Changes of saccadic eye movements in thyroid-associated ophthalmopathy.

PURPOSE: To establish whether or not the dynamics of saccadic eye movements are significantly changed in patients with different stages of thyroid-associated ophthalmopathy (TAO) and, subsequently, if analysis of saccades could serve as an additional diagnostic tool for early detection of inflammatory activity in TAO. METHODS: Thirty-seven patients with TAO and 10 age- and gender-matched control subjects were investigated. The patients were divided into four groups according to the stage of the disease: (i) early mild disease (n = 10), (ii) early severe disease (n = 11), (iii) long-standing restrictive disease (n = 10) and (iv) proven auto-immune hyperthyroidism without any signs of TAO (n = 6). Horizontal and vertical saccades with amplitudes of 10°, 20°, 30° and 40° were recorded binocularly using the induction scleral search coil technique. The two main sequence constants V(max) and C were calculated for each eye. Repeated measurement analysis of variance was carried out to test for differences between different gaze directions, eyes and groups. RESULTS: In horizontal saccades, significant differences were found between groups but not between abduction and adduction. In vertical saccades, differences between groups and the interaction between groups and up- and down-gaze saccades were significant. Compared with the control group, analysis of the main sequence curves revealed larger differences in patients of group 3 and 4 than in those of group 1 and 2. Whereas in the control group down-gaze saccades were faster than up-gaze saccades, the opposite behaviour was found in all patient groups. The largest differences were detected among those patients who had no signs of TAO (group 4). CONCLUSIONS: In this study, significant saccade differences were detected in all patients with TAO. In contrast to our earlier studies where evaluation of multiple individual saccade parameters did not reveal significant differences, analysis of the main sequence constants and mathematical reconstruction of the main sequence curves turned out to be a sensitive technique for reliable detection of subtle ocular motility changes. Significant differences were detected even in patients with auto-immune thyroiditis where no clinical signs of TAO were apparent.

Succinylcholine activation of human horizontal eye muscles.

PURPOSE: Succinylcholine (Sch) can induce contracture in slow, multiply innervated muscle fibres of the extraocular muscles in animals of different species. Slow muscle fibres also exist in human eye muscle but their physiological properties have not been studied. METHODS: Isometric tension development was recorded in the lateral and medial rectus muscles in 12 patients operated under general anaesthesia. A strain gauge probe was attached with 5-0 silk sutures to the muscle tendon. Recordings were made in 12 eye muscles with the tendon attached to the globe and in four muscles detached from the globe. Muscle activation was produced by i.v. injection of Sch at a dose of 0.2-0.3 mg/kg bodyweight. RESULTS: A single injection of Sch induced slow contractures lasting for several minutes. In the muscles attached to the globe, mean maximal isometric tension was 12.2 g in the lateral rectus and 12.8 g in the medial rectus. Similar tension was shown in the muscles detached from the globe. CONCLUSIONS: The contracture of eye muscles in response to Sch showed characteristics typical of slow muscle fibre activation in amphibian and avian muscle and confirmed the participation of slow fibre systems in ocular motor control.

Isometric force development in human horizontal eye muscles and pulleys during saccadic eye movements.

PURPOSE: The connective tissue elements forming the check ligaments and portals of the human eye muscles have recently been ascribed with a pulley function. Active positioning of the pulleys over orbital layer contraction during eye movements has been suggested. Other studies have instead demonstrated fibrous tissue connections between all parts of the muscle and the pulleys. We aimed to compare the isometric force developed at the muscle tendon and at the pulleys of the horizontal eye muscles, and to investigate which eye muscle structures might exert force on the pulleys. METHODS: Isometric force development was recorded from the lateral and medial rectus muscles in six patients operated for strabismus under topical anaesthesia. Two strain gauge probes were used, each attached with 5-0 silk sutures either to the muscle tendon or to the pulley. The eye muscles were activated by horizontal saccadic eye movements in steps from 30 degrees in the off-direction to 30 degrees in the on-direction of the muscles. RESULTS: The forces developed at the tendon and pulley were almost identical with respect to amplitude and other parameters. No differences were found in forces developed at the pulleys of the medial and lateral rectus muscles. CONCLUSIONS: The results support the presence of fibrous tissue connections between all eye muscle fibres and pulley structures, rather than orbital fibre control of the pulley.

Orthoptic findings and asthenopia in a population of Swedish schoolchildren aged 6 to 16 years.

PURPOSE: To determine the prevalence of refractive errors and binocular disorders in relation to asthenopia in a representative population of Swedish schoolchildren. METHODS: The study population included 216 schoolchildren, 60 in grade 1 (age 6-7 years), 96 in grade 4 (10-12 years) and 60 in grade 8 (14-16 years). Asthenopia was evaluated by questionnaire. Visual acuity was tested for distance and near, uncorrected and with the best subjective refraction. Refraction in cycloplegia and an orthoptic assessment was performed. RESULTS: Asthenopia was reported in 23.1% of schoolchildren; all but two of these schoolchildren had an abnormal eye examination. Asthenopia was related to uncorrected visual acuity < or = 0.65 (13.9%*) and myopia (8.8%*). No significant correlation could be found to accommodative or convergence insufficiency. CONCLUSION: Asthenopia was significantly associated with uncorrected visual acuity < or = 0.65 and with myopia (spherical equivalent -0.50 D or less) among Swedish schoolchildren.

Strabismus and eye muscle function.

Studies of external eye muscle morphology and physiology are reviewed, with respect to both motor and sensory functions in concomitant strabismus. The eye muscles have a more complex fibre composition than other striated muscle, and they are among the fastest and most fatigue-resistant muscles in the body. However, it is not generally believed that concomitant strabismus is due to a primary abnormality of the eye muscles or the ocular motor system. The gross anatomy of eye muscles, including the shape and position of the eye muscle pulleys, was not changed in strabismus. The histology of the eye muscle fibres was also basically the same, but changes have been observed in the cellular and biochemical machinery of the fibres, most notably in the singly innervated orbital fibres. Functionally, this was seen as slower contractions and reduced fatigue resistance of eye muscles in animals with strabismus and defects of binocular vision. Most likely the changes represented an adaptation to modified visual demands on the ocular motor control, because of the defects of binocular vision in strabismus from an early age. Adaptation of eye muscle function to visual demands could be seen also in the adult human ocular motor system, but here the effects could be reversed with treatment in some conditions. External eye muscles in the human have sensory organs, muscle spindles and tendon organs, responding to changes in muscle force and length. It is not known how these proprioceptors are used more specifically in ocular motor control, and there is no stretch reflex in the external eye muscles. However, a clear influence on space localization and eye position can be demonstrated with vibratory stimulation of the eye muscles, presumably activating muscle spindles. Different effects were observed in normal subjects and in adult patients with strabismus, which would indicate that the proprioceptive input from one eye of strabismic patients could be suppressed by the other eye, similar to visual suppression in concomitant strabismus. Such an interaction would most likely occur in the visual cortex, and not in the ocular motor system. Further studies of proprioceptive mechanisms, during the postnatal developmental stage and in adult concomitant strabismus may shed light on the mechanisms of childhood strabismus and may, in this respect, be a more fruitful avenue for further research than eye motor studies.

Eye muscle force development in thyroid-associated ophthalmopathy in different stages of disease.

PURPOSE: Ocular motility disturbances are common in patients with thyroid-associated ophthalmopathy (TAO). A quantitative evaluation of the isometric force of the eye muscles in TAO might be useful in the detection of early stages of this disease. METHODS: A total of 32 patients with TAO were divided into three groups according to whether they had mild active, pronounced, active, or longstanding, inactive disease. A group of six patients with Graves' disease without clinical signs of TAO and a group of 10 control subjects were also studied. The development of isometric force during saccadic eye movements of 5-, 10- and 20-degree amplitude in horizontal and vertical directions of gaze were recorded in the more affected eye in patients and the non-dominant eye in normal subjects, using a suction contact lens/strain gauge technique. RESULTS: Peak tension (Fp) in vertical and horizontal saccadic movements was not significantly different between groups. Steady-state tension (Fs) was significantly higher in the groups with pronounced, active and longstanding, inactive disease than in the other groups for vertical (p < 0.01) and horizontal movements (p < 0.05). Abnormal force development in any of the gaze directions was seen in all patients with pronounced, active and longstanding, inactive TAO, and in some of the patients with mild, active TAO and Graves' disease without TAO. CONCLUSIONS: Increased eye muscle tension was recorded in different gaze directions, confirming multiple extraocular muscle involvement in TAO. It is suggested that the increased force development reflected contractile compensations for restrictions of ocular motility due to higher muscle stiffness in thyroid-associated eye muscle disease. Tension measurements can be used to identify muscle involvement in TAO.

Magnetic resonance imaging and ultrasound measurements of extraocular muscles in thyroid-associated ophthalmopathy at different stages of the disease.

PURPOSE: To assess extraocular muscle (EOM) involvement in thyroid-associated orbitopathy (TAO) of different stages with magnetic resonance imaging (MRI) and ultrasound techniques. METHODS: A total of 32 patients with TAO were divided into three groups according to whether they had mild active, pronounced active or longstanding inactive disease. Six patients with Graves' disease but no clinical signs of TAO and 10 healthy control subjects were also studied. Muscle volume and cross-sectional area were measured with MRI. A-scan ultrasound was used to measure muscle thickness. RESULTS: The average MRI volume and maximal cross-sectional area of the EOM were significantly larger in patients with pronounced active and longstanding inactive TAO than in control subjects. Increased average muscle thickness measured by ultrasound was found mainly in patients with longstanding disease. Muscle enlargement was seen with MRI and ultrasound in individual patients in all patient groups, including those with Graves' disease but no TAO. Bilateral muscle enlargement was revealed by MRI in about two-thirds of patients with mild active TAO and in all patients with pronounced active and longstanding inactive TAO. Bilateral involvement estimated with ultrasound was less common in all patient groups. The MRI and ultrasound findings were not well correlated in any patient group. CONCLUSIONS: Extraocular muscle enlargement was seen in all patient groups with TAO of differing levels of severity. Measurements with MRI of muscle volume or maximal cross-sectional area are considered good indicators of muscle enlargement in TAO.

Isometric force measured in human horizontal eye muscles attached to or detached from the globe.

BACKGROUND: Human eye muscle tension has been measured directly only in detached condition. The purpose of this study is to compare force development in single, horizontal human eye muscle during saccadic eye movements, first when the muscle was still attached and later when it was detached from the globe. METHODS: Eleven horizontal muscles of eight patients were examined during surgery under topical anesthesia for concomitant strabismus. None of the muscles examined had been operated before. Isometric muscle tension was recorded with a strain gauge system, to which the muscle tendon was attached by a silk suture. The subjects made saccadic eye movements with the non-recorded eye by fixating light-emitting diodes in the center and at 10, 20, and 30 degrees horizontally to each side. Continuous and stepwise saccades were produced. In the tension signals, peak tension (Fp), steady tension (Fs), and the ratio Fp/Fs were measured. Statistical analysis was done with multivariate analysis of variance. RESULTS: The values of Fp, Fs, and Fp/Fs at different amplitudes of the saccadic eye movements were compared in the attached and the detached muscle. There were no consistent statistical differences between the values obtained in the two conditions. CONCLUSIONS: The muscle force development, measured at the tendon, was the same in muscles attached to the globe and in muscles free from the globe. Thus isometric muscle tension can be adequately recorded in muscles still attached to the globe, which increases the possibilities for studying contractile properties of various eye muscles during ophthalmic surgery procedures performed under topical anesthesia.

Strabismus and sensory-motor function of eye muscles.

Paul Bach-y-Rita and coworkers at the Smith-Kettlewell Institute of Visual Science of San Francisco were among the first to record activity in the muscle fibers of the eye muscles in animals. With their newly developed methods, they could describe fast and slow muscle fibers types and present possible patterns of recruitment of the fibers in different eye movements. These studies have been critical for continued animal research on eye muscle fibers and motor units in different species and in animals of different ages. Bach-y-Rita and coworkers also recorded from receptors in the muscles and demonstrated stretch reflexes different from those of skeletal muscles. Further research in animals revealed that it was difficult to delineate the functional role of the muscle receptors in oculomotor control. However, recent studies on sensory functions of human extra ocular muscles have suggested that proprioception participates in space localization, and the functions may differ in normal and strabismic subjects. The eye muscle studies initiated by Bach-y-Rita have enabled analysis of the sensory-motor components of strabismus or squint in greater detail than before.

Eye muscle force development and saccadic velocity in thyroid-associated ophthalmopathy.

BACKGROUND: Ocular motility disturbances are very common in patients with thyroid-associated ophthalmopathy (TAO). The force duction test has demonstrated that limitations of eye movements may be caused by mechanical restrictions in the muscles. A quantitative evaluation of isometric force production and ocular motility in all directions of gaze could further elucidate the mechanism of the movement disorder. METHODS: In eight patients with TAO and eight controls of the same age range, horizontal and vertical saccadic movements of both eyes were recorded by means of electro-oculography (EOG). The corresponding force development in muscles of the more affected eye in patients and the non-dominant eye in normals was measured, using a suction contact lens/strain gauge technique. RESULTS: Steady-state tension in the patients was increased in all directions of gaze both horizontally and vertically, most markedly for vertical fixations in the upper field of gaze. However, peak tension was increased only for the downward movements in the upper field of gaze and for the horizontal movements in the abduction field of gaze. Vertical saccadic velocity was slower than normal in downward movements, and horizontal saccadic velocity was reduced in the abduction field of gaze. CONCLUSION: The increased active eye muscle tension in different directions of gaze could represent an adaptational mechanism of the ocular motor system to overcome the eye movement restriction in TAO.

Significance of orbital fatty tissue for exophthalmos in thyroid-associated ophthalmopathy.

PURPOSE: To correlate exophthalmos with the volume of extraocular muscle and orbital fatty tissue in thyroid-associated ophthalmopathy (TAO), using MRI that enables the orbital soft tissues to be well defined. METHODS: Thirty-three orbits, 20 from 10 patients with TAO and 13 from 13 controls, were employed. T1-weighted orbital MR slices 2 or 3 mm thick were obtained in axial, coronal and sagittal planes. Tracing the outlines of each structure, we measured the total sectional areas. Volumes of the extraocular muscle, of the fatty tissue and of the bony orbital cavity were calculated by multiplying the slice thickness. Exophthalmos was also measured using axial MRI. RESULTS: In TAO the volume increment of orbital fatty tissue (6.19 cm(3)) was much greater than that of extraocular muscle (1.16 cm(3)). Increase of exophthalmos by 1 mm needed a total orbital volume increment of 0.92 cm(3). The total orbital fatty tissue volume (correlation coefficient 0.70, P=0.06%) and the anterior orbital fatty tissue volume (0.64, P=0.23%) were more closely correlated with the degree of exophthalmos than was extraocular muscle volume (0.58, P=0.8%). Moreover, the volume increment of extraocular muscle and orbital fatty tissue was not always proportional. CONCLUSION: The results show that the orbital fatty tissue involvement is closely related to the degree of exophthalmos. For studying exophthalmos in TAO, the volumetric change, not only in ocular muscles, but also in orbital fatty tissue, should be taken into consideration.

Assessment of ocular counterroll during head tilt using binocular video oculography.

PURPOSE: According to recent literature, the presence and the amount of true compensatory ocular counterroll is still debatable. The purpose of the current study was to assess compensatory counterroll in response to lateral head tilt using a new noninvasive recording technique, and, furthermore, to find out whether the amount of counterroll is influenced by the presence or absence of spatial orientation. METHODS: Eye movement recordings were performed using the infrared three-dimensional video oculography (3D-VOG) technique. Objective cycloposition of five healthy individuals was measured in presumed primary position and in head tilt positions of 15 degrees, 30 degrees, and 45 degrees to the right and left. The same paradigm was performed under three viewing conditions: binocularly without spatial orientation and both binocularly and monocularly with spatial orientation. RESULTS: A consistent ocular counterroll corresponding to the amount of head tilt was observed in all subjects. Maximum torsional amplitude was 10 degrees at a 45-degree head tilt. The relative amount of compensation ranged between 13% and 22% of the actual head tilt, decreasing with increasing head tilt. Compensatory counterroll and torsional conjugacy between both eyes revealed minor differences between the experimental paradigms. Incomplete cycloductional reorientation in primary position after head tilt was detected in all subjects, regardless of the stimulus. CONCLUSIONS: A consistent compensatory ocular counterroll was demonstrated in response to static lateral tilting of the head in healthy individuals. The amplitude of counterroll and the gain of compensatory cycloversion were higher than has been generally reported. Infrared 3D-VOG technique was a reliable and comfortable method for the assessment of ocular cycloduction. It can be considered to be a promising tool for advanced evaluation of disturbances of the oblique eye muscles.