing (TD) children. DCD SL Total MD A&C Bal
.554* (.021) .338 (.184) .459 (.064) .345 (.175)
TD DL .202 (.438) .123 (.637) .482* (.050) .204 (.433)
OL .329 .142 .373 .203
SR (.198) (.586) (.140) (.435)
.371 .131 .401 .286
DR (.142) (.617) (.111) (.266)
.117 (.654) .163 (.533) .488* (.047) .066 (.801)
OR .486* (.048) .242 (.350) .599* (.011) .212 (.414)
SL .243 .081 .340 .158
DL (.348) (.756) (.182) (.545)
.184 .026 .112 .169
OL (.480) (.921) (.668) (.518)
.358 .043 .490 .023
SR (.158) (.871) (.056) (.930)
.361 .056 .328 .201
DR (.154) (.832) (.199) (.440)
.168 .048 .185 .024
OR (.519) (.854) (.478) (.928)
.148 .000 .089 .166
(.571) (.999) (.734) (.525)
Total: the total score of M-ABC-2; MD: manual dexterity; A&C: aiming and catching; Bal: balance; SL: single left; SR: single right; DL: double left; DR: double right; OL: double-off left; OR: double-off right. * p < .05.
C.-H. Cheng et al. / Research in Developmental Disabilities 35 (2014) 2172–2179
2177
Table 5 Pearson correlation (with p value in the parenthesis) between the test 3 (motion coherence) and each component score of M-ABC-2 in children with DCD and in typically developing (TD) children. DCD Total MD A&C Bal
.670** (.003) .489* (.046) .275 (.286) .554* (.021)
TD .052 .172 .034 .175
(.844) (.509) (.897) (.501)
Total: the total score of M-ABC-2; MD: manual dexterity; A&C: aiming and catching; Bal: balance. ** p < .01. * p < .05.
4. Discussion This study was to examine the multiple aspects of the visual-perceptual abilities of the children with DCD, as well as their links to the motor deficits. The major findings were that children with DCD showed significantly poorer performance compared to TD on the visual-perceptual test. The visual discrimination, visual sequential memory, sequential coupling of eye and hand, and motion coherence demonstrated a moderate or strong correlation with the MABC-2. For everyday tasks and assessment batteries such as the MABC, a smooth transition between sequential movements is required (Wilmut et al., 2006). These indicated that the poor performance within DCD in the tasks like static visual discrimination, visual sequential memory and sequential coupling of eye and hand would inevitably lead to slowness in the completion of MABC-2 or everyday tasks. Unlike children with DCD, visual-perceptual abilities of the TD were not correlated with their motor performance as evaluated with MABC-2. Based on those results, the children with DCD could have problem in coordinating the visual signals to perform motor tasks, thus the visual-perceptual ability of the children with DCD should be carefully assessed when checking their motor functions. The sex ratio of male to female in the DCD group was around 2:1, which corresponds to the gender distribution of DCD population (Cermak & Larkin, 2002). Motor function assessments via the MABC-2, including the total score as well as the scores of its corresponding components, were all significantly different between the two groups. For the children with DCD, the total score of MABC-2 showed moderate to high correlation to its component scores, especially in the MD component compared to the TD group. Based on the user manual of MABC-2, the MD component measures the speed and accuracy of hand movement, bimanual coordination, and eye-hand coordination (Henderson & Sugden, 1992, 2007). These indicated that children with DCD demonstrated the soft neurological signs, suggesting the presence of cerebellar dysfunction (Cantin, Polatajko, Thach, & Jaglal, 2007). In test 1, the children with DCD showed significantly poorer accuracy of the visual-perceptual performance than the TD in all subtests. While comparing the test 1 to MABC-2, significant correlations were found between the visual discrimination and the A&C, and between the visual sequential-memory and the MD, in the children with DCD. No significant correlation among these variables was noted in the TD group (Table 2). The visual discrimination subtest is to find the correct design from a group of similar ones, which relies heavily on the process of the visual-perception codes. Previous study has shown that the children with DCD have difficulty in translating the signal from the visual-perception codes into the motor plan (Wilson & McKenzie, 1998). Aiming and catching, a dynamic task requiring the child to accurately perceive the trajectory and speed of an approaching object, is more susceptible to other factors such as motor planning of other effectors compared to a pure reaching to a static target (Lee, Poizner, Corcos, & Henriques, 2014). A poor performance on visual discrimination indicated more time is needed to discriminate and process the location of a moving object, therefore led to poorer performance on A&C. Thus the inferior ability of the A&C in the DCD group compared to the TD group in this study could attribute to the processing fault in the path from visual-perception to movement response. In regards to the visual sequential memory, it is the ability to examine a series of various designs and then identify that particular series from four others. Deficits in this ability reflect problems in signal processing, or in coping with complex signals and therefore causing motor clumsiness. As for test 2, children with DCD showed significantly longer reaction time than TD. There were also moderate correlations between most of the subtests and the total score of MABC-2. The findings indicated that the motor performance of children with DCD, especially during the A&C, was related to the sequential coupling process of eye and hand. In this study, the double-off condition, where two movements were made but both targets to which movements were generated disappeared prior to initiation of a hand movement, might lead to greater errors in children with DCD. In this condition, movements had to be completed purely on the basis of initial visual coding of target location rather than feedback information. Previous research indicated that, while executing simple or single-step goal-oriented visual motor tasks, the performance of children with DCD and was similar to that of TD. However during complex or multi-steps goal-oriented movements, children with DCD made more errors and took more time to focus on the target prior to the initiation of a hand movement (Wilmut et al., 2006). Regarding the motor control mechanism, these results indicated that children with DCD relied on feedback control to correct and coordinate their movements, which meant that they could not predict the upcoming event and plan their actions
2178
C.-H. Cheng et al. / Research in Developmental Disabilities 35 (2014) 2172–2179
in a feed-forward manner (Gheysen, Waelvelde, & Fias, 2011; Smits-Engelsman, Wilson, Westenberg, & Duysens, 2003; Wilmut & Wann, 2008; Wilson, Thamas, & Maruff, 2002). These facts led to a longer period in predicting signal directions and decision making and therefore poor aiming and catching ability. In regards to test 3, children with DCD demonstrated significantly higher threshold than TD, which meant that children with DCD were less sensitive to this dynamic random dot motion coherence test. The result was similar to those found by Sigmundsson et al. (2003). They found that the clumsy children, who were diagnosed solely on the basis of their motor difficulties, were significantly less sensitive than the control group on visual sensitivity tasks. Further correlation analyses found the average threshold in test 3 was moderately correlated with the total score of MABC-2, and the MD and the Bal component scores of MABC-2 in children with DCD. However such correlation was not found in TD group (Table 3). Test 3 measured global motion processing using a dynamic random dot kinematogram with embedded noise. Direct visual attention is therefore needed to justify the direction of those moving dots. According to Cherng et al., attention constitutes a mental resource that supports mental information processing of the mind (Cherng, Liang, Chen, & Chen, 2009). Various pools are involved in this mental resource, such as the stage of processing (perceptual, central or response), the codes of processing (verbal or spatial), and the modalities of input (visual or auditory) and response (manual or vocal). If two simultaneous tasks compete for the same pool of attention resource, they would interfere with each other and there will not be enough resource for both. The motor performance will be affected as a result. In addition, when a motor task is less automatic, it requires greater attention control and is more affected by a concurrently performed task (Tsai et al., 2008). Since children with DCD rely more on visual information during balance tasks, this explained why the coherence threshold is highly correlated with the Bal component in MABC-2. Limitations of the present study were that the comorbidities such as dyslexia or sensory processing disorders were not screened during subject recruitment. The exclusion criteria were any obvious deficits in attention such as having attention deficit hyperactivity disorder, experience in switching dominant hand, and visual deficits which cannot be corrected by surgical procedure or glasses. Since these co-existing disorders might also affect subject’s visual-perceptual function, it would be a plus if we consider the heterogeneous characteristics of children with DCD in future studies. 5. Conclusion In conclusion, this study showed that the motor problems screened by the tests of MABC-2 were significantly related to the visual-perceptual deficits of children with DCD. The correlation between the motor deficits and the visual-perceptual problems could be due to the fault of the input/output processing in the brain. MABC-2 is suggested to be a prescreening tool for verifying whether their motor deficits are linked to the visual-perceptual problems, therefore reducing the time needed for multiple clinical assessments. Findings could also be further used to develop integrated visual-motor examination tools or specific educational interventions for children with DCD. Conflict of interest The authors did not have any financial and personal relationship with other people or organization that could inappropriately influence this work. Acknowledgements The authors would like to thank for the participation of all children, parents, school teachers and staff in this study. This work was supported by the Ministry of Science and Technology (101-2221-E-182-020-MY3), and the Chang Gung Medical Research Program (CMRP), Taiwan (Grant no. CMRPD 1A0691 and 1A0692 ). References American Psychological Association (2013). Diagnostic and statistical manual of mental disorders: DSM-V. Washington, DC: American Psychological Association. Bonifacci, P. (2004). Children with low motor ability have lower visual-motor integration ability but unaffected perceptual skills. Human Movement Science, 23(2), 157–168. Cantin, N., Polatajko, H. J., Thach, W. T., & Jaglal, S. (2007). Developmental coordination disorder: Exploration of a cerebellar hypothesis. Human Movement Science, 26(3), 491–509. Cermak, S. A., & Larkin, D. (2002). Developmental coordination disorder. Canada: Thomson Learning. Cherng, R. J., Liang, L. Y., Chen, Y. J., & Chen, J. Y. (2009). The effects of a motor and a cognitive concurrent task on walking in children with developmental coordination disorder. Gait & Posture, 29(2), 204–207. Gardner, M. F. (1996). Test of visual perceptual skills (non-motor)-revised. Hydesville, CA: Psychological and Educatonal Publications -revised. Geuze, R. H., Jongmans, M. J., Schoemaker, M. M., & Smits-Engelsman, B. C. M. (2001). Clinical and research diagnostic criteria for developmental coordination disorder: A review and discussion. Human Movement Science, 20, 7–47. Gheysen, F., Waelvelde, H. V., & Fias, W. (2011). Impaired visuo-motor sequence learning in DCD. Research in Developmental Disabilities, 32, 749–756. Henderson, S. E., & Sugden, D. A. (1992). Movement assessment battery for children. London, UK: The Psychological Corporation. Henderson, S. E., & Sugden, D. A. (2007). Movement assessment battery for children (2nd ed.). London, UK: The Psychological Corporation. Hoare, D. (1994). Subtypes of developmental coordination disorder. Adapted Physical Activity Quarterly, 11(2), 158–169. Johnson, D. C., & Wade, M. G. (2009). Children at risk for developmental coordination disorder: Judgement of changes in action capabilities. Developmental Medicine and Child Neurology, 51(5), 397–403. Lee, D., Poizner, H., Corcos, D. M., & Henriques, D. Y. (2014). Unconstrained reaching modulates eye-hand coupling. Experimental Brain Research, 232(1), 211–223.
C.-H. Cheng et al. / Research in Developmental Disabilities 35 (2014) 2172–2179
2179
Macnab, J. J., Miller, L. T., & Polatajko, H. J. (2001). The search for subtypes of DCD: Is cluster analysis the answer? Human Movement Science, 20(1–2), 49–72. Merigan, W. H., & Maunsell, J. H. R. (1993). How parallel are the primate visual pathways? Annual Review of Neuroscience, 16, 369–402. Niemeijer, A. S., Smits-Engelsman, B. C. M., & Schoemaker, M. M. (2007). Neuromotor task training for children with developmental coordination disorder: A controlled trial. Developmental Medicine and Child Neurology, 49(6), 406–411. Piek, J. P., & Dyck, M. J. (2004). Sensory-motor deficits in children with developmental coordination disorder, attention deficit hyperactivity disorder and autistic disorder. Human Movement Science, 23(3–4), 475–488. Schoemaker, M. M., Wees, M., Flapper, v. d. B., Verheij-Jansen, N., Scholten-Jaegers, S., & Geuze, R. H. (2001). Perception skill of children with developmental coordination disorder. Human Movement Science, 20, 111–133. Sigmundsson, H., Hansen, P. C., & Talcott, J. B. (2003). Do ‘clumsy’ children have visual deficits. Behavioural Brain Research, 139(1–2), 123–129. Smits-Engelsman, B. C. M., Wilson, P. H., Westenberg, Y., & Duysens, J. (2003). Fine motor deficiencies in children with developmental coordination disorder and learning disabilities: An underlying open-loop control deficit. Human Movement Science, 22, 459–513. Tsai, C. L., Wilson, P. H., & Wu, S. K. (2008). Role of visual-perceptual skills (non-motor) in children with developmental coordination disorder. Human Movement Science, 27(4), 649–664. Van Waelvelde, H., De Weerdt, W., De Cock, P., & Smits-Engelsman, B. C. M. (2004). Aspects of the validity of the Movement Assessment Battery for Children. Human Movement Science, 23(1), 49–60. Venetsanou, F., Kambas, A., Ellinoudis, T., Fatouros, I., Giannakidou, D., & Kourtessis, T. (2011). Can the Movement Assessment Battery for Children-Test be the ‘‘gold standard’’ for the motor assessment of children with Developmental Coordination Disorder? Research in Developmental Disabilities, 32(1), 1–10. Wilmut, K., & Wann, J. (2008). The use of predictive information is impaired in the actions of children and young adults with Developmental Coordination Disorder. Experimental Brain Research, 191, 403–418. Wilmut, K., Wann, J. P., & Brown, J. H. (2006). Problems in the coupling of eye and hand in the sequential movements of children with Developmental Coordination Disorder. Child: Care, Health and Development, 32(6), 665–678. Wilson, P. H., & McKenzie, B. E. (1998). Information processing deficits associated with developmental coordination disorder: A meta-analysis of research findings. Journal of Child Psychology and Psychiatry, 39(6), 829–840. Wilson, P. H., Thamas, P. R., & Maruff, P. (2002). Motor imagery training ameliorates motor clumsiness in children. Journal of Child Neurology, 17(7), 491–498. Zwicker, J. G., Missiuna, C., Harris, S. R., & Boyd, L. A. (2012). Developmental coordination disorder: A review and update. European Journal of Paediatric Neurology, 16(6), 573–581.