Research in Developmental Disabilities 32 (2011) 1852–1859
Contents lists available at ScienceDirect
Research in Developmental Disabilities
The influence of manifest strabismus and stereoscopic vision on non-verbal abilities of visually impaired children Milica Gligorovic´ *, Vesna Vucˇinic´, Branka Esˇkirovic´, Branka Jablan University of Belgrade, Faculty of Special Education and Rehabilitation, Visokog Stevana 2, 11000 Belgrade, Serbia
A R T I C L E I N F O
A B S T R A C T
Article history: Received 9 March 2011 Received in revised form 17 March 2011 Accepted 17 March 2011 Available online 4 May 2011
This research was conducted in order to examine the influence of manifest strabismus and stereoscopic vision on non-verbal abilities of visually impaired children aged between 7 and 15. The sample included 55 visually impaired children from the 1st to the 6th grade of elementary schools for visually impaired children in Belgrade. RANDOT stereotest and polaroid glasses were used for the examination of stereoscopic vision, while Cover test and Hirschberg’s pupils reflex test were used for the evaluation of strabismus. In the area of non-verbal abilities was evaluated visual discrimination, visuomotor integration, constructive praxia, visual memory, strategy formation, nonverbal reasoning and the representational dimension of drawings. Subtests of ACADIA test of developmental abilities were used for the evaluation of non-verbal abilities (Atkinson et al., 1972). Statistically significant relations between strabismus and constructive praxia (p = 0.009), visual memory (p = 0.037), strategy formation (0.040) and the quality of drawings were determined by the results analysis. According to our findings, children with divergent strabismus achieve the best results. Children with stereoscopic vision generally achieve better results in all the examined areas of nonverbal abilities, and statistically significant relations were determined in the areas of visuomotor coordination (0.002), constructive praxia (0.026) and non-verbal reasoning (0.015), which are directly connected to visuospatial abilities. Children with convergent strabismus achieve significantly lower results in the areas of constructive praxia, visual memory, strategy formation and representational dimension of drawings, and children with the lack of stereoscopic vision – in the areas of visuomotor integration, constructive praxia and non-verbal reasoning. ß 2011 Elsevier Ltd. All rights reserved.
Keywords: Visual impairment Strabismus Stereoscopic vision Non-verbal abilities
1. Introduction Visual functioning and visual capacity do not relate only to the observation precision of the form, details, and colour of static or moving objects. They also include the success of processing and interpreting the received visual information. Actually, visual capacity is best expressed through visual efficacy, i.e. through the success in performing different visual tasks. Visual efficacy is very important for the development of integrative abilities and for the conceptualization of space and time (Atkinson, 2000). The ability to differentiate, as a prerequisite for establishing series and class systems, as foundations of logical thinking, is primarily based on visual perception. Children begin to create general categories very early, followed by subcategories, based upon the features of objects such as size, shape, colour etc. (Gligorovic´,
* Corresponding author. Tel.: +381 638832607; fax: +381 112183081. E-mail address:
[email protected] (M. Gligorovic´). 0891-4222/$ – see front matter ß 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.ridd.2011.03.018
M. Gligorovic´ et al. / Research in Developmental Disabilities 32 (2011) 1852–1859
1853
2010). The critical period of visual maturation, during which the quality of visual experience is shaped, is crucial for the later development (Hyva¨rinen, 1994; Wickham, Stewart, Charnock, & Fielder, 2002). Difficulties in the area of visual functions hinder the creation of mental representation of an object. These difficulties may influence the child’s ability to recognize and use letters, numbers, symbols, words or pictures, which impact academic skills, cognitive and adaptive abilities (Gligorovic´ & Radic´ Sˇestic´, 2010; Moguel-Ancheita, Ramı´rez-Sibaja, Reyes-Pantoja, & Orozco-Go´mez, 2010). A type or a model of visual functioning depends on a range of constellational, physiological and psychological parametres. These parameters need to be monitored for the purpose of diagnostics, differential diagnostics and treatment programming for visually impaired persons (Gligorovic´ & Vucˇinic´, 2010). Visual system consists of more subsystems, which to a great extent act independently and mainly perform different functions. They may develop or be impaired almost independently from each other. Thus, a person may demonstrate exceptional abilities in one of them, whereas in others, the abilities may be medium or bad. For example, children with the same vision acuity, whether from the stratum of emotropic or normal vision, often realize different levels of visual efficacy in the teaching process or in other situations. This is conditioned by other parameters of visual functioning characteristic for some eye diseases, the quality of vision field, the quality of binocular or stereoscopic vision and other parameters, as well as by the child’s cognitive and conative characteristics. The disorders of visual functions which most frequently affect learning are refraction anomalies, strabismus and amblyopia, system diseases of eyes and neuro-ophtalmological diseases (Koller, 1999). The assessment of factors, which often with other factors affect the developmental level and quality of cognitive abilities in children with low vision, should include various aspects of perceptive and integrative functions. Thus, we conducted this research with the aim of examining the influence of manifest strabismus and stereoscopic vision on non-verbal abilities of low vision children of elementary-school age. 2. Methods 2.1. Participants The sample consists of 55 low vision children aged between 7 and 15 (AS = 10.59, SD = 2.29), who attend schools for visually impaired children in Belgrade. There are 29 pupils from lower and 25 pupils from higher grades, 31 girls and 24 boys. Out of the total number of 98 children, low vision children who do not have any intellectual disabilities, autism, epilepsy or any additional sensory and/or motoric disorders were selected for the sample. The intellectual abilities of the participants range from slightly under average (16 participants) average (19 participants), to slightly above average (17 participants). According to vision acuity, the participants were divided into three categories: 0.05–0.1 category (15 participants), 0.1– 0.3 (26 participants) and above 0.3 category (13 participants). Manifest strabismus is present in 36 participants, i.e. esotropia in 18 participants, and exotropia in 12 participants. Stereoscopic vision is not present in 38 (69.1%). 2.2. Instruments and procedures 2.2.1. Assessment of visual function Manifest strabismus and stereoscopic vision were defined as independent variables. RANDOT-stereotest in the form of a booklet and polaroid glasses were used for examining stereoscopic vision. For the assessment of strabismus, we used Cover test for determining manifest and latent abnormal eye positions, and Hirschberg’s Pupil reflex test as the orientation and qualitative method for measuring the objective angle in convergent strabismus. 2.2.2. Assessment of non-verbal abilities In the area of non-verbal abilities, the following dependent variables were assessed: visual discrimination, visuomotor integration, constructive praxia, visual memory, strategy formation, non-verbal reasoning and representational dimension of drawings. For the assessment of non-verbal abilities, we used the subtests of Acadia Developmental Abilities Test (Atkinson et al., 1972), translated and adapted in Croatia in 1985 (Novosel et al., 1985), and additionally adapted and standardized in Serbia (Gligorovic´ et al., 2005). The Acadia test consists of 13 subtests out of which seven subtests were chosen for the assessment of non-verbal abilities. These subtests assess various skills and abilities necessary for successful mastering of academic skills in elementary school. The test can be applied individually or in groups. Since speed is not important in this test, it can be adapted to the pace of each child. Visuomotor integration was assessed by Subtest II of ACADIA test – Visuomotor Coordination and Sequencing. It consists of 10 tasks which test the ability to follow a marked path between different types of lines (concentric circle, square, triangle, etc.) and complete the shapes. A certain number of points is awarded for each task, counting mistakes, and the maximum number of points is 20. Visual discrimination was assessed by Subtest III of ACADIA test – Visual Discrimination. It consists of 20 tasks in which a child is expected to choose one out of four options based on a given model. The first part consists of drawings, while the second and the third part consist of words arranged from simple to more complex. One point is awarded for each correct answer.
1854
M. Gligorovic´ et al. / Research in Developmental Disabilities 32 (2011) 1852–1859
Constructive praxia was assessed by Subtest IV of ACADIA test – Shapes Drawing. It includes 20 models which a child has to copy. One point is awarded for each correct answer. Visual memory was assessed by Subtest V of ACADIA test – Visual Memory. After seeing the model, a child has to choose one of the given answers, or draw the appropriate shape. It consists of 10 tasks. Two points are awarded for each correctly completed task. Strategy formation was assessed by Subtest VII of ACADIA test – Sequence and Coding. It consists of 20 tasks. In the first part a child is expected to choose a geometric shape, a number or a word that continues the given sequence. In the second part a child has to discover and apply the principle of forming words by decoding numbers into letters. One point is awarded for each correct answer. Non-verbal reasoning was assessed by Subtest XII of ACADIA test – Visual Association. It consists of 10 tasks. In the first part of the test a child is expected to establish a functional relationship between the given model and one of the given options (e.g. ear and a receiver). In the second part a child has to reconstruct a whole from the given elements. Assessment depends on the complexity of tasks, and the maximum number of points is 20. Drawing quality (representational dimension of drawing) was assessed by Subtest XIII of ACADIA test – Drawing. Children were expected to draw a man standing under a tree, next to a house. Assessment depends on the accuracy of proportions, the number of details, and mutual relation between the set elements. The maximum number of points is 20. 2.3. Data analysis The relations significance between the independent non-parametric variables was determined using Wilcoxon’s rank significance test and Spearman’s coefficient of rank correlations. One-way variance analysis (ANOVA) and Scheffe Post hoc Test were used to determine the significance of the relations between the independent and parametrically dependent variables. 3. Results 3.1. General results The results analysis of non-verbal abilities assessment indicates that visually impaired children achieve results which are significantly below age standards on most subtests. This is particularly the case in the areas of visuomotor coordination (p < 0.005), visual discrimination (p = 0.001), constructive praxia (p = 0.001), visual memory (p < 0.000) and drawing quality (p < 0.000). No significant differences were determined on the subtests assessing complex abilities of strategy formation (p = 0.249) and non-verbal reasoning (p = 0.393). Age is a significant factor for visuomotor coordination (p = 0.031) and for constructive praxia (p = 0.031). In the area of visual discrimination the results are on the verge of being statistically significant (p = 0.052). It was determined that IQ is a significant factor for success in the areas of constructive praxia (p = 0.001), strategy formation (0.009), non-verbal reasoning (p = 0.010) and drawing quality (p = 0.003). Vision acuity proved to be a significant parameter of success in the areas of visuomotor coordination (p = 0.027) and visual memory (p = 0.016). Statistically significant relations between non-verbal abilities and gender were not determined. There are no statistically significant relations between manifest strabismus and IQ (p = 0.793), or between stereoscopic vision and IQ (p = 0.111). Statistically significant relations were also not determined between manifest strabismus and vision acuity (p = 0.121), and between strabismus and stereoscopic vision (p = 0.683). Statistically significant relations were determined between stereoscopic vision and vision acuity (p = 0.024). 3.2. Strabismus and non-verbal abilities Variance analysis indicated statistically significant relations between strabismus and dependent variables of non-verbal abilities: drawing shapes (p = 0.009), visual memory (p = 0.037), sequence and coding (0.040) and drawing (p = 0.034) (More details in Table 1). Post Hoc analysis of arithmetic means indicated that the children with convergent strabismus significantly differ from the children with divergent strabismus, but not from the children who do not have strabismus, in the areas of drawing shapes (Scheffe = 5.642, p = 0.013), sequence and coding (Scheffe = 3.456, p = 0.041) and drawing (Scheffe = 3.681, p = 0.035). The greatest variability of achievements is noticed in children with convergent strabismus. Although the children who do not have strabismus achieve better results than the children with convergent strabismus, the difference is not statistically significant. According to our findings, children with divergent strabismus achieve the best results. 3.3. Stereoscopic vision and non-verbal abilities Stereoscopic vision appears around the third month of a child’s life and develops very quickly until the sixth month, when it slows down to reach the adult level of development around the age of five or six (Hong & Park, 2008). Children with stereoscopic vision generally achieve better results in all examined areas of non-verbal abilities (more details in Table 2). Statistically significant relations were determined in the areas of visuomotor coordination (0.002), constructive
M. Gligorovic´ et al. / Research in Developmental Disabilities 32 (2011) 1852–1859
1855
Table 1 Manifest strabismus and non-verbal abilities of low vision children.
MS Mean
SD
Subtest
VD
VMI
CP
VM
SF
NR
D
None es ex None es ex
17.32 15.24 18.17 2.780 5.483 3.407 2.268 0.114
9.24 6.82 9.75 4.772 4.362 4.003 1.980 0.149
12.44 8.94 14.58 4.934 5.226 4.010 5.154 0.009
14.92 12.06 15.83 3.387 5.771 2.480 3.536 0.037
15.00 13.29 16.75 3.317 4.511 1.960 3.432 0.040
15.96 14.88 16.33 3.259 3.672 2.774 0.820 0.446
12.44 11.24 14.92 3.343 4.697 2.314 3.625 0.034
F (2,55) Sig.
MS: manifest strabismus; VD: visual discrimination; VMI: visuomotor integration; CP: constructive praxia; VM: visual memory; SF: strategy formation; NR: non-verbal reasoning; D: drawing; es: esotropia, ex: exotropia. Statistically significant results at 0.05 level is marked (bold).
Table 2 Stereoscopic vision and non-verbal abilities of low vision children.
SV
Mean SD F (1,55) Sig.
subtest
VD
VMI
CP
VM
SF
NR
D
None Yes None Yes
16.16 18.47 4.511 1.885 3.642 0.062
7.29 11.33 4.197 3.848 10.440 0.002
10.68 14.13 5.057 4.612 5.245 0.026
13.82 15.00 4.718 3.211 0.749 0.391
14.21 16.20 3.981 2.242 3.306 0.075
14.95 17.33 2.894 3.619 6.331 0.015
12.03 14.07 4.188 2.434 3.120 0.083
SV: stereoscopic vision; VD: visual discrimination; VMI: visuomotor integration; CP: constructive praxia; VM: visual memory; SF: strategy formation; NR: non-verbal reasoning; D: drawing. Statistically significant results at 0.05 level is marked (bold).
praxia (0.026) and non-verbal reasoning (0.015), which are directly connected to visuospatial abilities. In the areas of visual discrimination, strategy formation and drawing, the differences between children with and without stereoscopic vision are on the verge of being statistically significant. This indicates the significance of this segment of visual perception for the development of more complex cognitive abilities. It should also be emphasized that the achievements variability in all the tasks is greater in children without stereoscopic vision. 4. Discussion Our study was conducted with the aim of determining the impact of manifest strabismus and stereoscopic vision on non-verbal abilities of low vision children. The results generally point out convergent strabismus and the lack of stereoscopic vision as significant factors of low achievements in most assessed areas. In our research, the children with divergent strabismus achieve better results on all non-verbal abilities subtests than the children with convergent strabismus and the children without strabismus. They are also statistically more successful in the areas of constructive praxia, visual memory, strategy formation and representational dimension of drawings. Bearing in mind that statistically significant relations between manifest strabismus and vision acuity or IQ were not determined, the question of the reason for this advantage arises. Children with strabismus, once they are about 5 years old, like other children use the same vision strategies for sacadic movements of the eyes as adults. In children with strabismus, both eyes follow this strategy, but only one of them is fixed to the object (Kapoula & Bucci, 2002). It is possible that moving an eye to the inside narrows down the possibility of exploring the vision field and the choice of potential fixation points, more than moving it to the outside, which influences the quality of visual perception, and consequently also the quality of the assessed abilities in children with convergent strabismus. It is also possible that exploring and fixation strategies of children with divergent strabismus require more precise focusing, which positively influences the quality of visual attention and other non-verbal abilities. This presumption is strengthened by statistically significant differences in the areas of constructive abilities, visual memory, visuomotoric integration and strategy formation, for which visual attention is of esential importance. The idea that children with strabismus apply more energy to the maintaining of motor components of their vision, and thus have far less time for cognitive processing (Hyva¨rinen, 1988), can to some extent explain the difficulties of children with convergent strabismus. However, this is not in accordance with our findings as far as divergent strabismus is concerned. The examination of cognitive/perceptive style in persons with strabismus indicated the existence of significant differences only among male participants. This is explained by gender specific hemispheric specialization. The participants with convergent strabismus used analytical and differentiated style of information processing more than the participants with divergent strabismus (Birnbaum, 1981). This is also not corroborated, bearing in mind the nature of the tasks applied in our research. Also, we did not determine significant differences in IQ between the children with esotropia and those with exotropia (p = 0.469). It is of course also possible
1856
M. Gligorovic´ et al. / Research in Developmental Disabilities 32 (2011) 1852–1859
that the quality of tactile-kinesthetic and auditive perception, which we did not examine in this research, plays a role in such distribution of the results. In some studies, the significance of touch is emphasized for carrying out specific tasks, in which persons with visual impairments achieve the same or better results than their peers of typical population (Noordzij, Zuidhoek, & Postma, 2007). Nevertheless, a more detailed analysis is necessary to explain significantly lower results of children with convergent, as well as significantly better results of children with divergent strabismus. Depth perception, i.e. three-dimensionality, implies a combination of more types of depth cues, grouped in monocular and binocular categories. Consequently, the relation between stereoscopic vision and the assessed areas of non-verbal abilities is quite expected in low vision children. Visual impairments such as optic nerve hypoplasia, strabismus and amblyopia, may significantly influence the quality of depth perception and thus also the quality of mental representation of objects, visuomotor integration and visuospatial abilities. Our results confirm the significance of stereoscopic vision for the mentioned abilities, assessed by means of visuomotor coordination tasks, drawing shapes and non-verbal reasoning. In other words, by the assessment of Drawing and Drawing Shapes subtests, the priority is given to spatial reconstruction and the construction of given elements, regardless of the quality of their motor performance. Furthermore, a clear mental representation is necessary for visual association, i.e. the functional connection of objects. Binocular (stereoscopic) vision is more significant than monocular for the improvement of precise catching (Suttle et al., in press). Thus, its significant connectivity with visuomotor coordination is quite understandable. The results in the area of visuomotor coordination could also be explained by cumulative effect of the lack of stereoscopic vision and of vision acuity. Strabismic amblyopia drastically influences the development of higher levels of visual functions (Barnes, Hess, Dumoulin, Achtman, & Pike, 2001; Mendola et al., 2005; Sharma, Levi, & Klein, 2000). With regard to this our next step will be examining the effect of different types of protection mechanisms (suppression, anomal retinal correspondence and amblyopia) in children with convergent and divergent strabismus. In a future research, it would also be necessary to create groups of children with strabismus, with and without low vision, as well as groups of low vision children and children without visual impairments who do not have strabismus. This might provide a broader insight into the way in which strabismus, isolated or in interaction with other factors, influences nonverbal abilities.
5. Conclusion According to the obtained results, low vision children achieve results which are significantly below age standards on most subtests, particularly in the areas of visuomotor coordination, visual discrimination, constructive praxia, visual memory and drawing quality. Statistically significant differences on subtests assessing complex abilities of strategy formation and nonverbal reasoning were not determined. The results of examining the influence of manifest strabismus and stereoscopic vision on non-verbal abilities of low vision children indicate that convergent strabismus and the lack of stereoscopic vision influence the majority of the assessed non-verbal abilities. Children with convergent strabismus achieve significantly lower results in the areas of constructive praxia, visual memory, strategy formation and representational dimension of drawings. Children with the lack of stereoscopic vision achieve significantly lower results in the areas of visuomotor integration, constructive praxia and non-verbal reasoning. Constructive praxia, assessed by means of copying the models of growing complexity, is the only assessed ability influenced both by convergent strabismus and the lack of stereoscopic vision, which confirms its multifactorial causality and complexity. Our participants, including the yungest ones, have outgrown the age in which adequate intervention could fully eliminate the consequences of convergent strabismus and of the absence of stereoscopic vision on the development of higher functions. Although early intervention is undoubtedly the most efficient method in special education and rehabilitation, when not timely applied for different subjective and/or objective resons, it is necessary to design a clear methodological framework of tertiary prevention programmes. We should bear in mind that cognitive abilities, particularly mathematical and linguistic ones, are significant employment predictors of visually impaired persons (McDonnall, 2010). Cognitive abilities in these persons are more closely related to daily living skills than in sighted persons during mature and old age (Heyl & Wahl, 2010). Thus, continued rehabilitation is necessary.
M. Gligorovic´ et al. / Research in Developmental Disabilities 32 (2011) 1852–1859
Appendix A Tasks examples (smaller version).
1857
1858
M. Gligorovic´ et al. / Research in Developmental Disabilities 32 (2011) 1852–1859
References Atkinson, J. S., Johnston, E. E., & Lindsay, A. (1972). Acadia test of developmental abilities. Wolfville, Nova Scotia, Canada: University of Acadia. Atkinson, J. (2000). The developing visual brain. Oxford: Oxford University Press. Barnes, G. R., Hess, R. F., Dumoulin, S. O., Achtman, R. L., & Pike, G. B. (2001). The cortical deficit in humans with strabismic amblyopia. Journal of Physiology, 533, 281–297. Birnbaum, M. H. (1981). Esotropia, exotropia and cognitive/perceptual style. Journal of the American Optometric Association, 52(8), 635–639. Gligorovic´, M., Glumbic´, N., Mac´esˇic´-Petrovic´, D., et al. (2005). Specific Learning Disabilities in Children (in Serbian). In S. Golubovic´ (Ed.), Smetnje u razvoju kod dece mlapeg sˇkolskog uzrasta (pp. 415–523). Beograd: Defektolosˇki fakultet, Merkur. Gligorovic´, M. (2010). Numericˇke sposobnosti u detinjstvu [Numerical abilities in childhood]. Specijalna edukacija i rehabilitacija, 9, 85–109 (in Serbian). Gligorovic´, M., & Radic´ Sˇestic´, M. (2010). Procena sposobnosti neophodnih za uspesˇno ovladavanje akademskim vesˇtinama kod dece sa smetnjama u ucˇenju [Assessment of abilities which are indispensable for academic achievement in children with learning disabilities]. Specijalna edukacija i rehabilitacija, 9, 15–36 (in Serbian). Gligorovic´, M., & Vucˇinic´, V. (2010). Kognitivni aspekti vizuelnih sposobnosti kod slabovide dece. Cognitive aspects of visual abilities in low vision children]. Smetnje i poremec´aji: fenomenologija, prevencija i tretman, deo II, Beograd: Fakultet za specijalnu edukaciju i rehabilitaciju. pp. 155–171 (in Serbian). Heyl, V., & Wahl, H. W. (2010). Cognitive ability as a resource for everyday functioning among older adults who are visually impaired. Journal of Visual Impairment & Blindness, 104, 391–403. Hong, S. W., & Park, S. C. (2008). Development of distant stereo-acuity in visually normal children as measured by Frisby-Davis distance stereostest. British Journal of Ophthalmology, 9, 1186–1189. Hyva¨rinen, L. (1988). Vision in children, normal and abnormal. Toronto: Canadian Deaf-Blind Rubella Association. Hyva¨rinen, L. (1994). Assessment of visually impaired infants. Ophthalmology Clinics of North America, 7, 219–225. Koller, H. P. (1999). How does vision affect learning? Journal of Ophthalmic Nursing & Technology, 18, 12–18. Kapoula, Z., & Bucci, M. P. (2002). Distribution-dependent saccades in children with strabismus and in normals. Experimental Brain Research, 2, 264–268. McDonnall, M. C. (2010). The Employment and postsecondary educational status of transition-age youths with visual Impairments. Journal of Visual Impairment & Blindness, 104, 298–303. Mendola, J. D., Conner, I. P., Roy, A., Chan, S. T., Schwartz, T. L., Odom, J. V., et al. (2005). Voxel-based analysis of MRI detects abnormal visual cortex in children and adults with amblyopia. Human Brain Mapping, 25, 222–236.
M. Gligorovic´ et al. / Research in Developmental Disabilities 32 (2011) 1852–1859
1859
Moguel-Ancheita, S., Ramı´rez-Sibaja, S., Reyes-Pantoja, S. A., & Orozco-Go´mez, L. P. (2010). Visuomotor functions and intelligence subsequent to strabismus treatment. Second phase. Cirugı´a y Cirujanos, 78, 468–472. Noordzij, M. L., Zuidhoek, S., & Postma, A. (2007). The influence of visual experience on visual and spatial imagery. Perception, 36, 101–112. Novosel, M. I., & Marvin Cavor, Lj. (1985). Acadia test razvoja sposobnosti. Primijenjena psihologija, 1–2, 103–108. Sharma, V., Levi, D. M., & Klein, S. A. (2000). Undercounting features and missing features: Evidence for a high-level deficit in strabismic amblyopia. Nature Neuroscience, 3, 496–501. Suttle, C. M, Melmoth, D. R., Finlay, A. L., Sloper, J. J., & Grant, S. Eye–hand coordination skills in children with and without amblyopia. Investigative Ophthalmology and Visual Science, in press. Wickham, L., Stewart, C., Charnock, A., & Fielder, A. (2002). The assessment and management of strabismus and amblyopia. Eye, 16, 522–529.