Brain, Vol. 122, No. 8, 1495-1505,
August 1999
© 1999 Oxford University Press
Impaired analysis of moving objects due to deficient smooth pursuit eye movements
Department of Neurology, University of Tübingen, Tübingen, Germany
Correspondence to:
Dr Thomas Haarmeier, Sektion für Visuelle Sensomotorik, Klinikum Schnarrenberg, Hoppe-Seyler-Strasse 3, 72076 Tübingen, Germany E-mail: thomas.haarmeier{at}uni-tuebingen.de
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Abstract |
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It is usually assumed that the raison d'être for smooth pursuit eye movements is an advantage in the visual analysis of moving objects due to the stabilization of the retinal image on the fovea. Although such benefits resulting from foveal pursuit are plausible, there have been few attempts to demonstrate them rigorously. Moreover, it is unknown whether and to what extent pursuit deficits due to neurological disease impair vision. In this study, therefore, we measured psychophysical thresholds for two different discrimination tasks assessing the visual analysis of moving objects as a function of smooth pursuit performance. Results from a group of healthy subjects were compared with those obtained from patients exhibiting catch-up saccades (n = 9) or saccadic intrusions in the form of square-wave jerks (n = 2). In a first set of experiments we measured acuity thresholds for Landolt optotypes moving horizontally at velocities of up to 14°/s (dynamic visual acuity, DVA). In the control group (n = 20), DVA thresholds were indistinguishable from thresholds observed under stationary fixation due to efficient pursuit eye movements allowing continuous foveal stabilization of the retinal Landolt image. In contrast, all patients with catch-up saccades showed pursuit gains that decreased with increasing velocity, paralleled by a dramatic rise in DVA thresholds. Patients with square-wave jerks in turn revealed sufficient pursuit velocity but impaired foveation due to the involuntary saccades that occurred at similar frequencies independent of target velocity. In these patients, thresholds were more or less independent of the Landolt velocity but significantly raised compared with controls. Similar results were obtained in a test determining the sensitivity for vertical position steps of a given pursuit target. In summary, our results indicate that the lack of adequate pursuit eye movements is indeed deleterious for the visual analysis of moving objects.
smooth pursuit eye movements; catch-up saccades; square-wave jerks; dynamic visual acuity; visual deficits
ADCA I = autosomal dominant cerebellar ataxia I; ANOVA = analysis of variance; DVA = dynamic visual acuity; SVA = static visual acuity
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Introduction |
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Our ability to distinguish differences in light intensity and to identify such differences as belonging to different areas in the visual field is the major prerequisite for seeing shapes or patterns (Westheimer, 1972
). Traditionally, this ability has been described in terms of the limits of spatial resolution thresholds assessed for stationary objects observed during stable fixation (static visual acuity, SVA). In many of our everyday activities, however, either the observer or the object or both are in motion, and this establishes the need for compensatory eye movements in order to keep the retinal object image on the fovea. The ability to resolve a target when there is relative motion between the target and the observer is commonly referred to as the dynamic visual acuity [DVA (Ludvigh and Miller, 1958)]. Since relative motion between a target and an observer is prompted by many practical activities, such as driving a car, flying and athletics, it has been suggested that DVA provides a more realistic estimate of visual performance under everyday conditions than SVA (e.g. Long and Riggs, 1991).
Studies on DVA have been performed in recent years in order to elucidate the roles of different types of compensatory eye movements. For example, deficient vestibulo-ocular reflexes in patients suffering from peripheral vestibulopathy have been found to result in severe impairment in visual acuity during head rotation (Demer et al., 1994). More recently, Lempert and colleagues (Lempert et al., 1997) have convincingly demonstrated the essential role of the otolith–ocular reflexes in maintaining visual acuity during linear head movements. While the contribution of short-latency ocular reflexes to our visual perception is thus well established, there have been few attempts to test whether and to what extent perceptual deficits result from impaired voluntary eye movements such as smooth pursuit. This is unfortunate in view of the fact that pursuit eye-movement deficits are much more common than, for example, vestibulo-ocular reflex deficits, reflecting the high vulnerability of an extended neural network encompassing cortical areas V1, MT, MST, the frontal eye fields, the pontine nuclei, parts of the cerebellum and the brainstem (for a review, see Keller and Heinen, 1991). Beyond lesions of each of these structures as a consequence of neurological disease, there are other causes resulting in pursuit deficits, such as intoxication by drugs and physiological ageing (Sharpe and Sylvester, 1978; Spooner et al., 1980). In view of the fact that the raison d'être for smooth pursuit eye movements has always been seen as an advantage in the visual analysis of moving objects, which is achieved by the stabilization of the retinal image on the fovea, it is to be expected that pursuit disorders should result in visual deficits. However, these are not assessed by standard physical examinations, including tests of SVA.
The present study was performed in order to evaluate the perceptual consequences of insufficient pursuit eye movements. To this end, we measured resolution thresholds for moving objects in a group of healthy subjects as a function of smooth pursuit performance and compared the results with those obtained from patients suffering from pursuit disorders. The difference between the groups serves as a direct estimate of the perceptual benefits resulting from foveal pursuit.
Further, the work presented here provides a detailed experimental analysis of the underlying oculomotor and retinal factors that contribute to the (expected) loss of visual acuity in patients with insufficient pursuit eye movements. High visual acuity is generally thought to be the consequence of minimized retinal image motion and stabilization of the target image on the fovea, i.e. small retinal position errors. Specifically, it is usually held that vision is degraded if retinal image motion exceeds a speed of 2.5–4.0°/s (Westheimer and McKee, 1975; Murphy, 1978; Barnes and Smith, 1981). Since impaired pursuit velocity results in increased retinal image motion, this factor may be responsible for deficits in visual acuity for moving targets. However, in view of the known exponential decay of visual resolution with increasing retinal eccentricity, visual deficits in patients with saccadic pursuit eye movements could, in principle, also be explained in terms of an extrafoveal position of the target image, i.e. in terms of increased retinal position errors. Finally, a detrimental effect on the visual analysis of moving objects might directly result from the occurrence of saccades, as the sensitivity of visual perception in the presence of saccades is known to be strikingly reduced. This phenomenon is typically referred to as `saccadic suppression' or `saccadic omission' and has been extensively studied for voluntary saccades (for a review, see Matin, 1974; Volkmann et al., 1978). Although we are not aware of studies demonstrating that saccadic suppression extends to catch-up saccades and square-wave jerks, it is clearly possible that vision during tracking eye movements is mainly restricted to the saccade-free periods and is thus significantly limited in patients with saccadic pursuit. In order to evaluate the contributions of the three possible sources of visual deficits expected in our patients, their individual oculomotor performance was rigorously analysed and correlated with the psychophysical results.
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Subjects
Eleven patients participated in the study (nine males and two females; mean age 38 years, range 20–58 years). All patients suffered from neurological diseases mainly compromising the cerebellar system, nine of the patients exhibiting global cerebellar atrophy as revealed by MRI and the remaining two suffering from focal cerebellar lesions affecting only one of the cerebellar hemispheres. Neurological diagnoses included autosomal dominant cerebellar ataxia I (ADCA I, n = 4), idiopathic cerebellar ataxia (IDCA) without (n = 1) and with (n = 1) additional extracerebellar symptoms, early-onset cerebellar ataxia of unknown aetiology (n = 2), Friedreich's ataxia (n = 1), right cerebellar medulloblastoma (n = 1) and left cerebellar arteriovenous malformation (n = 1). For further analysis, patients were grouped according to their pattern of pursuit problem rather than on the basis of the underlying aetiology. The first group comprised nine patients who exhibited saccadic pursuit eye movements characterized by reduced pursuit velocity and catch-up saccades (Fig. 3A
). A second, smaller group comprised two patients (one Friedreich ataxia patient and one of the ADCA I patients) who exhibited normal pursuit velocity but suffered from saccadic intrusions in the form of square-wave jerks (Fig. 6A). As will be shown in the Results section, these two patterns of pursuit impairment resulted in different disturbances of the visual analysis of moving objects.
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Normal controls were recruited either from the clinical staff or from the pool of patients in our clinic with diseases of the peripheral nervous system but no oculomotor disorder. Twenty control subjects participated in the acuity measurements (eight males, 12 females; mean age 32 years, range 23–58 years); in a second series of experiments (detection of vertical position steps, see below) the patients were compared with a second group of controls comprising eleven subjects (seven males, four females; mean age 38 years, range 24–59 years). Patients and control subjects suffering from refractive errors wore their glasses during testing. Informed consent was obtained from all patients and normal subjects according to the guidelines of the local ethics committee, which approved the study.
Psychophysical tests
SVA and DVA
Resolution thresholds were measured binocularly, for both stationary Landolt C (SVA) and for moving Landolt C to be tracked by eye movements with the head restrained (DVA). Stimuli were presented on a 19-inch computer monitor (Mitsubishi, frame rate 72 Hz, 1280 x 1024 pixels) in a brightly lit experimental room at a viewing distance of 225 cm. At this viewing distance the pixel resolution of the monitor was 0.45' of arc. Resolution of the optotypes was further improved by a factor of four by anti-aliasing techniques, i.e. smoothing of the contours of Landolt C by grey-shading, allowing the adequate testing of visual acuities ranging from 0.4' to 8.0' (Bach, 1995). Two control experiments on normal observers performed at a viewing distance of 5 m resulted in acuity thresholds that were indistinguishable from those observed for the closer viewing distance, and thus confirmed the latter to be sufficient for reliable acuity measurements.
Landolt C optotypes were presented on a local background (white circle, luminance = 60 cd/m2, extending the Landolt C by 20' on either side) on an otherwise grey screen (luminance = 7.8 cd/m2). In the measurements of SVA, single trials started with a 500 ms presentation of the stationary local background followed by the Landolt C being visible for 250 ms (Fig. 1A). Dynamic visual acuity was determined using a ramp paradigm with the local background moving in a horizontal direction at a given velocity (visual angle = 8°; Fig. 1B). Unpredictably within this sweep (330–1000 ms after the background had started to move), the Landolt C was added to the local background and participated in the movement for 250 ms. Subjects were instructed to fixate the stationary background (SVA) and to track the moving background (DVA) as accurately as possible and then press one of two buttons according to the orientation of the Landolt gap, which was either to the left or to the right (two-alternative forced-choice paradigm). The acuity threshold was defined as the Landolt C gap resulting in 75% correct responses, where 50% correct is the chance performance level. These thresholds were determined by means of a probit analysis (McKee et al., 1985) with subsequent 
2 goodness-of-fit tests performed on the responses obtained from at least 50 trials in each session. The sequence of Landolt rings presented during the course of one measurement was controlled by an adaptive staircase procedure (PEST; Lieberman and Pentland, 1982), the size of the Landolt gap presented in the first trial being 6.5'.
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Each experimental session in an individual subject started with an SVA measurement followed by several DVA measurements that differed with respect to the target velocity chosen. While in the control subjects DVA thresholds were determined for seven different Landolt velocities, which were varied randomly from 2° to 14°/s in steps of 2°/s, patients participated in at least three DVA measurements (4°, 8° and 12°/s), three of the patients additionally being tested under the 14°/s condition. Pursuit direction in the DVA experiments was always to the right. Only in those patients who suffered from an asymmetrical cerebellar lesion with asymmetrical pursuit (n = 2) were tests performed for both horizontal directions.
SVA and DVA as functions of retinal position error
In order to clarify whether position errors alone can account for the DVA loss expected in patients with saccadic pursuit, we performed a second series of control experiments testing DVA as function of retinal eccentricity in a group of eight healthy subjects. These measurements allowed us to decide whether the patients' DVA could be predicted solely on the basis of the retinal position error prevailing by deciding if the patients' thresholds would fall within the normal range after correcting for their (increased) position errors. In this set of experiments, a white circle (diameter 0.2°) served as the pursuit target, which was spatially separated from the Landolt optotype moving at the same velocity (Fig. 1C
). By varying the vertical distance between the pursuit target and the Landolt ring in 1° steps (1°, 2° and 3°), acuity thresholds were measured for different retinal eccentricities and four target velocities (0°, 4°, 8° and 12°/s). Experiments and analyses were performed as described for the standard DVA experiments.
Discrimination of position steps
In addition to the DVA measurements, one further test was applied in order to assess the visual discrimination of moving objects. In this second task subjects were instructed to track a small diamond (size 10' x 10', local contrast 0.1 compared with the otherwise dark screen) which moved horizontally at a constant velocity (Fig. 1D). After a variable time interval (450–1000 ms) the target jumped upwards or downwards from one frame to the next (i.e. within 14 ms) and continued moving horizontally (total ramp length = 8°). The size and direction of the vertical target step were varied. Subjects were asked to indicate whether the target displacement was upwards or downwards. Thresholds, defined as the step size resulting in 75% correct responses, were again determined on the basis of at least 50 trials controlled by an adaptive staircase procedure that started from a position step of 16.7'. In order to exclude the influence of relative distance or relative motion between the stimulus and stationary points of reference, such as the monitor frame, these experiments were carried out in complete darkness. Stimuli were again observed under binocular viewing at a distance of 225 cm. Target velocity was varied from 4° to 12°/s in steps of 2°/s in the control group and in steps of 4°/s in the patients.
Recording and analysis of eye movements
SVA and DVA
In order to correlate the acuity thresholds with the oculomotor performance, eye movements were recorded in each individual trial using an infrared reflection system (CCD eyetracker, AmTech®, Weinheim, Germany). Eye records were sampled at a rate of 72 Hz, i.e. they were synchronized with the monitor display. Head movements were minimized by means of a bite bar.
The records were stored on the workstation that also controlled the presentation of the stimuli, and were analysed off-line for the period of Landolt C presentation (Fig. 2). Prior to analysis, the eye recordings were filtered at 15.9 Hz. For individual measurements, three different measures were determined which have been assumed to be crucial for visual acuity (e.g. Ludvigh, 1949; Brown, 1972): (i) the velocity of the movement of the target image on the retina; (ii) the retinal position of the target image relative to the fovea; and (iii) the number of saccades. Based on the analysis of each single trial, the mean retinal image slip velocity was obtained from the difference between target velocity given and eye velocity for periods of saccade-free smooth pursuit. The retinal position error was given by the mean distance between target and eye position. Distances were first calculated for all sample points, separately, by vectorially adding horizontal and vertical position errors, and they were then averaged for the given measurement. Saccades were detected by visual inspection of the eye records, counted for all trials, and were expressed as the mean number (frequency) of saccades during one Landolt presentation (250 ms).
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Discrimination of position steps
In the experiments on the detection of vertical position steps, eye movements were recorded in the same way as specified for the Landolt measurements. The analysis of the records was slightly modified in view of the facts that the event to be detected occurred at just one point in time and that the target step itself introduced an increase in retinal position error. For this reason, the analysis of position errors was restricted to the final sample point before the position step occurred. Pursuit and retinal image slip velocities were estimated for a period of time subtending 100 ms before and after the position step.
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Results |
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SVA and DVA in control subjects
In our normal subjects, visual acuity did not depend on the different Landolt velocities tested (Fig. 3B
, upper left panel; Fig. 4). Although there was a slight tendency for acuity thresholds to be higher with higher target velocity (e.g. 0.70' under stationary fixation compared with 0.83' for the 14°/s condition), a one-way analysis of variance (ANOVA) did not reveal a statistically significant effect of the factor Landolt velocity [F(7,152) = 2.0; P = 0.06]. The analysis of eye movements suggested that this excellent resolution of moving optotypes was the direct consequence of precise pursuit eye movements. Specifically, the group means of pursuit gain (pursuit velocity/target velocity) were >0.88 for all speeds, resulting in only minor retinal image slip velocities that peaked at 1.12°/s (14°/s condition; Fig. 3B, upper right panel). As a consequence of fairly effective pursuit eye movements, catch-up saccades were rarely observed in the control subjects, only one saccade occurring for, on average, every 14 Landolt presentations (14°/s; frequency of saccades = 0.069/250 ms; Fig. 3B, lower left panel). Both the retinal velocity of the Landolt image [F(7,152) = 9.9; P < 0.001] and the frequency of saccades [F(7,152) = 5.4; P < 0.001] depended significantly on target velocity, with higher values for higher velocities, suggesting that the image of targets that moved at higher velocities tended to slide off the fovea and had to be recaptured by means of small catch-up saccades (Fig. 3B). The resulting retinal position errors depicted in Fig. 3B (lower right panel) show that smooth pursuit supplemented by catch-up saccades allowed for foveation of the Landolt image for all velocities: even the highest error observed (0.51°, 14°/s condition) was small enough to keep the image inside the foveal area believed to provide the highest acuity (e.g. Millodot, 1972). Despite the fact that comparably small retinal position errors were measured for all conditions, they increased significantly with target velocity [F(7,152) = 4.5; P < 0.001].
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SVA and DVA in patients with catch-up saccades
All patients exhibiting catch-up saccades (n = 9) showed the same principal pattern of results, exemplified in Fig. 3
for an individual patient, a 20-year-old female suffering from cerebellar degeneration (ADCA I). Figure 3A shows samples of her pursuit for two velocities of target movement, 8°/s and 12°/s. As can be seen from the almost linear rise in retinal image slip with increasing target velocity (Fig. 3B, upper right panel), this patient was unable to perform pursuit eye movements exceeding 4°/s, resulting in retinal image shifts of up to 10°/s in the 14°/s condition. The increasing mismatch between target and pursuit velocity was paralleled by an increase in the frequency of corrective saccades, which saturated in this patient at a probability of 0.8 that a saccade occurred during the 250 ms of the Landolt presentation (Fig. 3B, lower left panel). Concordant with the obvious limitation of the number of corrective saccades that allowed only brief foveation periods, the resulting retinal position error increased with increasing target velocity (Fig. 3B, lower right panel). Most importantly, the insufficiency of pursuit eye movements was mirrored by a dramatic deterioration of the DVA, thresholds increasing to more than threefold compared with the control group for the 14°/s condition (Fig. 3B, upper left panel).
The group results for the patients clearly confirmed the strong dependency of DVA on target velocity by showing a loss of visual acuity that increased with target velocity (Fig. 4, upper left panel). This impression was supported by a two-way ANOVA with the factors group and target velocity, which gave significant main effects for both factors [velocity: F(4,129) = 10.97; P < 0.001; group: F(1,129) = 108.2; P < 0.001]. A highly significant interaction of the two factors [F(4,129) = 6.94; P < 0.001] reflected the fact that the loss of DVA in patients relative to controls increased with target velocity. Also evident in Fig. 4 is the marked influence of Landolt velocity on the frequency of saccades, retinal position error and retinal image slip velocity in the group of patients, values for each of these variables being highly significantly different from the corresponding values for the control subjects (P < 0.001). As can be seen from Fig. 4 (upper left), the mean static acuity of the group of patients was slightly inferior to that of the control subjects. When group analysis was restricted to those patients who showed static acuity thresholds within the normal range (means plus 2 SD derived from the control data), we observed the same statistically highly significant effects.
The fact that the decline in visual acuity coincided with the insufficiency of the pursuit response of patients suggested that the visual impairment was the direct consequence of the oculomotor deficit rather than a consequence of cognitive deficits or a possible handicap in the use of the keys due to the ataxia of the upper limbs that was present in most of the patients. This conclusion is supported by two patients who suffered from an asymmetrical cerebellar lesion (right cerebellar medulloblastoma and left cerebellar arteriovenous malformation, respectively). As has been noted in recent years, unilateral cerebellar lesions can result in an ipsiversive pursuit deficit while pursuit to the contralesional side remains intact (e.g. Straube et al., 1997). The same asymmetry in pursuit response was noted in both patients (for an example see Fig. 5). In these two patients, the ipsiversive pursuit deficit was paralleled by a purely ipsiversive reduction in DVA (Fig. 5B, upper left panel) as well as purely ipsiversive increases in retinal image slip velocity, retinal position error and the frequency of saccades (Fig. 5B, upper right, lower left and lower right respectively). On the other hand, the acuity thresholds for the unimpaired contraversive pursuit were within the normal range.
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SVA and DVA in patients with square-wave jerks
The pattern of visual disturbances seen in patients with square-wave jerks differed from that of the patients showing catch-up saccades. Figure 6
reveals that the pursuit velocity in the two patients with square-wave jerks matched the target velocity fairly well, as indicated by the small retinal image shifts observed under all conditions (Fig. 6B, upper right panel). Despite normal pursuit velocities, retinal position errors were increased (Fig. 6B, lower right panel) due to involuntary saccades, which were present during both stationary fixation (Fig. 6A, upper panel) and ocular tracking (Fig. 6A, lower panel). The fact that the probability of these square-wave jerks was the same for the different target velocities (Fig. 6B, lower left panel) translated into a loss of visual acuity that did not reveal any convincing dependency on target velocity. Rather, this loss was apparent as an almost constant offset that separated the patients' thresholds from those of controls (Fig. 6B, left upper panel).
SVA and DVA as functions of retinal position error
The results of the series of experiments testing dynamic visual acuity as function of retinal position error in a group of normal control subjects are summarized in Fig. 7 in the form of a three-dimensional plot of acuity threshold as a function of position error and target velocity. The plot shows a linear increase in acuity threshold with increasing retinal eccentricity independent of target velocity. A two-way ANOVA with the factors target velocity and vertical distance between pursuit target and Landolt optotype proved that thresholds depended exclusively on retinal position [F(3,151) =388.6; P < 0.001]. On the other hand, neither the effect of Landolt velocity (F = 1.6; P = 0.19) nor the interaction of the two factors was significant [F(9,151) = 0.51; P = 0.86]. Two further two-way ANOVAs with the factors target velocity and vertical distance between pursuit target and Landolt ring confirmed that the increase in acuity thresholds was indeed due to the increased position error: neither retinal image slip nor the frequency of saccades was significantly different for the different retinal eccentricities tested [retinal image slip: F(3,151) = 0.35; P = 0.78; frequency of saccades: F(3,151) = 2.3; P = 0.08].
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For the comparison of the patients' results with those of normal controls, the data were analysed separately for the different velocities (4°, 8° and 12°/s). The DVA thresholds of controls were plotted as a function of retinal position error and subjected to linear regression analysis (Fig. 8
). A normal range was then defined by two borderlines running parallel to the regression line at a distance equalling two standard deviations. The standard deviation of the sample was based on the residuals obtained after subtraction of the linear estimate of the dependence of acuity as a function of retinal position error. As shown in Fig. 8 for the 12°/s target velocity, DVA thresholds of seven of the 11 patients fell within the distribution of the control data, i.e. their DVAs were fully explained by the retinal position error. This subgroup of patients was similar for the 8°/s condition (eight out of 11 patients) but larger for the 4°/s condition (10 out of 11 patients), the later due to the fact that many of the patients showed normal DVA thresholds for the lower velocities (Fig. 4). Considering only the significantly increased DVA thresholds of the patients (the normal range being defined by means of the control group plus 2 SD), 17 (68%) of the 25 pathological DVA thresholds (pooled over target velocities of 4°, 8° and 12°/s) could be sufficiently explained by an increase in retinal position error.
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As can be seen in Fig. 8
, dynamic visual acuity in a minority of patients (n = 4, 12°/s condition) fell outside the range predicted by the retinal position error. Unpaired t tests, which compared mean retinal image slip, static visual acuities and frequency of saccades of this subgroup of patients with those of the other patients falling within the range predicted by the retinal position error, revealed higher retinal image slip velocities (P < 0.01) and slightly inferior static visual acuities (P = 0.04) in the first group but did not show a significant difference in the frequency of saccades between groups (P = 0.14). Specifically, the three patients who most markedly fell outside the range predicted revealed the highest retinal image slip velocities (8.1°, 7.4° and 6.5°/s, respectively), clearly surpassing the level beyond which acuity is believed to be degraded. Conversely, only one of the patients whose DVA fell within the predicted range surpassed this level marginally (4.2°/s). In summary, in patients whose retinal image slip stayed below 4°/s, the increase in the mean retinal position error alone was able to account for the DVA decrease relative to the controls. In the other patients, retinal image slip as well as retinal position error probably contributed to the overall DVA losses. Furthermore, deficient SVAs in some of these patients may suggest additional impairment of the afferent visual pathway.
Discrimination of position steps
The results of the tests assessing the sensitivity for vertical position steps of a pursuit target moving horizontally very much resembled those of the Landolt measurements. Again, in the controls, thresholds did not depend on target velocity [e.g. 2.25' (4°/s) compared with 2.38' (12°/s); non-significant ANOVA with the factor target velocity: F(4,50) = 0.4; P = 0.80] (Fig. 9). Mean retinal position errors were of the order of the foveal radius with a maximum of 0.50° for the 12°/s condition (Fig. 9C). In contrast, the thresholds of patients with catch-up saccades strongly depended on target velocity, with increasing values for higher velocities [F(2,24) = 12.54; P < 0.001] and were paralleled by increasing retinal image slip velocities (F = 11.15; P < 0.001) and position errors (F = 5.325; P = 0.012) (Fig. 9A–C). Patients with square-wave jerks in turn revealed thresholds and retinal position errors that were more or less invariant for the different velocities but significantly higher than those of the control group (Fig. 9A and C). This impression was supported by a two-way ANOVA with the factors target velocity and group (controls versus patients with square-wave jerks), which revealed no significant effect of target velocity on the thresholds [F(2,33) = 1.6; P = 0.21] but a highly significant difference in thresholds between groups (F = 83.26; P < 0.001).
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Discussion |
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It has usually been taken for granted that the evolution of smooth pursuit eye movements in foveate animals was promoted by an advantage in the visual analysis of moving objects due to continuous foveal stabilization of the retinal object image. Although this is plausible, there have been few attempts to rigorously demonstrate such benefits resulting from foveal pursuit. The present study clearly demonstrates that this assumption is indeed justified. Two main results emphasize the important perceptual role of smooth pursuit eye movements: (i) the invariance of acuity thresholds with respect to target velocity observed in the control group; and (ii) the deterioration of acuity thresholds in patients suffering from pursuit disorders.
The first observation is in conflict with a number of other studies in that they point towards a profound dependency of DVA on the velocity of objects to be tracked by eye movements (Ludvigh and Miller, 1958; Long and Riggs, 1991; Long and Homolka, 1992; Geer and Robertson, 1993). The most likely explanation for this discrepancy lies in the fact that, in the studies cited, thresholds were measured for stimuli moving at velocities of up to 90 (150)°/s while the range of velocities tested here was restricted to a maximum of 14°/s. Apart from the fact that object velocity in some of these studies clearly exceeded the physiological limit of the pursuit system (e.g. Robinson, 1965), thresholds were usually not measured for periods of steady-state pursuit but rather for pursuit initiation due to presentation times which were set shorter than pursuit latencies are. Thus, instead of determining acuity threshold as a function of pursuit performance, tests were done under conditions varying grossly with respect to the eye movements elicited. Unfortunately, these studies do not allow more detailed discussion of the underlying factors that might have given rise to the DVA decrease observed for higher target velocities, as eye movements were not recorded. As far as we can tell in view of our own results, efficient pursuit eye movements allow the resolution of moving objects which is as excellent as that under stationary fixation, at least for velocities of up to 14°/s. The analysis of eye movements suggests that this resolution is indeed due to continuous stabilization of the object image on the fovea, as indicated by minor retinal image shifts and retinal position errors in the order of the foveal radius.
This investigation of the deterioration of DVA in patients suffering from pursuit disorders adds to a number of studies evaluating the consequences of disturbances of different types of compensatory eye movements for visual perception. Specifically, deficits in visual acuity have been shown to result from impaired vestibulo-ocular (Demer et al., 1994) or otolith-ocular reflexes (Lempert et al., 1997) and from abnormalities of visual fixation such as congenital nystagmus (Bedell et al., 1989). As far as we are aware, ours is the first study that directly demonstrates visual deficits as a consequence of impaired pursuit eye movements. The pattern of visual disturbances found depended on the characteristics of the underlying pursuit disturbance. Thus, the visual performance of patients with catch-up saccades was characterized by an increasing reduction in DVA with increasing target velocities. This finding suggests that such patients are considerably handicapped in everyday life when faced with object motion that exceeds their individual pursuit capacity. In contrast, the visual performance of the two patients showing square-wave jerks, although worse than that of controls, did not depend on target velocity. Since the occurrence of involuntary saccades was more or less the same for periods of fixation and periods of smooth pursuit, the resulting visual disturbance is probably present all the time and is at least approximately independent of the type of eye movement carried out.
In both groups of patients, the increased retinal position error appeared to be the crucial factor responsible for the visual deficits. This is indicated by the fact that the majority of the pathological results (68%) could be explained solely on account of an increase in retinal position error. A similar interpretation has been suggested for the loss in visual acuity observed in patients with congenital nystagmus: acuity is improved when the eyes are held in the null position, i.e. the orbital position at which the nystagmus is minimized, allowing more precise and longer foveation periods (Dell'Osso and Daroff, 1975; Bedell et al., 1989; Dell'Osso et al., 1992; Sheth et al., 1995). Those patients who revealed acuity thresholds higher than the thresholds of controls with comparable retinal position errors showed the highest retinal image shift velocities within the patient group. Specifically, retinal image velocities in most of these patients surpassed the limit beyond which visual acuity has been shown to be impaired in normal subjects during fixation (4°/s; Westheimer and McKee, 1975). In contrast, only one of the patients whose DVA fell within the range predicted by the retinal position error slightly surpassed the 4°/s level of retinal image motion. These findings suggest that the DVA can be predicted on the basis of retinal position alone as long as retinal image shifts are smaller than 4°/s. Conversely, higher retinal image slip velocities contribute to the overall visual impairment in patients with markedly reduced pursuit gains. Saccadic suppression or saccadic omission does not seem to make a specific contribution to the total DVA loss observed, since the frequency of saccades in patients falling outside the range predicted by retinal position was not significantly different from that found in the other patients. Finally, we cannot exclude the possibility that some of the patients whose DVA thresholds fell outside the range of DVAs predicted by the retinal position errors suffered from additional deficits of the afferent visual pathway. The reason is that the static visual acuities of some of these patients were slightly worse than those of the rest of the patients.
We suspect that the deficits in the visual analysis of moving objects reflected by the marked elevation of DVA thresholds in our patients are of the utmost significance for everyday life. The reason is that performance on many activities, such as guiding a vehicle and athletics, has been shown to correlate significantly with DVA (Shinar and Schieber, 1991; Ishigaki and Miyao, 1993). Hence, pursuit disturbances recognized on physical examination should not only be used in order to identify and localize putative CNS lesions but should also be evaluated with respect to the patients' visual performance under everyday conditions.
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References |
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Received February 1, 1999. Accepted March 12, 1999.
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