Original articleVoluntary control of saccadic and smooth-pursuit eye movements in children with learning disorders
Introduction
Learning disorders (LDs) are defined as a developmental disorder in children and are characterized by learning difficulties at school. These difficulties do not occur as a result of low intelligence, lack of educational opportunity, visual, auditory or any other neurological disorder [1]. LDs include several specified disorders. According to the DSM-IV categorization, they are divided into the following four groups: reading disorder, mathematics disorder, disorder of written expression and learning disorder not otherwise specified.
Eye movement is important in allowing humans to acquire accurate vision. Saccadic eye movement is used to rapidly adjust the visual axis between the foveae and an object in order to aim, the foveae of both eyes at an object of interest (e.g. as in reading).
Many researchers have discussed the characteristics of eye movements during reading in dyslexia (reading disorder). Pavlidis [2] reported that the eye movements of dyslexics during reading were different from those of normal controls, suggesting that abnormal eye movements were responsible for the reading disability. However, other studies revealed no abnormalities in the eye movements of dyslexics during reading compared with those of control subjects [3], [4]. It has been reported that there was no significant difference between dyslexia and normal controls in saccadic eye movements [5], [6], [7]. These reports suggest that abnormal eye movement during reading is not the cause of reading disability.
On the other hand, Biscardi et al. [8] reported that dyslexic patients showed a greater number of express saccades with latencies of 85–135 ms. They also reported that patients who showed higher rates of express saccades could not suppress reflexive saccades to the target in the memory-guided saccade task. This suggests that dyslexics may have difficulties in the voluntary control of saccadic eye movements, despite not showing any abnormalities in simple visually guided saccades. A previous study, we carried out on normal children also showed that maturation in executing complex saccade tasks (i.e. anti-saccades and memory-guided saccades) was delayed, compared with the results for a simple visually guided saccade task [9].
Children with LDs often have difficulties in more than two subcategories of DSM-IV, indicating that dyslexic children may also have other types of learning disabilities [10], [11]. It has been reported that dyslexic subjects often showed sensorimotor abnormalities other than reading disabilities [12], [13]. Moe-Nilssen reported that dyslexic subjects showed disturbances of balance and gait [13]. These studies suggest that the abnormal eye movements found in dyslexia may be a consequence of brain dysfunction or delayed development and not merely the cause of reading difficulties. It is possible that eye movement disorders may be characteristic of learning disorders in general. Therefore, we examined eye movement, not only in dyslexics but also in other LD subjects both with and without dyslexic symptoms. The primary aim of the present study was to compare performances in saccade tasks between LD subjects and age-matched normal children.
Another subsystem of eye movement is smooth-pursuit eye movement (SPEM), which is used to pursue a slowly moving small object [14]. Here, subjects must match the velocity of the eyes to the velocity of an object in order to keep the images of that object near the foveae in order to ensure online processing of visual signals during target movement. The major brain areas related to SPEM are the middle temporal (MT) and medial superior temporal (MST) visual areas. From there, descending fibers project directly to the dorsolateral pontine nucleus. There are also pathways through the frontal eye fields (FEF) and the supplementary eye fields (SEF) to the pontine nuclei. It has been reported that neurons in the FEF and SEF respond to SPEM [15], [16], [17]. Since the FEF and SEF are involved in both saccadic and smooth-pursuit eye movements, it is possible that LD subjects who show abnormalities in the control of saccadic eye movements may also show abnormalities in SPEM.
So far, little research has been done on SPEM in LD subjects. Ygge et al. [18] examined dyslexics using both sinusoidal and ramp-stimuli, and concluded that dyslexics showed no abnormalities. Black et al. [19] reported that there was no significant difference compared to controls, but that about 25% of dyslexics showed more intrusive saccades in response to a triangular wave stimulus. According to these studies, dyslexic subjects revealed no major abnormalities in SPEM. However, none of these studies examined initiation of pursuit. Also, it is necessary to further examine steady state SPEM quantitatively.
Because the latency of smooth-pursuit to a ramp target motion is 100–120 ms, the initial eye movement within 100–120 ms of onset of pursuit is driven entirely by visual inputs. During this open-loop condition [14], the eye accelerates to peak values with eye velocity usually overshooting target velocity, and sometimes showing oscillation after overshooting. However, with the later periods that allow visual feedback (i.e. closed loop condition), eye velocity is stable and almost identical to target velocity. A step-ramp stimulus [20] is commonly used to examine peak velocity in the open-loop condition and average velocity in the closed-loop condition. The second aim of this study, therefore, was to examine open and closed-loop responses in SPEM in LD subjects by using step-ramp target motion.
Section snippets
Subjects
This study has been approved by the ethics committee of Hokkaido University, School of Medicine. Informed consent was obtained from the subjects and their guardians following a full explanation of the procedures to be undertaken. LD subjects were recruited from an organization of parents of children with learning problems at school. All subjects fulfilled the criteria set out in the ‘Report by the Japanese Ministry of Science and Education’ (1999), which defines such subjects as those whose
Saccade, anti-saccade and memory-guided saccade tasks
Performances with poor fixation, with head moving or without any appropriate eye movement within 1000 ms after target presentation were excluded from the measurements, because of the possibility that the subjects might not have paid sufficient attention in these cases. For LD patients, the average ±SD discarded rates were 6.4±3.2% for the visually guided saccade task, 9.1±14.0% for the anti-saccade task and 25.6±21.6% for the memory-guided saccade task. In normal children, the mean exclusion
Discussion
The present results are summarized as follows: (1) LD subjects showed higher discarded rates, even though they cooperated fully in the completion of tasks; (2) LD subjects showed normal results in latency, gain and peak velocity in the visually guided saccade task; (3) LD subjects did show longer latencies in the anti-saccade task, even though they did not show higher error rates; (4) LD subjects showed higher error rates and longer latencies in the memory-guided saccade task; (5) LD subjects
Acknowledgements
We would like to thank all the subjects and their guardians involved in this study, with special thanks to the organization of parents with children with learning problems at school. We would also like to thank Dr. J. Katayama at the Department of Education, Hokkaido University for his cooperation in this experiment. Ms. Fumiyo Osanai, Ms. Reina Oyama and Ms. Kayoko Hatakeyama participated in the early part of this study.
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Reading deficits in schizophrenia and their relationship to developmental dyslexia: A review
2018, Schizophrenia ResearchCitation Excerpt :Qualitative ratings used in early studies of smooth pursuit yielded deficits in three of four studies (Eden et al., 1994; Adler-Grinberg and Stark, 1978; Bogacz et al., 1974; cf. Ygge et al., 1993). Quantitative studies have also found deficits, with replicable findings of reduced gain and elevated saccade rates (e.g., Black et al., 1984; Eden et al., 1994; Fukushima et al., 2005; Judge et al., 2006; Lennerstrand et al., 1993; Masters, 1988; Sucher and Stewart, 1993; cf. Brown et al., 1983a, 1983b; Yang et al., 2010). Reflexive saccade studies have been equivocal, with some studies reporting longer latencies (Bucci et al., 2008; Dossetor and Papaioannou, 1975; Fischer and Weber, 1990; Pirozzolo and Rayner, 1978), others reporting shorter latencies and more express saccades (Bednarek et al., 2006; Biscaldi et al., 1994; Fischer et al., 1993), and yet others reporting no differences (Adler-Grinberg and Stark, 1978; Black et al., 1984; Brown et al., 1983a, 1983b; Leisman et al., 1978; Stanley et al., 1983).
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2016, Psychiatry ResearchCitation Excerpt :Nkam et al. (2010) have reported that poor pursuit performance during smooth pursuit was primarily a consequence of a predictive deficit in SCZ patients. Indeed, both frontal eye fields and supplementary eye fields make important contributions to predictive aspects of smooth pursuit, based on internal representation of a target motion (Leigh and Zee, 1999; Fukushima et al., 2005). Previous studies have also shown that SCZ patients and their non-schizophrenic relatives have deficits in P50 inhibition, relative to healthy subjects (Louchart-de la Chapelle et al., 2005a; Adler et al., 2008).
Unaffected smooth pursuit but impaired motion perception in monocularly enucleated observers
2014, Vision ResearchCitation Excerpt :Our data show that the smooth pursuit gain of the enucleated participants is as good, if not slightly better, than that of the age-matched controls for whom there was no binocular advantage. While some researchers have found that the development of closed-loop smooth pursuit continues into late adolescence (Katsanis, Iacono, & Harris, 1998; Luna, Velanova, & Geier, 2008), others have found no significant differences in either open or closed-loop smooth pursuit gain between adults and 7–15 year olds (Fukushima et al., 2005). For simple pursuit stimuli such as the small white dot used in the present study, children generally (but not adults) exhibit lower pursuit gain than for more complex stimuli such as pictures of cartoon characters (Irving et al., 2011).
Children with a learning disorder show prospective control impairments during visuomanual tracking
2010, Research in Developmental DisabilitiesCitation Excerpt :Furthermore, it requires a fast, continuous updating of this predictive model and adjustments of the movements accordingly (Magdaleno, Jex, & Johnson, 1970; Mounoud et al., 1983). Recently, it has been shown that children with learning disorders (LD) evince disturbances in smooth pursuit eye movements (i.e., visual tracking; Fukushima, Tanaka, Williams, & Fukushima, 2005). This is probably due to a less adequate use of prospective control, caused by problems with processing feedback and (predictive) perceptual information in the task environment (Weiler et al., 2000).
Development of eye-movement control
2008, Brain and CognitionEye tracking studies of normative and atypical development
2007, Developmental Review