Profiles of visual perceptual functions in Down syndrome

Research in Developmental Disabilities 37 (2015) 112–118

Contents lists available at ScienceDirect

Research in Developmental Disabilities

Profiles of visual perceptual functions in Down syndrome Yi-Ting Wan a, Ching-Sui Chiang a, Sharon Chia-Ju Chen b, Chih-Chung Wang c, Yee-Pay Wuang a,c,* a

Department of Occupational Therapy, Kaohsiung Medical University, Kaohsiung, Taiwan Department of Medical Imaging and Radiological Sciences, Kaohsiung Medical University, Kaohsiung, Taiwan c Department of Rehabilitation Medicine, Kaohsiung Medical University Chung-Ho Memorial Hospital, Kaohsiung, Taiwan b

A R T I C L E I N F O

A B S T R A C T

Article history: Received 26 September 2014 Accepted 11 November 2014 Available online

The primary purpose of this study was to investigate the visual perceptual functions measured by the Test of Visual Perceptual Skill-Third Edition (TVPS-3) in Down syndrome (DS). Seventy individuals with DS, seventy with typical development (TD), and forty mental-age-matched participants with intellectual disabilities (ID) were recruited for the assessment session. Significant between-group differences in TVPS-3 were observed between either DS or ID and TD groups. There was no significant difference on TVPS-3 between DS and ID groups. Implications for clinical professionals and recommendations for further research are discussed. ß 2014 Published by Elsevier Ltd.

Keywords: Down syndrome Visual perception

1. Introduction Down syndrome (DS) is the most common genetic cause of intellectual disabilities (ID) (Picker & Walsh, 2013), with prevalence of 1 in 737 live births (Parker et al., 2010). Most previous studies have stressed that the neuropsychological profile of DS is mainly characterized by a remarkable deficit in language abilities solely (Abbeduto, Warren, & Connors, 2007; Chapman, 1997). Much of the research that established visuo-spatial ability as a relative strength in DS however, contrasted it with verbal and other cognitive abilities (Klein & Mervis, 1999; Wang & Bellugi, 1994; Wang, Doherty, Rourke, & Bellugi, 1995). Therefore, visual perceptual functions are rarely discussed or even treated in DS compared to other groups of ID such as Williams syndrome (WS) or fragile X syndrome (FXS). Recent studies from different labs have demonstrated more complex neuropsychological features in DS, with deficits in visual perceptual functions as well (Vicari, 2006). The study results showed that DS have deficits in the following visual perceptual functions: mental rotation (Hinnell & Virji-Babul, 2004; Uecker, Obrzut, & Nadel, 1994), visual organization (Wuang & Su, 2011), figure ground and visual imaginary (Vicari, Bellucci, & Carlesimo, 2006), and visuospatial working memory (Carretti, Lanfranchi, & Mammarella, 2013; Lanfranchi, Carretti, Spano`, & Cornoldi, 2009). In addition, on the tasks requiring organization of the visual stimuli from part to whole, like house drawing, block designing and local-to-global tasks; DS tend to exhibit a global organization while ignoring internal details (Bellugi, Lichtenberger, Mills, Galaburda, & Korenberg, 1999). Since visual perceptual functions are less understood in DS, utilization of appropriate assessment tools to evaluate their performance on visual perceptual tasks is of importance. The most commonly used assessments of visual perception by

* Corresponding author at: Department of Occupational Therapy, 100 Shih-Chuan 1st Road, Kaohsiung 807, Taiwan. Tel.: +886 7 3121101x2658; fax: +886 7 3215845. E-mail address: [email protected] (Y.-P. Wuang). http://dx.doi.org/10.1016/j.ridd.2014.11.008 0891-4222/ß 2014 Published by Elsevier Ltd.

Y.-T. Wan et al. / Research in Developmental Disabilities 37 (2015) 112–118

113

occupational therapists are Development Test of Visual Perception, Second Edition (DTVP-2; Hammill, Pearson, & Voress, 1993), Motor-Free Visual Perception Test, Third Edition (MVPT-3; Colarusso & Hammill, 2003), and Test of Visual Perceptual Skill, Third Edition (TVPS-3; Martin & Gardner, 2006). The above tests all have good psychometric properties; the TVPS-3 was chosen in the present study because it has been designed to analyze comprehensive visual perceptual functions framed by seven over-arching dimensions. The test items are arranged according to difficulty (from the easiest to the most difficult), and it only requires verbal responses to the test items. It is particularly suitable for children with disabilities (i.e. DS in the present study) because of their poor motor abilities and low frustration tolerance levels. The study aimed to assess the visual perception of functions in DS by using the standardized visual perception test (TVPS3) and determine whether their visual perceptual functions were age-linked like typically-developing individuals.

2. Materials and methods 2.1. Participants Three groups participated in this study. Individuals with DS and ID were recruited from two public special schools, 2 non-profit agencies serving disabled citizens, and 3 hospitals in southern Taiwan. In these settings, individuals were selected for participation if they met the following criteria: they (1) were aged between 6 and 20 years; (2) had a diagnosis of DS defined by board-certified physicians with a full-scale IQ of 55–70 on Wechsler Intelligence Scale for Children, Fourth Edition (WISC-IV) (Wechsler, 2003) or Wechsler Adult Intelligence Scale, Third Edition (WAIS-III) (Wechsler, 1997); (3) did not receive any visual perceptual training program in the preceding year; (4) were without serious emotional or behavioral disturbances; and (5) were right-handed. Excluded were those carrying coexisting autism, cerebral palsy, blindness and deafness in an attempt to minimize confounding of data. Also excluded were individuals with known etiologies of ID (e.g., WS, FXS, etc.) or previous history of neurological disorders such as traumatic brain injury, muscular dystrophies, and epilepsy. The TD group was recruited by contacting school nurses at 11 mainstream schools. Participants were excluded if screening of school medical records revealed any history of diagnosis of developmental, intellectual, psychiatric, or physical disabilities. The TD and DS groups were matched for chronological age, and ID and DS group was matched for IQ (mental age). The three groups were matched for gender and socioeconomic status as well. 2.2. Measures In the present study, TVPS-3 (Martin & Gardner, 2006) was used to assess the visual perceptual functions in DS. The TVPS3 assesses visual perception for individuals aged 4 years to 18 years 11 months in seven comprehensive subtests: visual discrimination, visual memory, visual spatial relationship, visual form constancy, visual sequential memory, visual figureground, and visual closure. The established norm of age 18 years could also be applied while assessing the visual perception functions of older adults (Brown, Mullins, & Stagnitti, 2008). TVPS-3 is an individually administered test, and it takes approximately 30–40 minutes to complete. All seven subtests include 2 trial items and 16 formal items, which are presented in multiple-choice formats. The raw score of seven subtests and total score can be converted to scale score and percentile rank. The average age-adjusted scale score for subtests are 10 (SD = 3) and average age-adjusted standard score for total scores is 100 (SD = 15). The test–retest reliability is .97 (Martin & Gardner, 2006). The TVPS-3 correlated fairly well with other measures of visual perception such as MVPT-3 and the Developmental Test of Visual Perception, Adolescent and Adult (Reynolds, Pearson, & Voress, 2002); the correlation coefficient ranged from 0.39 to 0.51 (Brown, Mullins, & Stagnitti, 2009). 2.3. Procedure This study was conducted during 2010–2014. Informed consent was obtained from the participant and his/her parent or guardian using assent (for the adolescents) and consent (for parent/guardian) forms approved by the Institutional Review Board of Kaohsiung Medical University Hospital. All the assessments were conducted on an individual basis in a specially designated space in the respective schools or facilities by experienced occupational therapists. After consent had been granted, the therapist used TVPS-3 to assess the visual perceptual functions of 70 TD, 70 DS, and 40 ID. 2.4. Data analysis The raw scores of seven subtests and total score of the TVPS-3 was used for further data analysis by SPSS 18.0. 2.4.1. Inter-groups analysis Analysis of variance (ANOVA) was applied to investigate the difference on visual perceptual functions among DS, ID, and TD groups.

114

Y.-T. Wan et al. / Research in Developmental Disabilities 37 (2015) 112–118

2.4.2. Correlational studies To examine whether the visual perceptual function was age-linked, Pearson correlation was used to investigate the relations between age and total/subtests scores in all 70 TD, 70 DS, and 40 ID participants. Correlation coefficients (r) of 0.1, 0.3, and 0.5 were considered as small, medium, and large while interpreting the strength of correlation (Cohen, 1988). 3. Results 3.1. Demographic data In the final sample of DS (n = 70), 42.9% (n = 30) were female and the average age was 11.3 years (range = 6.54–20.75, SD = 3.58). The TD group included 70 participants (26 females) with a mean age of 11.2 years (range = 6.63–20.56, SD = 3.34 years), and the ID group consisted of 40 participants (17 females) with a mean age of 9.4 years (range = 6–15, SD = 2.18 years). All participants were right-hand dominant. Sample demographics and their performance on TVPS-3 are presented in Table 1. The averaged TVPS-3 score was 45 (SD = 23.75) for DS group, 44.95 for the ID group (SD = 23.45) and 96.1 (SD = 6.68) for the TD group. 3.2. Visual perceptual functions in DS Using ANOVA, a significant difference (F = 155.65, p = 0.000) was identified in the TVPS-3 mean score for participants among DS, TD, and ID groups. Dunnett’s T3 was adopted for post-hoc analysis. The TD group outperformed the DS group in all seven TVPS-3 subtests and total scores, and there was no difference on these scores between DS and ID groups (Table 2). 3.3. Correlational studies Correlations between age and the visual perceptual functions measured by TVPS-3 were analyzed by computing Pearson correlation coefficient (r). As shown in Table 3, total score and seven subtests of TVPS-3 were significantly correlated with age in the three groups. 4. Discussion The current study characterized the visual perceptual functions of children and adolescents with DS. This study also examined the relationships between age and all dimensions of visual perception in the DS group. 4.1. Visual perceptual functions in DS DS has been considered as associated with extreme difficulty in verbal skills and relatively better visual spatial skills. Nevertheless, most studies that identified visual perceptual abilities as a strength in DS compared it to etiologies with known spatial impairments (e.g., WS) (Brown et al., 2003a; Fayasse & Thibaut, 2002; Vicari, Bellucci, & Carlesimo, 2005). In addition, the visual perceptual functions explored or discussed in the above comparative studies were limited to visuo-spatial ability and visual memory. To reduce the drawback of using the TD group as a comparison group only (Yang, Conners, & Merrill, 2014), this study also recruited another control group (ID) at similar general cognitive level (IQ) with the DS group. In our study, DS had deficits in general and specific visual perceptual functions suggested by their performance on TVPS-3 compared to the TD group. Even contrasted with ID group at the similar cognitive level, visual perceptual abilities seem not to be the relative strength of the cognitive phenotypes in DS as commonly stated (Chapman & Hesketh, 2000; Silverman, 2007). The correlation study revealed that the DS group would develop better visual perceptual functions with increasing age; however, they might have atypical developmental patterns or a longer developmental course contrasting with the TD group (Vicari, 2006; Wuang & Su, 2011). Table 1 Sample demographics. TD group (n = 70)

ID group (n = 40)

DS group (n = 70)

Sex Males Females

44(62.9%) 26(37.1%)

23(57.5%) 17(42.5%)

40(57.1%) 30(42.9%)

Age (years) M  SD Range

11.20  3.34 6.63–20.56

9.35  2.18 6.00–15.00

11.34  3.58 6.54–20.75

TVPS-3 Total raw score (M  SD)

96.10  6.68

44.95  23.45

45.00  23.75

Y.-T. Wan et al. / Research in Developmental Disabilities 37 (2015) 112–118

115

Table 2 Group comparisons on TVPS-3 scores. Subtest

DIS MEM SPA CON SEQ FGR CLO TRC

TD group

ID group

DS group

Mean

SD

Mean

SD

Mean

SD

13.76 13.66 13.71 13.59 13.67 13.99 13.69 96.06

1.26 1.19 1.33 1.19 1.50 1.45 1.43 6.68

7.28 7.00 7.00 4.90 7.05 5.43 6.30 44.95

2.97 3.36 3.76 3.61 3.92 3.55 4.31 23.45

7.49 7.04 7.29 5.14 6.76 5.54 5.74 45.00

3.23 3.49 4.10 3.68 4.20 3.53 4.58 23.75

F

Dunnett post hoc test

130.22* 120.71* 88.35* 178.87* 88.97* 182.23* 98.37* 155.65*

TD > ID, TD > ID, TD > ID, TD > ID, TD > ID, TD > ID, TD > ID, TD > ID,

TD > DS TD > DS TD > DS TD > DS TD > DS TD > DS TD > DS TD > DS

DIS = visual discrimination, MEM = visual memory, SPA = spatial relationships, CON = form constancy, SEQ = sequential memory, FGR = figure ground, CLO = visual closure, TRC = total raw score. * p < .001.

4.1.1. Visual discrimination Individuals with poor discrimination abilities may demonstrate impaired ability to recognize, match, and categorize (Schneck, 2010). While performing the visual discrimination tasks of TVPS-3, DS demonstrated difficulty matching the same shape presented in a different spatial orientation, confused similar shapes, or recognizing form in a complex field. Our study results were in line with other studies (Nandakumar & Leat, 2010). Besides, DS showed significant bias in attention toward global forms (Porter & Coltheart, 2006). Thus, DS with poor visual discrimination tended to exhibit correct overall gestalt but make many mistakes on the internal details while performing a visuo-spatial construction task such as drawing a house (Bellugi et al., 1999). 4.1.2. Visual memory (memory of object) and visual sequential memory (memory of locations) Visual memory involves the integration of visual information with previous experiences, and it can be categorized into either short-term and long-term visual memory or object and spatial visual memory. Long-term memory has expansive capacity while short-term memory can hold a limited number of unrelated bits of information for about 30 seconds (Schneck, 2010). Two distinct systems are responsible for the visual perception: the dorsal stream is involved in processing spatial localization while the ventral stream is related to object perception (Kravitz, Saleem, Baker, & Mishkin, 2011; Kravitz, Saleem, Baker, Ungerleider, & Mishkin, 2013; Mishkin, Ungerleider, & Macko, 1983; Ungerleider & Haxby, 1994). The visual memory subtest of TVPS-3 requires the child to remember for immediate recalling (after 5 seconds) all the characteristics of a given form and to recognize this form from an array of similar forms (Hollingworth, 2004). Our results demonstrated that DS have impairments in visual memory subtest of TVPS-3 compared to TD group. In terms of visual short-term memory, DS have difficulty in carrying out the following visual-object memory tasks: (1) visual short-term memory for one complex design: remember one complex design at a short time and subsequently find the same design; and (2) visual short-term memory for object span task: view several figures one at a short limited time, and then point out the order that they appeared (Menghini, Costanzo, & Vicari, 2011). DS performed worse than TD and Williams syndrome participants on the visual short-term memory test (Vicari et al., 2006). Regarding the visual long-term memory, DS showed difficulties in pattern recognition memory task where they need to remember a series of abstract patterns in a short time and then choose the same series of figures among different choices (Pennington, Moon, Edgin, Stedron, & Nadel, 2003; Visu-Perta, Benga, Tincas, & Miclea, 2007). DS also had much poorer performance than the normative data (Z = 1.25) on similar visual object long-term memory test (Menghini et al., 2011). Besides, a dissociation between more preserved visual spatial memory and greater impairment of visual-object learning ability was observed in a previous study. Individuals with Table 3 Correlations between age and TVPS-3 performance in TD group, DS group and ID group. TVPS-3 subtests

TD (n = 70) r

p value

r

p value

r

p value

Visual discrimination Visual memory Spatial relationships Form constancy Sequential memory Figure ground Visual closure Total raw score

0.36** 0.38** 0.51** 0.36** 0.41** 0.52** 0.60** 0.64**

0.002 0.001 0.000 0.002 0.000 0.000 0.000 0.000

0.41** 0.36** 0.37** 0.29* 0.41** 0.37** 0.25* 0.39**

0.000 0.005 0.002 0.014 0.000 0.002 0.040 0.001

0.80** 0.61** 0.69** 0.63** 0.77** 0.72** 0.76** 0.77**

0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000

** Correlation is significant at the 0.01 level. * Correlation is significant at the 0.05 level.

DS (n = 70)

ID (n = 40)

116

Y.-T. Wan et al. / Research in Developmental Disabilities 37 (2015) 112–118

WS showed the opposite profile, i.e., typical learning of visual-objective patterns but impaired learning of visual-spatial sequences (Vicari et al., 2005). The sequential memory subtest of TVPS-3 aims to examine the memory for locations (Yang et al., 2014). Our study showed that DS also had below-averaged sequential memory, and the deficit became more prominent as the memory loading increased. The results are in accordance with another study showing that DS have deficits simultaneously in both spatial and object working memory (Vicari et al., 2006). In children with ID, DS performed worse than non-DS on bead memory test (Bower & Hayes, 1994), a short-term sequential memory test in Stanford–Binet Intelligence Scale, 4th edition (S-B IV) (Thorndike, Hagen, & Sattler, 1986). From the results of our study and other research adopting the spatial memory subtest from the Kaufman of Assessment Battery for Children (K-ABC) (Kaufman & Kaufman, 1983), DS have deficits in remembering the locations of the objects arranged in either a row-or-column form and matrix forms (Cornish, Munir, & Cross, 2001; Munir, Cornish, & Wilding, 2000). 4.1.3. Spatial relationship Spatial relationship refers to the ability to perceive the position of objects in relation to oneself and/or other objects (Martin & Gardner, 2006). Visuo-spatial ability has often been considered as a relative strength in DS before. DS in the present study performed the second highest in spatial relationship among seven TVPS-3 subtests as well; however, they had significantly poor spatial relationship compared to TD. DS have difficulties in detecting the minor changes of object orientation or spatial relationship between the constitutive elements of a certain design. Our results echoed previous studies that different domains of spatial abilities: visuo-spatial memory, visuo-spatial construction, mental rotation, and way finding were below their general cognitive ability (Yang et al., 2014). Deficits in spatial relationships will adversely affect academic learning, especially in the development of the lexical process, writing, and mathematics (Brown, Rodger, & Davis, 2003). 4.1.4. Form constancy Form constancy is defined as the ability to recognize forms and objects as the same in various environment, size, positions, and shapes (Tseng & Chow, 2000). In our results, DS had the worst performance on form constancy among the seven TVPS-3 subtests. In a previous study conducted by Nandakumar and Leat (2010), (14) DS aged 8–18 years performed lower in form constancy subtest of TVPS-R. Form constancy requires not only visual discrimination but also mental rotation ability. Mental rotation, a particular kind of visual-spatial skills, refers to the ability of an individual to change the orientation of the 2D or 3D figures in mind around some axis in three-dimensional space (Linn & Petersen, 1985; Zacks, 2008). Some of the previous research has shown that DS had compromised and delayed mental rotation skills (Hinnell & Virji-Babul, 2004; Uecker et al., 1994), while another study did not show the difference in mental rotation between DS and TD (Vicari et al., 2006). To investigate the mental rotation in DS and their associations with form constancy, more in-depth research using larger DS sample and different mental rotation test materials developmentally appropriate to DS is suggested (Yang et al., 2014). 4.1.5. Figure ground Figure ground recognition refers to the ability to differentiate between foreground or background objects and forms (Grossberg, 1997). DS had deficient figure ground recognition measure by DTVP (Menghini et al., 2011; Vicari, 2006), Map search task (Cornish et al., 2001), as well as figure ground subtest of TVPS-3 in the current study. DS with poor figure ground recognition have difficulty in separating essential data from distracting surrounding information that she/he would be unable to visually attend to what is important in daily living or school work. 4.1.6. Visual closure Visual closure refers to the ability to visualize a complete whole when given incomplete information or a partial picture (Read, 1988). It is a fundamental skill for fluency and speed in reading and spelling. This skill can also help children recognize inferences and predict outcomes. In some studies using the K-ABC Gestalt Closure subtest to examine the visual closure ability in DS, DS performed poorly than TD (Cornish, Munir, & Cross, 1999; Pueschel, Gallagher, Zartler, & Pezzullo, 1987) and Fragile-X syndrome on naming an object or scene picture in a partially complete inkblot drawing (Cornish et al., 1999; Hodapp et al., 1992). DS with poor visual closure may have difficulty completing a thought or making an accurate judgment from partial information. They may also confuse similar objects or words, especially words with close beginning or endings. Taken together, individuals with DS indeed have deficit in various aspects of visual perceptual functions other than language skills. Deficits in visual perceptual may adversely affect the academic performance and functional status of DS (Brown et al., 2011; Schneck, 2005, 2010). As a consequence, it is crucial for clinicians to adjust the directions and contents of the intervention protocols for DS with more emphasis on remediating visual perceptual dysfunctions. 5. Conclusions This is the first study that characterized overall visual perceptual functions in DS by utilizing psychometric-sound standardized assessment to date. The present study also used mental-age-matched controls (the ID group) rather than TD group only to verify the visual perceptual functions in DS; however, it might be preferable to use a comprehensive verbal

Y.-T. Wan et al. / Research in Developmental Disabilities 37 (2015) 112–118

117

ability measure to select the comparison group as suggested (Yang et al., 2014). Functional magnetic resonance imaging (fMRI) used to examine the neural correlates of visual perceptual causality will be adopted in our future studies. Funding No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the author(s) or upon any organization with which the author(s) is/are associated. Acknowledgments This study was supported by grants from the Ministry of Science and Technology (NSC-99-2314-B-037-033-MY3). We also express our great gratitude to the participants and their families. References Abbeduto, L., Warren, S. F., & Connors, F. A. (2007). Language development in Down syndrome: From the prelinguistic period to the acquisition of literacy. Mental Retardation and Developmental Disabilities Research Reviews, 13, 247–261. Bellugi, U., Lichtenberger, L., Mills, D., Galaburda, A., & Korenberg, J. R. (1999). Bridging cognition, the brain and molecular genetics: Evidence from Williams syndrome. Trends in Neurosciences, 22, 197–207. Bower, A., & Hayes, A. (1994). Short-term memory deficits and Down syndrome: A comparative study. Down Syndrome Research and Practice, 2, 47–50. Brown, T., Elliott, S., Bourne, R., Sutton, E., Wigg, S., Morgan, D., et al. (2011). The discriminative validity of three visual perception tests. New Zealand Journal of Occupational Therapy, 58, 14–22. Brown, J. H., Johnson, M. H., Paterson, S. J., Gilmore, R., Longhi, E., & Karmiloff-Smith, A. (2003). Spatial representation and attention in toddlers with Williams syndrome and Down syndrome. Neuropsychologia, 41, 1037–1046. Brown, T., Mullins, E., & Stagnitti, K. (2008). The reliability of performance of healthy adults on three visual perception tests. British Journal of Occupational Therapy, 71, 438–447. Brown, T., Mullins, E., & Stagnitti, K. (2009). The concurrent validity of three visual perception tests used with adults. Occupational Therapy in Healthcare, 23, 99–118. Brown, T., Rodger, S., & Davis, A. (2003). Test of visual perceptual skills–revised: An overview and critique. Scandinavian Journal of Occupational Therapy, 10, 3–15. Carretti, B., Lanfranchi, S., & Mammarella, I. C. (2013). Spatial-simultaneous and spatial-sequential working memory in individuals with Down syndrome: The effect of configuration. Research in Developmental Disabilities, 34, 669–675. Chapman, R. S. (1997). Language development in children and adolescents with Down syndrome. Mental Retardation and Developmental Disabilities Research Reviews, 3, 307–312. Chapman, R. S., & Hesketh, L. J. (2000). Behavioral phenotype of individuals with Down syndrome. Mental Retardation and Developmental Disabilities Research Reviews, 6, 84–95. Cohen, J. (1988). Statistical power analysis for behavioral science (2nd ed.). Hillsdale, NJ: Erlbaum. Colarusso, R. P., & Hammill, D. D. (2003). Motor-Free Visual Perception Test (3rd ed.). Novato, CA: Academic Therapy Publications. Cornish, K. M., Munir, F., & Cross, G. (1999). Spatial cognition in males with fragile-X syndrome: Evidence for a neuropsychological phenotype. Cortex, 35, 263–271. Cornish, K. M., Munir, F., & Cross, G. (2001). Differential impact of the FMR-1 full mutation on memory and attention functioning: A neuropsychological perspective. Journal of Cognitive Neuroscience, 13, 144–150. Fayasse, M., & Thibaut, J. P. (2002). Local and global processing by persons with Williams syndrome: The case of visuo-constructive tasks. Journal of Cognitive Education and Psychology, 2, 266–282. Grossberg, S. (1997). Cortical dynamics of three-dimensional figure–ground perception of two-dimensional pictures. Psychological Review, 104, 618–658. Hammill, D. D., Pearson, N. A., & Voress, J. K. (1993). Developmental Test of Visual Perception (2nd ed.). Austin, TX: Pro-Ed. Hinnell, C., & Virji-Babul, N. (2004). Mental rotation abilities in individuals with Down syndrome – A pilot study. Down Syndrome: Research and Practice, 9, 12–16. Hodapp, R. M., Leckman, J. F., Dykens, E. M., Sparrow, S. S., Zelinsky, D. G., & Ort, S. I. (1992). K-ABC profiles in children with Fragile X syndrome. Down syndrome and nonspecific mental retardation. American Journal on Mental Retardation, 97, 39–46. Hollingworth, A. (2004). Constructing visual representations of natural scenes: The roles of short-and long-term visual memory. Journal of Experimental Psychology: Human Perception and Performance, 30, 519–537. Kaufman, A. S., & Kaufman, N. L. (1983). Kaufman Assessment Battery for Children. Circle Pines, MN: American Guidance Service. Klein, B. P., & Mervis, C. B. (1999). Contrasting patterns of cognitive abilities of 9-and 10-year-olds with Williams syndrome or Down syndrome. Developmental Neuropsychology, 16, 177–196. Kravitz, D. J., Saleem, K. S., Baker, C. I., & Mishkin, M. (2011). A new neural framework for visuospatial processing. Nature Reviews Neuroscience, 12, 217–230. Kravitz, D. J., Saleem, K. S., Baker, C. I., Ungerleider, L. G., & Mishkin, M. (2013). The ventral visual pathway: An expanded neural framework for the processing of object quality. Trends in Cognitive Sciences, 17, 26–49. Lanfranchi, S., Carretti, B., Spano`, G., & Cornoldi, C. (2009). A specific deficit in visuospatial simultaneous working memory in Down syndrome. Journal of Intellectual Disability Research, 53, 474–483. Linn, M. C., & Petersen, A. C. (1985). Emergence and characterization of sex differences in spatial ability: A meta-analysis. Child Development, 56, 1479–1498. Martin, N., & Gardner, M. F. (2006). Test of Visual Perceptual Skills (3rd ed.). Novato, CA: Academic Therapy Publications. Menghini, D., Costanzo, F., & Vicari, S. (2011). Relationship between brain and cognitive processes in Down syndrome. Behavior Genetics, 41, 381–393. Mishkin, M., Ungerleider, L. G., & Macko, K. A. (1983). Object vision and spatial vision: Two cortical pathways. Trends in Neurosciences, 6, 414–417. Munir, F., Cornish, K. M., & Wilding, J. (2000). Nature of the working memory deficit in fragile-X syndrome. Brain and Cognition, 44, 387–401. Nandakumar, K., & Leat, S. J. (2010). Bifocals in children with Down syndrome (BiDS)–visual acuity, accommodation and early literacy skills. Acta Ophthalmologica, 88, e196–e204. Parker, S. E., Mai, C. T., Canfield, M. A., Rickard, R., Wang, Y., Meyer, R. E., et al. (2010). Updated national birth prevalence estimates for selected birth defects in the United States, 2004–2006. Birth Defects Research. Part A: Clinical and Molecular Teratology, 88, 1008–1016. Pennington, B. F., Moon, J., Edgin, J., Stedron, J., & Nadel, L. (2003). The neuropsychology of Down syndrome: Evidence for hippocampal dysfunction. Child Development, 74, 75–93. Picker, J. D., & Walsh, C. A. (2013). New innovations: Therapeutic opportunities for intellectual disabilities. Annals of Neurology, 74, 382–390. Porter, M. A., & Coltheart, M. (2006). Global and local processing in Williams syndrome, autism, and Down syndrome: Perception, attention, and construction. Developmental Neuropsychology, 30, 771–789. Pueschel, S. M., Gallagher, P. L., Zartler, A. S., & Pezzullo, J. C. (1987). Cognitive and learning processes in children with Down syndrome. Research in Developmental Disabilities, 8, 21–37. Read, D. E. (1988). Age-related changes in performance on a visual-closure task. Journal of Clinical and Experimental Neuropsychology, 10, 451–466. Reynolds, C. R., Pearson, N. A., & Voress, J. K. (2002). Developmental Test of Visual Perception - Adolescent and Adult, Austin, TX: Pro-Ed.

118

Y.-T. Wan et al. / Research in Developmental Disabilities 37 (2015) 112–118

Schneck, C. M. (2005). Visual perception. In J. Case-Smith (Ed.), Occupational therapy for children (5th ed., pp. 412–416). St. Louis Mosby. Schneck, C. M. (2010). Visual perception. In J. Case-Smith & J. C. O’Brien (Eds.), Occupational therapy for children (6th ed., pp. 373–403). Maryland Heights, MO: Mosby. Silverman, W. (2007). Down syndrome: Cognitive phenotype. Mental Retardation and Developmental Disabilities Research Reviews, 13, 228–236. Thorndike, R. L., Hagen, E. P., & Sattler, J. M. (1986). Stanford-Binet Intelligence Scale (4th ed.). Chicago: Riverside. Tseng, M. H., & Chow, S. M. (2000). Perceptual-motor function of school-age children with slow handwriting speed. American Journal of Occupational Therapy, 54, 83–88. Uecker, A., Obrzut, J. E., & Nadel, L. (1994). Mental rotation performance by learning disabled and Down’s syndrome children: A study of imaginal development. Developmental Neuropsychology, 10, 395–411. Ungerleider, L. G., & Haxby, J. V. (1994). ‘What’ and ‘where’ in the human brain. Current Opinion in Neurobiology, 4, 157–165. Vicari, S. (2006). Motor development and neuropsychological patterns in persons with Down syndrome. Behavior Genetics, 36, 355–364. Vicari, S., Bellucci, S., & Carlesimo, G. A. (2005). Visual and spatial long-term memory: Differential pattern of impairments in Williams and Down syndromes. Developmental Medicine & Child Neurology, 47, 305–311. Vicari, S., Bellucci, S., & Carlesimo, G. A. (2006). Evidence from two genetic syndromes for the independence of spatial and visual working memory. Developmental Medicine and Child Neurology, 48, 126–131. Visu-Perta, L., Benga, O., Tincas, I., & Miclea, M. (2007). Visual-spatial processing in children and adolescents with Down syndrome: A computerized assessment of memory skills. Journal of Intellectual Disability Research, 51, 942–952. Wang, P. P., & Bellugi, U. (1994). Evidence from two genetic syndromes for a dissociation between verbal and visual-spatial short-term memory. Journal of Clinical and Experimental Neuropsychology, 16, 317–322. Wang, P. P., Doherty, S., Rourke, S. B., & Bellugi, U. (1995). Unique profile of visuo-perceptual skills in a genetic syndrome. Brain and Cognition, 29, 54–65. Wechsler, D. (2003). Wechsler intelligence scale for children (4th ed.). San Antonio, TX: Psychological Corporation. Wechsler, D. (1997). Wechsler adult intelligence scale (3rd ed.). San Antonio, TX: Psychological Corporation. Wuang, Y. P., & Su, C. Y. (2011). Correlations of sensory processing and visual organization ability with participation in school-aged children with Down syndrome. Research in Developmental Disabilities, 32, 2398–2407. Yang, Y., Conners, F. A., & Merrill, E. C. (2014). Visuo-spatial ability in individuals with Downsyndrome: Is it really a strength? Research in Developmental Disabilities, 35, 1473–1500. Zacks, J. M. (2008). Neuroimaging studies of mental rotation: A meta-analysis and review. Journal of Cognitive Neuroscience, 20, 1–19.