Eye Movement Disorders
This chapter discusses the characteristics, diagnosis, and management of fixational, saccadic, and pursuit eye movement disorders. We use the term ocular motor dysfunction to refer to the condition in which there are problems in all three areas of eye movement function. In our experience, this is the most common clinical presentation. It is unusual to find saccadic dysfunction in isolation of fixational or pursuit anomalies, or pursuit dysfunction in isolation of fixational or saccadic anomalies.
Eye movement disorders are a diagnostic and management concern for optometrists because of the effect such problems may have on the functional capability of an individual. Unlike accommodative1 and binocular vision skills,2 which reach adult levels of development very early in infancy, clinical assessment indicates that eye movement development is considerably slower, continuing through the early elementary school years.3,4 The clinical picture of slow development is not consistent with the basic research data that suggest the presence of normal eye movements by approximately age 1 or 2 years. This apparent difference is likely to be related to cognitive and attentional factors affecting eye movements through about age 12. Because of the long developmental process for eye movement control, slow development can leave a child with inadequate skills to meet the demands of the classroom.5 Saccadic and pursuit dysfunction, therefore, primarily interfere with performance in schoolchildren, although some authors have reported the presence of these problems in adults as well.6,7
Much of the emphasis of both researchers and clinicians has been on the relationship between eye movements and reading. During reading, the three important components of eye movements are saccades, fixations, and regressions. Saccades take up approximately 10% of the reading time. The average saccade is about eight to nine character spaces, which is about a 2-degree visual angle.8 The duration of the saccade is a function of the distance covered. For instance, a 2-degree saccade takes about 25 to 30 ms, and a 5-degree saccade takes about 35 to 40 ms.8 Between saccades, the eye is relatively still in a fixational pause. For normal readers, the average duration of the fixation is 200 to 250 ms. An important characteristic of normal reading eye movements is the great variability both within and between subjects. Saccade lengths can vary from 2 to 18 character spaces, and fixation duration values can range from 100 to over 500 ms, for a single reader within a single passage.8 The third important characteristic of reading eye movements is the regression. A regression is a right-to-left movement, and it occurs 10% to 20% of the time in skilled readers. Regressions occur when the reader overshoots the target, misinterprets the text, or has difficulty understanding the text.
Because eye movement deficiencies intuitively seem to be so closely linked with reading, there have been numerous studies investigating this relationship. Unfortunately, the results of these investigations are equivocal and, at times, confusing. Limitations and differences in experimental design, methodology, statistical procedures, and assumptions among these studies have created difficulty in their interpretation.5 Two basic viewpoints have evolved about the relationship between eye movements and reading. The first suggests that eye movement disorders can cause below-average reading ability.9,10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27 Investigators, using a variety of methods to assess eye movements, have found that poor readers tend to make more fixations and regressions than normal readers.10,11,12,13,14,15,16,17,18,19,20,27 The second view is that the random and unskilled eye movement skills observed in poor readers are secondary to deficient language skills that cause reading disorders. Thus, the reading difficulty itself leads to erratic and inconsistent eye movements.26,28,29,30,31,32
A third perspective is probably most likely to be correct and is essentially a combination of the first two viewpoints. This alternative4 suggests that, in some cases, problems with fixation and saccadic abilities may be a primary factor interfering with a child’s ability to read quickly, comfortably, and with adequate comprehension. In other cases, the eye movement deficiencies observed during reading may simply be a reflection of poor reading ability.
Another important background issue is that during reading, eye movements are integrated with higher cognitive processes such as attention, memory, and the utilization of the perceived visual information.3,33,34,35,36,37,38,39,40 Some optometrists believe that there is a relationship between poor ocular motor skills and attentional problems.41 When such a relationship exists, treatment of eye movement disorders may lead to improvement in attention and concentration.37,38,39
There have been few studies of the prevalence of eye movement disorders, particularly in the population of normally achieving children and adults. In children with reading and other learning difficulties, several studies have found a very high prevalence of eye movement anomalies.42,43,44 In a sample of 50 children between the ages of 6 and 13 years with learning disabilities, Sherman42 found that 96% had problems with ocular motor inefficiency (saccadic and pursuit problems). He did not state how eye movements were evaluated or his criteria for establishing a diagnosis of ocular motor inefficiency. Hoffman43 reported on a sample of 107 children between the ages of 5 and 14 years with learning problems. He evaluated pursuits and saccades using the qualitative scales described in Chapter 1 along with an objective assessment using the Eye Trac. The criteria for a diagnosis of ocular motor dysfunction were performance below a 3+ on the subjective clinical observation or 2 years below age-expected values on the objective assessment. His results revealed that 95% of the sample had ocular motor problems. He also reported on the results of 25 children without learning problems and found that 24% had ocular motor problems. It is interesting to note that both Hoffman and Sherman found that ocular motor dysfunction was the most prevalent vision disorder in their samples of learning disabled children. Lieberman44 studied the prevalence of vision disorders in 55 children between the ages of 8 and 10 years at a school for children with emotional disorders. He used observational scales and the New York State Optometric Association King-Devick (NYSOA K-D) test to evaluate saccades. The NYSOA K-D test is similar to the developmental eye movement (DEM) test described in Chapter 1. Pursuits were evaluated using subjective observational scales; 53% of the children had saccadic dysfunction and 43% had pursuit anomalies. In this same study, Lieberman reported that in a sample of 1,681 children in a normal population, the prevalence of saccadic dysfunction (using the NYSOA K-D test) was 22.6%.
Jainta and Kapoula45 examined the relationship between saccades and vergence control during real text reading. Thirteen dyslexic and seven non-dyslexic children read the French text “L’Allouette” in two viewing distances (40 cm vs. 100 cm), while binocular eye movements were measured with an objective eye-tracking system. They found that the binocular yoking of reading saccades was poor in dyslexic children (relative to non-dyslexics) resulting in vergence errors and fixation disparity. The fixation disparity was larger for dyslexic children, making a larger demand on their sensory fusion processes. The authors concluded that visual/ocular motor imperfections may exist in dyslexics that lead to fixation instability and thus, to instability of the letters or words during reading.
In our experience, and in the three studies described earlier,42,43,44 eye movement disorders are rarely present in isolation. Rather, they are generally found associated with accommodative, binocular, and visual perceptual dysfunctions. As a result, treatment of eye movement deficiencies generally occurs within the context of an overall treatment approach designed to deal with other problems as well.
It is clear that more investigation is needed into the prevalence of eye movement disorders to clarify their role in reading and other areas of function. Regardless of these shortcomings in the literature, clinicians are regularly faced with children and adults presenting with signs and symptoms suggestive of fixation, saccadic, and pursuit disorders. Psychologists and educators often refer children with concerns about poor tracking, skipping words and lines, and losing place when reading. In addition, Solan6 has demonstrated that there are adults with eye movement problems that interfere with their performance in school and at work. Although these individuals often achieve at satisfactory levels, they complain of slow and inefficient reading.7 It is important for clinicians to be able to evaluate eye movement function and to prescribe appropriate treatment if a disorder is detected. An important concept that must be emphasized is that optometrists treat eye movement disorders to normalize these functions and eliminate the patient’s symptoms. We are not directly treating the reading disorders, although in some cases more accurate and efficient eye movements may lead to better reading performance.
Prognosis with Treatment
The primary treatment approach for ocular motor dysfunction is vision therapy. This suggests, of course, that eye movement function can be modified and improved through therapy. Two very different approaches have been used to investigate whether eye movement function can be altered and improved with treatment.
The plasticity and adaptability of the oculomotor system have been studied extensively by basic scientists. This approach has uncovered a broad range of behaviorally induced adaptive responses and a strong potential for central nervous system plasticity within the vestibular-oculomotor system.46,47 Many of these studies have involved investigation aimed at identifying adaptive effects in human neuro-ophthalmologic disorders such as oculomotor paresis. This line of investigation has generally found the presence of adaptive mechanisms that serve to offset degradation of ocular motor performance resulting from interference in neural conduction, neuromuscular transmission, and muscle function because of such factors as aging, injury, and disease.46,47
One investigative approach that has been used to demonstrate that saccades can be modified involves the use of a paradigm called parametric adjustment. This is an approach in which the subject’s saccades toward a target are made artificially inaccurate by shifting the target while the eye is already in flight.48 Using this approach, researchers have demonstrated substantial recalibration of saccadic amplitude after only a small number of saccades.48,49,50,51 Another basic science approach has been to study the changes that occur in ocular motility function after a paresis. Kommerrell et al52 studied the adaptability of the human saccadic system after the development of a sixth nerve paresis. They found evidence that the central nervous system can readjust saccadic innervation and thereby improve performance. Abel et al53 performed a similar study with patients with third nerve palsies. They were able to demonstrate that the adaptive readjustment of saccadic amplitude that occurs after a third nerve paresis depends on alteration of saccadic duration, not saccadic velocity. These basic science studies have demonstrated ocular motor adaptation and plasticity, even in adult subjects. The studies described earlier have found that saccadic function can be modified both in normal subjects and in those with ocular motor disorders.
Clinical studies have also been performed to investigate the efficacy of treating ocular motor dysfunction. Wold et al54 reported on a sample of 100 patients who had completed a vision therapy program for a variety of problems, including accommodation, binocular vision, pursuits, and saccades. Saccadic and pursuit functions were determined using subjective clinical performance scales such as those described in Chapter 1. Vision therapy consisted of three 1-hour visits per week. The number of visits ranged from 22 to 53. It is important to understand that these patients did not only have eye movement disorders, but almost all patients had accommodative and binocular vision problems too. Pretesting and posttesting revealed statistically significant changes in both saccadic and pursuit functions.
In a study of 63 achieving high school students, Solan55 found increased reading rate, fewer fixations, and fewer regressions after treatment. A shortcoming of this study was that subjects received other forms of treatment along with vision therapy. The subjects each received twelve 2-hour sessions of treatment consisting of work with a tachistoscope, a controlled reader, and vocabulary, skimming and scanning, and study skills. Rounds, Manley, and Norris56 used a Visagraph Eye-Movement Recording Systema to assess reading eye movements before and after vision therapy. This investigation is one of the few to specifically study eye movement therapy alone. They used a study population of 19 adults with reading problems and assigned 12 to the experimental group and 9 to a control group. The experimental group received 4 weeks (12 hours) of exclusively oculomotor skill enhancement vision therapy. The therapy consisted of three 20-minute office sessions and six 20-minute home sessions per week for 4 weeks. The control group received no intervention of any kind. The experimental group trended toward improving reading eye movement efficiency (fewer regressions and number of fixations and increased span of recognition) compared with the control group. Statistically significant differences, however, were not evident.
Young et al57 also used an objective eye movement recording instrument (Eye Trac) to assess reading eye movements before and after therapy. The authors studied 13 schoolchildren who had failed a vision screening. Each child had three 5-minute vision therapy sessions per day for 6 weeks, receiving a total of 6 hours of eye movement vision therapy. Testing after the therapy revealed a significant decrease in the number of fixations, an increase in reading speed, and a decrease in fixation duration.
Fujimoto, Christensen, and Griffin58 investigated the potential for using vision therapy procedures prerecorded on videocassettes for eye movement vision therapy. They had three groups of subjects. The first group of nine subjects received standard eye movement vision therapy. The second group received videocassette-based eye movement therapy, and the third group received no treatment. The results showed that both standard eye movement vision therapy and videocassette-based therapy were equally effective in improving saccadic ability, whereas the control group showed no significant change.
Punnett and Steinhauer59 also studied two different approaches for eye movement therapy. They compared the effectiveness of vision therapy for eye movements using feedback versus no feedback. They used the Eye Trac to monitor eye movements and studied nine subjects. They found that the use of verbal feedback and reinforcement during vision therapy led to better treatment results.
Solan, Feldman, and Tujak7 provided vision therapy to improve the efficiency of reading eye movements in 20 older adults (aged 62 to 75 years). Subjects were divided into a training group and a control group. The training group received 16 sessions of vision therapy over an 8-week period. The control group did not receive any treatment for 8 weeks. After posttesting, 8 of the 12 subjects in the control group were randomly selected to receive the 16 sessions of vision therapy. The authors reported a statistically and clinically significant improvement in all aspects of reading efficiency, including reduced number of fixations and regressions per 100 words, increased average span of recognition, and improved reading rate without loss of comprehension. There were no gains in the control group. The authors concluded that vision therapy to improve reading eye movement skills is appropriate at all age levels.
More recently, Solan et al37 identified 31 sixth graders with reading comprehension scores about 1.5 to 3.5 years below grade level. The Visagraph II was used to evaluate eye movements and obtain baseline data. The 31 subjects were divided into two groups. Half of the subjects received individualized reading comprehension therapy first, whereas the others received individual eye movement therapy for twelve 1-hour sessions. After 12 sessions of treatment, reading comprehension and eye movements were reassessed. The eye movement and reading comprehension treatment groups were reversed for the next 12 sessions. After completion of 24 sessions, reading comprehension and eye movement ability were reevaluated. They found significant improvements in the number of fixations, regressions, and rate of reading after the eye movement therapy. This was true irrespective of whether the eye movement therapy was done first or second.
In a subsequent study, Solan et al38 identified 30 children (mean age 11.3 years) with moderate reading disorders; 15 children received attention therapy, and 15 children were placed in a control group. The treatment therapy group received twelve 1-hour sessions of individually monitored, computer-based attention therapy. This attention therapy included five procedures commonly used in traditional vision therapy treatment: three programs from Computerized Perceptual Therapyb and two programs from the Perceptual Accuracy/Visual Efficiency Program.a Attention and reading scores improved significantly in the treatment group, whereas there were no significant improvements in reading scores after 12 weeks in the control group.
Other researchers have investigated the use of biofeedback to improve ocular motor ability in patients with nystagmus and eccentric fixation. Goldrich60 used a technique called emergent textual contour training to provide visual biofeedback regarding eye position and was successful in improving fixational ability. Other investigators have used auditory biofeedback to treat nystagmus. Ciuffreda, Goldrich, and Neary61 and Abadi, Carden, and Simpson62 achieved significant reduction in the amplitude and velocity of eye movements in congenital nystagmus. Flom, Kirschen, and Bedell63 were able to improve fixational skills in amblyopes with eccentric fixation using auditory biofeedback.