July 2008
Volume 49, Issue 7
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Eye Movements, Strabismus, Amblyopia and Neuro-ophthalmology  |   July 2008
Task-Induced Stress and Motivation Decrease Foveation-Period Durations in Infantile Nystagmus Syndrome
Author Affiliations
  • Kwang M. Cham
    From the Department of Optometry and Vision Sciences, University of Melbourne, Melbourne, Victoria, Australia.
  • Andrew J. Anderson
    From the Department of Optometry and Vision Sciences, University of Melbourne, Melbourne, Victoria, Australia.
  • Larry A. Abel
    From the Department of Optometry and Vision Sciences, University of Melbourne, Melbourne, Victoria, Australia.
Investigative Ophthalmology & Visual Science July 2008, Vol.49, 2977-2984. doi:10.1167/iovs.07-1626
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      Kwang M. Cham, Andrew J. Anderson, Larry A. Abel; Task-Induced Stress and Motivation Decrease Foveation-Period Durations in Infantile Nystagmus Syndrome. Invest. Ophthalmol. Vis. Sci. 2008;49(7):2977-2984. doi: 10.1167/iovs.07-1626.

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      © 2016 Association for Research in Vision and Ophthalmology.

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Abstract

purpose. To investigate the effect of visual demand, task-related physiological stress, and motivation on the nystagmus waveform of 19 subjects with infantile nystagmus syndrome (INS).

methods. Subjects viewed a Landolt C of varying orientation and size, and indicated its orientation via arrow keys on a keyboard. Mental arithmetic was performed in conjunction with the visual task. Subjects then underwent a reward-penalty paradigm. Eye movements and heart rates were recorded during all experiments.

results. Task-related physiological stress and motivation were reflected in an increase in heart rate and led to an increase in the amplitude, frequency, and intensity of the nystagmus waveform and a decrease in foveation-period durations. Changes in heart rate did not correlate with changes in waveform parameters for all experiments.

conclusions. The results show, for the first time, the negative impact of task-induced stress and/or motivation on the characteristics of INS. This finding has important implications for individuals with INS, because stress may arise in everyday situations, such as driving or when undertaking an examination.

Infantile nystagmus syndrome 1 (INS) is an involuntary ocular motor oscillation that manifests at or shortly after birth 2 —or, rarely, in later life 3 —and persists throughout life. 4 5 INS possesses certain characteristics that are individually imprecise but jointly, highly diagnostic. One is the often-stated observation that INS increases with fixation effort, fatigue, attention, mental concentration, and psychological factors (such as stress and anxiety). 6 7 8 However, only a few studies 6 7 (Wiggins et al. IOVS 2006:47:ARVO E-Abstract 2503) have been undertaken to assess and quantify the influence of psychological states on INS, with contradictory results. 
Abadi and Dickinson 8 found that fixation effort qualitatively increased INS in eye-movement recordings, but no quantitative analyses were performed. In addition, the fixation target was a light-emitting diode (LED) that required little fixation effort. Tkalcevic and Abel 6 used a range of optotype targets and observed that INS parameters (amplitude, frequency, intensity, and foveation-period duration) did not worsen when a task was visually demanding possibly due to subjects lacking any motivational drive to perform. Nonetheless, they might have failed to induce maximum visual demand for several reasons, including unlimited viewing time of the optotypes. Also, practice trials were performed, which may have reduced stress as subjects became more familiar with the procedures. Finally, no physiological correlate of stress was used to monitor the subjects during testing. 
Wiggins et al. (IOVS 2006:47:ARVO E-Abstract 2503) showed an increase in nystagmus intensity and skin conductance—an established indicator of physiological stress 9 —when INS subjects were stressed by an 88-dB siren. However, the foveation-period duration, which is a better predictor of visual performance than intensity, 4 10 was not reported. In addition, it would be preferable to induce stress visually or mentally rather than via an unpleasant auditory stimulus, as this would more closely parallel the everyday conditions that subjects with INS typically encounter when stressed. In a later study, 7 it was reported that increased visual demand leads to a reduction in the amplitude, frequency, and intensity of the nystagmus waveform, as well as prolonged foveation-period durations. However, task demand may have been reduced by having subjects perform the visual task in their null zones and with correction, and by not restricting viewing time. No measure of stress/arousal was used during testing. Nonetheless, both studies 6 7 are in agreement that visual demand per se does not worsen INS. In the present study, we addressed several limitations of previous studies and investigated the effect of visual demand, task-induced physiological stress, and motivation on the nystagmus waveform of INS subjects. 
Methods
Our study conformed to the Declaration of Helsinki and was approved by the Human Research Ethics Committee of the University of Melbourne, and all subjects gave written informed consent before participating. Eye-movement recordings were performed in 19 subjects with INS (8 men and 11 women, mean age 33 ± 13.2 years). The diagnosis of INS was primarily made by the referring ophthalmologist and was verified later on the basis of clinical examination and eye-movement recording analysis performed by the investigators. Sixteen subjects were classified as idiopathic, and three had associated visual disorders: One had retinitis pigmentosa, one had albinism, and one had congenital cataract and glaucoma. The subjects were free of medications and drugs. They were nonsmokers and were advised not to consume alcohol or coffee and to abstain from vigorous exercise at least 4 hours before the session. All subjects were naive with respect to the purpose of the study. Table 1summarizes some of the relevant characteristics of the subjects. Pilot studies on normal observers ensured that the experimental paradigms used in the present study were significantly stressful or motivating to induce a significant change in heart rate. 
Eye movements were recorded with a binocular infrared oculographic system (Microguide Corp., Downers Grove, IL). 11 The bandwidth was DC-100 Hz, and the sensitivity of the system was 1 min arc. Testing was performed at 1.5 m without correction and in darkness. Ten nonstrabismic subjects performed the task binocularly. The remaining nine subjects had manifest strabismus and thus undertook the experiments monocularly, with the nonstrabismic eye as the viewing eye during recordings. Head movement was minimized by cheek restraints, with residual movement monitored by a laser pointer strapped to the back of the head that then projected to a series of concentric circles, spaced approximately 1° apart at 1.85 m. The cheek restraints allowed the subjects to respond verbally without disrupting the eye-movement recordings. Eye movements were calibrated by consecutively presenting LEDs from −20° to +20° mounted on a 1.6-m arc in radius at 1.6 m. Fixation data were scaled with a best-fit regression line. 
We selected heart rate as a physiological variable related to stress/motivation in this study, because of the ready availability of instrumentation and the ease of monitoring by noninvasive means. Heart-rate recordings were obtained with an amplifier (model 801; Neuroscientific Corp, Farmingdale, NY) that has a gain of 1000 and bandwidth of 1 to 300 Hz. Gold-capped surface electrodes with electrode cream were secured on both upper forearms with the reference electrode on the right ear. Eye position and heart-rate signals were digitized at 1000 Hz with 12-bit resolution. A baseline heart rate was obtained during the calibration trial. Subsequently, the heart rates of each subject were measured in conjunction with the eye-movement recordings for all experiments. 
The present study consisted of three parts, namely the unrestricted-viewing, restricted-viewing, and the reward-manipulation tasks. Baseline waveform parameters were obtained by averaging over 15 s of primary gaze position during calibration at 1.6 m. In the unrestricted-viewing task, logMAR equivalent Landolt Cs of various orientations (up, down, left, and right) and angular size (ranging from −0.1 to 1.2 logMAR in 0.1 steps) were presented individually in the center of a 19-in. flat-screen LCD monitor of 73-cd/m2 background luminance. Each subject was instructed to press one of four arrow keys on a computer keyboard that corresponded to the orientation of the Landolt C. The viewing time for each optotype was unlimited, though prompt responses were encouraged. Resolution thresholds were determined by a one-up/two-down staircase presentation with asymmetric step sizes (0.2-logMAR step decrement and 0.1-logMAR step increment). Landolt Cs were presented in descending order, starting with the largest optotype size (logMAR 1.2). Orientation was randomized by the computer. The trial was completed when four reversals were obtained. If the subject failed to see the largest optotype or detected the smallest optotype presented, testing was terminated. 
In the restricted-viewing task, the experimental protocols were largely the same as for the unrestricted-viewing task. However, the Landolt C targets were presented for a limited time and were followed by a 100-ms visual mask, with a central red fixation cross, to eliminate any aftereffects. The subject could respond only when the visual mask disappeared, leaving the fixation cross on the screen. To increase stress, the subjects were informed only about the nature of the visual task and how to respond using the arrow keys, but not when to respond (unclear task difficulty). After several trials, if the subjects still failed to work out the correct sequence in responding to the optotypes, further instructions were given. As testing continued, stimulus presentation time decreased (Table 2) . If the subject failed to respond within one second, it was considered a miss, and the same-sized optotype, but of random orientation, was then presented. Mental arithmetic (serial subtraction of 17 from 700) with verbalization was performed in conjunction with the visual task. Annoying verbal prompts (e.g., “please respond now, you are taking too much time”) were delivered when the subject exceeded the allocated 5-second response time for the mental arithmetic task. The trial ended when 10 reversals were obtained or when the largest/smallest optotype was detected. 
As our purpose was to increase the visual demand by making the task as stressful as possible, no practice runs were conducted. In addition, all subjects performed the restricted-viewing task first before undertaking the unrestricted-viewing task. We chose not to randomize the task order, as increased familiarity (analogous to giving practice runs) with the task could reduce the task-induced stress. The increase in reversals in the restricted-viewing task (10 vs. 4) was to keep the subjects at a near-threshold letter size for an extended period. 
Subsequently, the reward-manipulation task was performed. The experimental protocols were the same as for the restricted-viewing task, except that specific instructions were delivered to the subjects, no mental arithmetic was performed, and a reward/penalty paradigm was introduced. Each subject was told that $0.50 would be rewarded for correctly detecting two optotypes in a row. Incorrect responses would be penalized by a deduction of $1.00 from the amount earned. No punishment was given for missed targets—that is, failing to respond to the presented optotype within 1 second. Auditory feedback was provided to inform the subjects if they had responded correctly or made an error. Contrary to this deceptive instruction, a fixed reward of $20.00 was given to all subjects at the end of the experiment, regardless of performance. We allowed a 2-minute interval between all three tasks. 
We analyzed eye-movement data for changes in the type and parameters of the waveform, in particular the foveation-period durations, during all three experiments. Any differences in heart rate were also measured. We defined foveation-period durations in which eye velocity was ≤4 °/s and eye position was inferred to be ±2° from the fixation point from cycle to cycle. This ±2° position criterion was less stringent than the typical ±0.5° position setting used in previous studies, to allow for albino subjects who lack a functional fovea. 6 12 13 14 15 Indeed, some studies did not use any position criterion when examining foveation-period durations in INS subjects; only a velocity criterion was used. 16 17 18 We manually estimated an average fixation position by placing a line through the beginning of as many slow phases as possible in a given fixation interval to serve as the basis for foveation calculations. Blinks and nonfixation points (e.g., times when the subject momentarily looked away from the computer screen or appeared drowsy) were excluded from analysis by visual inspection. We also rejected artifacts in the electrocardiogram waveforms (e.g., spikes due to hand movement). Subject N did not participate in the reward-manipulation task. 
Results
We compared the heart rate and waveform parameters among the baseline (from Table 1 ), unrestricted-viewing, and restricted-viewing tasks, with 1-way ANOVA with repeated measures. Unlike visual acuity, all other waveform parameters and heart rate differed significantly (Fig. 1)
For the reward-manipulation task, paired t-test also illustrated significant changes in heart rate and waveform parameters when compared with baseline. Again, visual acuity was not significantly altered (Fig. 2)
When the heart rates and waveform parameters were examined during minimum (largest optotype read) and maximum (smallest optotype read) visual demand, significant differences were found with paired t-tests only for the restricted-viewing task, not for the unrestricted-viewing or the reward-manipulation tasks (Table 3)
The effects of increased visual demand on INS parameters (i.e., decreased—that is, improved—amplitude, frequency and, hence, intensity, as well as decreased—thus, deteriorated—foveation-period durations) and increased heart rate during the restricted-viewing task are shown for all subjects in Table 4 , indicating considerable intersubject variability. When compared between the restricted-viewing and the reward-manipulation tasks, heart rate increased significantly more in the restricted-viewing task (paired t-test: t = 3.64, P = 0.002). Figure 3illustrates the INS waveform of a subject at minimum and maximum visual demand during the restricted-viewing task. 
A Pearson correlation was performed to investigate the relationship between changes in heart rate and changes in waveform parameters by obtaining the difference between them when responding to the smallest optotypes during the unrestricted- and restricted-viewing tasks. The correlation was performed on a subject-by-subject basis using within-subject data. Changes in heart rate did not correlate with changes in waveform parameters (amplitude, r 2 = 0.001, P = 0.9; frequency, r 2 = 0.01, P = 0.7; intensity, r 2 = 0.0003, P = 1.0; and foveation-period durations, r 2 = 0.0001, P = 0.9). 
When task performance was evaluated (change from baseline heart rate versus correct response of mental arithmetic or skipped optotypes), Pearson correlation was again nonsignificant for the restricted-viewing (mental arithmetic, r 2 = 0.02, P = 0.61; skipped optotypes, r 2 = 0.02, P = 0.61) and the reward-manipulation (skipped optotypes, r 2 = 0.0002, P = 0.96) tasks. Changes in direction and predominant type of waveform were noted in seven subjects for all three tasks (Table 5)
Discussion
Our study is the first to provide evidence for the negative impact of stress and/or motivation on the characteristics of the nystagmus waveform. Task-induced physiological stress, as evident by an increased in heart rate during the restricted-viewing task, led to an increase in the amplitude, frequency, and intensity of the nystagmus waveform and decreased foveation-period durations. The results lend quantitative support to previous observations that INS increases with psychological factors (such as stress and anxiety) that affect visual performance. 6 7 8  
INS is also said to intensify with fixation effort. 8 10 In contrast, we found decreased INS intensity at maximum visual demand during the restricted-viewing task, consistent with Wiggins et al. 7 We failed to find any significant changes in waveform type at maximum visual demand, which would otherwise explain the observed inconsistencies in INS intensity. Such intensity changes are probably functionally less important than changes in the foveation-period duration, which are a better predictor and a more direct measure of visual performance in INS. 4 10  
The findings of decreased foveation-period durations at maximum visual demand in the restricted-viewing task in our study contradict earlier results by Tkalcevic and Abel, 6 who found no changes in the foveation-period duration of the nystagmus waveform, and of Wiggins et al., 7 who reported prolonged foveation-period durations. The cause of this discrepancy may be the failure of both studies to produce sufficient visual demand, as mentioned previously. This finding is supported by those for our unrestricted-viewing task (analogous to the task used in previous studies), which yielded no significant differences between minimum and maximum visual demands (i.e., largest versus smallest optotype). Hence, visual demand per se will exacerbate INS if the task is stressful enough. 
In the present study, foveation-period durations decreased significantly during the visual tasks, while visual acuity remained relatively unchanged. This result is in contrast with those in previous studies, 4 10 in which it was found that prolonged foveation-period durations enhance visual acuity in INS. Our study was not primarily designed to measure visual acuity but rather to produce a stressful visual environment by briefly presenting optotypes with slightly blurred edges. This unconventional visual acuity task might account for the increased variability (hence, nonsignificant) in visual acuity among the visual tasks. The infrared limbus eye tracker also precluded the use of patients’ spectacles for refractive error correction, thus further limiting our ability to evaluate best corrected visual acuity. 
We noted a change in fast-phase direction in two of our subjects with INS when they performed tasks other than baseline fixation. This suggests that stress and/or motivation may be added to factors such as smooth pursuit, choice of fixating eye and time in the aperiodic alternating nystagmus cycle, which are already known to shift the null position in INS. 
Investigators in previous studies 6 7 have proposed that the absence of rewards failed to motivate subjects, which may have influenced the findings. In the present study, we examined this assertion using the reward-manipulation paradigm. We observed that the reward/penalty paradigm produced a significant increase in nystagmus amplitude, frequency, intensity, and decreased foveation-period durations. Concurrently, heart rate increased, but not as much when compared with the restricted-viewing task. This finding reflects a greater motivational role compared to stress in the reward-manipulation task. We propose that the monetary reward increased motivation, and with its associated stress, increased INS significantly. 
We failed to find any significant correlation between changes in the nystagmus parameters and changes in heart rate when the subjects performed different visual tasks, suggesting that, although both observed changes co-vary with stress, they do not co-vary with each other. It is possible that the variability of the data in our study results in insufficient power to illustrate the correlation, or the nature of how both changes vary cannot be demonstrated by correlation, or both. The underlying functional relationship between stress, changes in heart rate, and changes in nystagmus parameters is unknown. Furthermore, recording heart rate over a short period is a coarse measure. Being an episodic rather than a continuous measure, heart rate is less robust and less sensitive than other measures, such as galvanic skin response, for the detection of subtle changes when monitoring the psychological state of the subjects. Future studies should include additional, more continuous measures to improve quantification of the psychological state of an individual. 
The mechanism by which INS waveform alters with changes in stress and/or arousal remains unknown. However, it is worth considering the interactions between the brain regions that modulate emotion/motivation and the slow eye-movement (SEM) control system, which has been postulated to give rise to INS. 10 19 The amygdala is a key structure in the neural basis of emotion, 20 playing an influential role in a vast range of behavior. 21 It forms an essential connection between brain areas that process sensory information (e.g., cerebral cortex) and brain regions for eliciting emotional and motivational responses (i.e., the hypothalamus, brain stem, and striatum). 22 Complex internal circuits allow the amygdala to link autonomic responses with specific behavior. 23 Another brain region of interest is the anterior cingulate cortex (ACC), which has been linked with attention and cognitive processes, 24 25 perhaps with a motivational role. 26 27 The ACC is also known to influence emotional and affective behavior. 20 Activity in the rostral and dorsal cingulate cortices correlates with (and predicts) cardiovascular and electrodermal arousal evoked by a range of cognitive, emotional, and motivational tasks. 9 28 29 The ACC shares reciprocal connections with the amygdala. Both structures are anatomically linked with the nucleus accumbens, 30 31 which mediates the motivational effects of emotionally significant stimuli. 32 33 The posterior part of the ACC, the posterior cingulate cortex (PCC), generates eye movements by early activation of frontal ocular motor areas and through direct projections to the brain stem. 34  
Reward expectancy modulates neural activity in various brain regions, including the dorsolateral prefrontal cortex (DLPFC), orbitofrontal cortex, ACC, premotor area, posterior parietal cortex, PCC, and caudate nucleus. 35 36 37 38 The basal ganglia are among the most significant structures in translating motivational context into ocular motor behavior. 36 Reward expectation can affect saccadic latency. 39 40 41 Changes in mental state (e.g., anxiety) have also been observed to increase the gain and slow-phase velocity of optokinetic nystagmus 42 43 and to prolong the time constant and increase the gain of the vestibulo-ocular reflex in normal subjects. 44 45  
In the present study, stress and/or motivation led to exacerbation of INS. Tkalcevic and Abel 6 suggested that the projections from ACC and amygdala to the brain stem could modulate activity in the vestibular nuclei, which had been postulated to be one of the structures implicated in the pathogenesis of INS. 46 Other possibly involved regions that contribute to smooth-pursuit eye movements include the subregion of the frontal eye fields, 47 supplementary eye field, 48 DLPFC, 49 anterior and posterior cingulate cortices, 50 basal ganglia, 51 and thalamus. 52 Of course, such sites are only relevant if INS is presumed to be an instability originating from the SEM control system. 10 19  
Conclusion
In summary, we have for the first time experimentally demonstrated the long-standing assertion that task-induced stress and/or motivation may have a negative impact on INS. They led to decreased foveation-period durations, which may affect the visual functions of INS subjects. Variations in these internal states may also lead to increased INS variability. This has important implications for individuals with INS, since stress may arise in everyday situations, such as driving or when undertaking an examination. We propose that the psychological status of individuals should be taken into consideration when they are either undergoing assessment of visual functions or when pre- and posttreatment modalities are compared. More precise manipulation of psychological behavior, such as attention, should help in extending our current knowledge of INS and how we can better assess and manage individuals with this condition. 
 
Table 1.
 
Clinical Data of 19 Subjects with INS
Table 1.
 
Clinical Data of 19 Subjects with INS
Subj. Age/ Sex Clinical Diagnosis Distance- Corrected VA Near Uncorrected VA Wave. Amp. (°) Freq. (Hz) Fov. (% ±2°, ≤4°/s) Null (°)
A 22 F Idiopathic 0.7 0.7 JL 1.79 3 66.67 0
B 22 F Idiopathic 0.4 0.5 JL 3.76 2.5 18.55 0
C 15 F Idiopathic 0.2 0.1 JLef 5.62 3 59.04 0
D 36 F Idiopathic 0.8 0.8 JL 7.06 5.5 12.4 15°
E 39 M Idiopathic 0.5 0.5 JL 1.71 3 57.75 ∼ −35°
F 30 M Idiopathic 0.8 0.8 JR 2.71 5.5 12.75 ∼35°
G 42 M Idiopathic 0.6 0.7 JL 2.1 4 45.43 20°
H 20 F Idiopathic 0.3 0.3 JL 1.07 3 40.92 15°
I 52 M Idiopathic 0.1 0.1 JLef 0.42 1.5 96.45 0
J 45 M Idiopathic 0 0 JRef 0.9 3.5 85.81 0
K 15 F Idiopathic 0.1 0.1 JRef 0.46 0.5 97.94 0
L 46 F Idiopathic 0.9 0.9 JR & RPC 2.2 4 25.93 10°
M 11 F Idiopathic 0 0 JLef 0.6 1 99.19 0
N 33 F Idiopathic 0.6 0.7 DJL 3.22 3 19.23 0
O 16 M Idiopathic 1.2 1.2 PPfs 4.56 2.5 39.73 0
P 13 M Idiopathic 0.2 0.3 JR 3.34 3 52.42 −15°
Q 41 F RP 1.5 1.5 JL 1.39 4 31.58 0
R 28 M Albinism 0.6 0.7 RPC 6.56 4 22.07 15°
S 29 F Cong. cataract & glaucoma 0.7 0.7 JL 3.53 3.5 40.28 0
Table 2.
 
Stimulus Presentation Time
Table 2.
 
Stimulus Presentation Time
LogMAR Acuity Presentation Period (s)
1.2 2.000
1.1 1.500
1.0 1.000
0.9 0.631
0.8 0.562
0.7 0.501
0.6 0.447
0.5 0.398
0.4 0.355
0.3 0.316
0.2 0.282
0.1 0.251
0.0 0.224
−0.1 0.200
Figure 1.
 
Differences in heart rate and waveform parameters among the baseline, unrestricted-, and restricted-viewing tasks. Pair-wise interactions were investigated with the Tukey multiple comparison test. ***P < 0.0001; **P < 0.001– 0.01; *P = 0.01–0.05. Repeated-measures 1-way ANOVA: heart rate: F 2,18 = 17.7, P < 0.0001; amplitude: F 2,18 = 4.0, P = 0.03; frequency: F 2,18 = 32.5, P < 0.0001; intensity: F 2,18 = 7.1, P = 0.003; foveation-period durations: F 2,18 = 25.8, P < 0.0001; and visual acuity: F 2,17 = 0.2, P = 0.86. Error bars, SE of mean.
Figure 1.
 
Differences in heart rate and waveform parameters among the baseline, unrestricted-, and restricted-viewing tasks. Pair-wise interactions were investigated with the Tukey multiple comparison test. ***P < 0.0001; **P < 0.001– 0.01; *P = 0.01–0.05. Repeated-measures 1-way ANOVA: heart rate: F 2,18 = 17.7, P < 0.0001; amplitude: F 2,18 = 4.0, P = 0.03; frequency: F 2,18 = 32.5, P < 0.0001; intensity: F 2,18 = 7.1, P = 0.003; foveation-period durations: F 2,18 = 25.8, P < 0.0001; and visual acuity: F 2,17 = 0.2, P = 0.86. Error bars, SE of mean.
Figure 2.
 
Differences in heart rate and waveform parameters between baseline and restricted-viewing tasks in the reward-manipulation paradigm. Paired t-test: heart rate: t = 2.2, P = 0.04; amplitude: t = 2.2, P = 0.04; frequency: t = 4.1, P = 0.001; intensity: t = 2.9, P = 0.01; foveation-period durations: t = 4.9, P = 0.0001; and visual acuity: t = 0.2, P = 0.8. Error bars, SE of mean.
Figure 2.
 
Differences in heart rate and waveform parameters between baseline and restricted-viewing tasks in the reward-manipulation paradigm. Paired t-test: heart rate: t = 2.2, P = 0.04; amplitude: t = 2.2, P = 0.04; frequency: t = 4.1, P = 0.001; intensity: t = 2.9, P = 0.01; foveation-period durations: t = 4.9, P = 0.0001; and visual acuity: t = 0.2, P = 0.8. Error bars, SE of mean.
Table 3.
 
Parameter Measurements for All Three Tasks
Table 3.
 
Parameter Measurements for All Three Tasks
Task Visual Effort Amplitude (deg) Frequency (Hz) Intensity (deg · Hz) Foveation Period Durations (% ±2°, ≤4°/s) Heart Rate (bpm)
Unrestricted viewing Min 4.4 ± 3.5 3.6 ± 1.4 16.8 ± 14.8 33.0 ± 32.3 76.6 ± 12.1
Max 3.6 ± 3.5, P = 0.11 3.9 ± 1.1, P = 0.11 14.9 ± 14.6, P = 0.29 32.0 ± 29.2, P = 0.61 75.8 ± 11.3, P = 0.64
Restricted viewing Min 5.8 ± 5.2 4.1 ± 1.2 23.2 ± 20.7 28.9 ± 31.7 76.4 ± 11.4
Max 4.0 ± 3.1, P = 0.02 3.7 ± 1.3, P = 0.03 15.7 ± 12.4, P = 0.02 26.4 ± 29.7, P = 0.003 79.1 ± 11.3, P = 0.04
Reward manipulation Min 3.6 ± 2.4 3.9 ± 1.2 14.6 ± 9.9 36.7 ± 32.1 75.4 ± 12.0
Max 3.1 ± 2.9, P = 0.26 3.6 ± 1.4, P = 0.35 12.9 ± 12.5, P = 0.33 35.6 ± 34.1, P = 0.60 75.4 ± 11.9, P = 0.97
Table 4.
 
Parameter Measurements during the Restricted-Viewing Task
Table 4.
 
Parameter Measurements during the Restricted-Viewing Task
Subj. Amplitude (deg) Frequency (Hz) Intensity (Deg · Hz) Foveation-Period Durations (% ±2 ≤4°/s) Heart Rate (bpm)
Min Max Min Max Min Max Min Max Min Max
A 1.91 0.91 3.00 3.00 5.73 2.73 66.99 63.92 87.19 80.47
B 6.29 5.13 3.50 4.50 22.02 23.09 6.40 3.89 81.10 77.56
C 16.61 11.47 3.50 3.00 58.14 34.41 13.18 14.08 75.21 87.81
D 15.77 8.42 5.00 5.00 78.85 42.10 0.90 3.54 71.31 86.80
E 3.74 2.37 4.00 4.00 14.96 9.48 19.43 12.89 58.10 58.80
F 3.67 3.49 6.25 6.00 22.94 20.94 8.11 5.82 90.25 90.27
G 3.62 3.83 5.50 6.00 19.91 22.98 6.78 6.17 82.19 84.07
H 9.85 3.14 4.00 3.00 39.40 9.42 20.48 14.78 88.82 96.66
I 2.58 0.04 3.00 2.50 7.74 0.10 85.84 84.39 62.70 64.29
J 1.39 1.38 6.00 4.50 8.34 6.21 46.38 48.55 85.71 82.35
K 1.53 0.99 3.00 2.00 4.59 1.99 85.98 82.32 81.00 83.75
L 2.57 2.12 5.00 5.00 12.85 10.60 15.52 17.88 70.45 71.43
M 1.27 1.29 2.50 1.00 3.18 1.29 90.79 75.84 95.65 94.29
N 10.81 5.60 4.00 3.50 43.24 19.60 1.95 0.18 77.41 86.64
O 15.10 7.97 3.00 3.50 45.30 27.90 6.70 8.21 64.00 65.85
P 2.85 3.18 2.50 2.00 7.13 6.36 51.00 42.35 54.70 57.59
Q 1.73 1.27 5.25 4.50 9.06 5.72 12.59 12.22 80.16 78.91
R 5.91 6.91 4.00 3.50 23.64 24.19 4.62 4.50 79.08 82.82
S 3.10 7.14 4.25 4.00 13.18 28.56 4.57 0.79 66.37 72.86
Mean ± SD 5.80 ± 5.19 4.03 ± 3.14 4.07 ± 1.15 3.71 ± 1.34 23.17 ± 20.72 15.67 ± 12.41 28.85 ± 31.66 26.44 ± 29.67 76.39 ± 11.38 79.12 ± 11.30
Figure 3.
 
(A) Recording of subject M who was attempting the 1.2 logMAR equivalent optotype. This optotype required minimum visual demand. Foveation-period durations were met 91% of the time. (B) Recording of the same subject who was attempting the −0.1 logMAR equivalent optotype. This optotype required maximum visual demand. Foveation-period durations were met 76% of the time. Horizontal line: fixation. The time origin is arbitrary.
Figure 3.
 
(A) Recording of subject M who was attempting the 1.2 logMAR equivalent optotype. This optotype required minimum visual demand. Foveation-period durations were met 91% of the time. (B) Recording of the same subject who was attempting the −0.1 logMAR equivalent optotype. This optotype required maximum visual demand. Foveation-period durations were met 76% of the time. Horizontal line: fixation. The time origin is arbitrary.
Table 5.
 
Direction and Waveform Type Changes in Seven Subjects
Table 5.
 
Direction and Waveform Type Changes in Seven Subjects
Subject Baseline Unrestricted Viewing Restricted Viewing Reward Manipulation
A JL JR DJR DJR
D JL JL JL & LPC JL & LPC
E JL PPfs & BDJL PPfs & BDJL PPfs & BDJL
J JRef JRef JR JR
K JRef JRef JR JRef
L JR & RPC JR JR JR & BDJR
P JR JR JR JL
The authors thank Louis Dell’Osso, MD, and Jonathan Jacobs, MD, for providing the modified Zoomtool software packages and Gari Clifford and Jos van der Geest, who wrote the manual off-line analysis program and the arrow-keys program used for subjects’ responses in the study, which were downloaded from the MathWorks (Natick, MA) user-contribution Web site under the general public license. 
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Figure 1.
 
Differences in heart rate and waveform parameters among the baseline, unrestricted-, and restricted-viewing tasks. Pair-wise interactions were investigated with the Tukey multiple comparison test. ***P < 0.0001; **P < 0.001– 0.01; *P = 0.01–0.05. Repeated-measures 1-way ANOVA: heart rate: F 2,18 = 17.7, P < 0.0001; amplitude: F 2,18 = 4.0, P = 0.03; frequency: F 2,18 = 32.5, P < 0.0001; intensity: F 2,18 = 7.1, P = 0.003; foveation-period durations: F 2,18 = 25.8, P < 0.0001; and visual acuity: F 2,17 = 0.2, P = 0.86. Error bars, SE of mean.
Figure 1.
 
Differences in heart rate and waveform parameters among the baseline, unrestricted-, and restricted-viewing tasks. Pair-wise interactions were investigated with the Tukey multiple comparison test. ***P < 0.0001; **P < 0.001– 0.01; *P = 0.01–0.05. Repeated-measures 1-way ANOVA: heart rate: F 2,18 = 17.7, P < 0.0001; amplitude: F 2,18 = 4.0, P = 0.03; frequency: F 2,18 = 32.5, P < 0.0001; intensity: F 2,18 = 7.1, P = 0.003; foveation-period durations: F 2,18 = 25.8, P < 0.0001; and visual acuity: F 2,17 = 0.2, P = 0.86. Error bars, SE of mean.
Figure 2.
 
Differences in heart rate and waveform parameters between baseline and restricted-viewing tasks in the reward-manipulation paradigm. Paired t-test: heart rate: t = 2.2, P = 0.04; amplitude: t = 2.2, P = 0.04; frequency: t = 4.1, P = 0.001; intensity: t = 2.9, P = 0.01; foveation-period durations: t = 4.9, P = 0.0001; and visual acuity: t = 0.2, P = 0.8. Error bars, SE of mean.
Figure 2.
 
Differences in heart rate and waveform parameters between baseline and restricted-viewing tasks in the reward-manipulation paradigm. Paired t-test: heart rate: t = 2.2, P = 0.04; amplitude: t = 2.2, P = 0.04; frequency: t = 4.1, P = 0.001; intensity: t = 2.9, P = 0.01; foveation-period durations: t = 4.9, P = 0.0001; and visual acuity: t = 0.2, P = 0.8. Error bars, SE of mean.
Figure 3.
 
(A) Recording of subject M who was attempting the 1.2 logMAR equivalent optotype. This optotype required minimum visual demand. Foveation-period durations were met 91% of the time. (B) Recording of the same subject who was attempting the −0.1 logMAR equivalent optotype. This optotype required maximum visual demand. Foveation-period durations were met 76% of the time. Horizontal line: fixation. The time origin is arbitrary.
Figure 3.
 
(A) Recording of subject M who was attempting the 1.2 logMAR equivalent optotype. This optotype required minimum visual demand. Foveation-period durations were met 91% of the time. (B) Recording of the same subject who was attempting the −0.1 logMAR equivalent optotype. This optotype required maximum visual demand. Foveation-period durations were met 76% of the time. Horizontal line: fixation. The time origin is arbitrary.
Table 1.
 
Clinical Data of 19 Subjects with INS
Table 1.
 
Clinical Data of 19 Subjects with INS
Subj. Age/ Sex Clinical Diagnosis Distance- Corrected VA Near Uncorrected VA Wave. Amp. (°) Freq. (Hz) Fov. (% ±2°, ≤4°/s) Null (°)
A 22 F Idiopathic 0.7 0.7 JL 1.79 3 66.67 0
B 22 F Idiopathic 0.4 0.5 JL 3.76 2.5 18.55 0
C 15 F Idiopathic 0.2 0.1 JLef 5.62 3 59.04 0
D 36 F Idiopathic 0.8 0.8 JL 7.06 5.5 12.4 15°
E 39 M Idiopathic 0.5 0.5 JL 1.71 3 57.75 ∼ −35°
F 30 M Idiopathic 0.8 0.8 JR 2.71 5.5 12.75 ∼35°
G 42 M Idiopathic 0.6 0.7 JL 2.1 4 45.43 20°
H 20 F Idiopathic 0.3 0.3 JL 1.07 3 40.92 15°
I 52 M Idiopathic 0.1 0.1 JLef 0.42 1.5 96.45 0
J 45 M Idiopathic 0 0 JRef 0.9 3.5 85.81 0
K 15 F Idiopathic 0.1 0.1 JRef 0.46 0.5 97.94 0
L 46 F Idiopathic 0.9 0.9 JR & RPC 2.2 4 25.93 10°
M 11 F Idiopathic 0 0 JLef 0.6 1 99.19 0
N 33 F Idiopathic 0.6 0.7 DJL 3.22 3 19.23 0
O 16 M Idiopathic 1.2 1.2 PPfs 4.56 2.5 39.73 0
P 13 M Idiopathic 0.2 0.3 JR 3.34 3 52.42 −15°
Q 41 F RP 1.5 1.5 JL 1.39 4 31.58 0
R 28 M Albinism 0.6 0.7 RPC 6.56 4 22.07 15°
S 29 F Cong. cataract & glaucoma 0.7 0.7 JL 3.53 3.5 40.28 0
Table 2.
 
Stimulus Presentation Time
Table 2.
 
Stimulus Presentation Time
LogMAR Acuity Presentation Period (s)
1.2 2.000
1.1 1.500
1.0 1.000
0.9 0.631
0.8 0.562
0.7 0.501
0.6 0.447
0.5 0.398
0.4 0.355
0.3 0.316
0.2 0.282
0.1 0.251
0.0 0.224
−0.1 0.200
Table 3.
 
Parameter Measurements for All Three Tasks
Table 3.
 
Parameter Measurements for All Three Tasks
Task Visual Effort Amplitude (deg) Frequency (Hz) Intensity (deg · Hz) Foveation Period Durations (% ±2°, ≤4°/s) Heart Rate (bpm)
Unrestricted viewing Min 4.4 ± 3.5 3.6 ± 1.4 16.8 ± 14.8 33.0 ± 32.3 76.6 ± 12.1
Max 3.6 ± 3.5, P = 0.11 3.9 ± 1.1, P = 0.11 14.9 ± 14.6, P = 0.29 32.0 ± 29.2, P = 0.61 75.8 ± 11.3, P = 0.64
Restricted viewing Min 5.8 ± 5.2 4.1 ± 1.2 23.2 ± 20.7 28.9 ± 31.7 76.4 ± 11.4
Max 4.0 ± 3.1, P = 0.02 3.7 ± 1.3, P = 0.03 15.7 ± 12.4, P = 0.02 26.4 ± 29.7, P = 0.003 79.1 ± 11.3, P = 0.04
Reward manipulation Min 3.6 ± 2.4 3.9 ± 1.2 14.6 ± 9.9 36.7 ± 32.1 75.4 ± 12.0
Max 3.1 ± 2.9, P = 0.26 3.6 ± 1.4, P = 0.35 12.9 ± 12.5, P = 0.33 35.6 ± 34.1, P = 0.60 75.4 ± 11.9, P = 0.97
Table 4.
 
Parameter Measurements during the Restricted-Viewing Task
Table 4.
 
Parameter Measurements during the Restricted-Viewing Task
Subj. Amplitude (deg) Frequency (Hz) Intensity (Deg · Hz) Foveation-Period Durations (% ±2 ≤4°/s) Heart Rate (bpm)
Min Max Min Max Min Max Min Max Min Max
A 1.91 0.91 3.00 3.00 5.73 2.73 66.99 63.92 87.19 80.47
B 6.29 5.13 3.50 4.50 22.02 23.09 6.40 3.89 81.10 77.56
C 16.61 11.47 3.50 3.00 58.14 34.41 13.18 14.08 75.21 87.81
D 15.77 8.42 5.00 5.00 78.85 42.10 0.90 3.54 71.31 86.80
E 3.74 2.37 4.00 4.00 14.96 9.48 19.43 12.89 58.10 58.80
F 3.67 3.49 6.25 6.00 22.94 20.94 8.11 5.82 90.25 90.27
G 3.62 3.83 5.50 6.00 19.91 22.98 6.78 6.17 82.19 84.07
H 9.85 3.14 4.00 3.00 39.40 9.42 20.48 14.78 88.82 96.66
I 2.58 0.04 3.00 2.50 7.74 0.10 85.84 84.39 62.70 64.29
J 1.39 1.38 6.00 4.50 8.34 6.21 46.38 48.55 85.71 82.35
K 1.53 0.99 3.00 2.00 4.59 1.99 85.98 82.32 81.00 83.75
L 2.57 2.12 5.00 5.00 12.85 10.60 15.52 17.88 70.45 71.43
M 1.27 1.29 2.50 1.00 3.18 1.29 90.79 75.84 95.65 94.29
N 10.81 5.60 4.00 3.50 43.24 19.60 1.95 0.18 77.41 86.64
O 15.10 7.97 3.00 3.50 45.30 27.90 6.70 8.21 64.00 65.85
P 2.85 3.18 2.50 2.00 7.13 6.36 51.00 42.35 54.70 57.59
Q 1.73 1.27 5.25 4.50 9.06 5.72 12.59 12.22 80.16 78.91
R 5.91 6.91 4.00 3.50 23.64 24.19 4.62 4.50 79.08 82.82
S 3.10 7.14 4.25 4.00 13.18 28.56 4.57 0.79 66.37 72.86
Mean ± SD 5.80 ± 5.19 4.03 ± 3.14 4.07 ± 1.15 3.71 ± 1.34 23.17 ± 20.72 15.67 ± 12.41 28.85 ± 31.66 26.44 ± 29.67 76.39 ± 11.38 79.12 ± 11.30
Table 5.
 
Direction and Waveform Type Changes in Seven Subjects
Table 5.
 
Direction and Waveform Type Changes in Seven Subjects
Subject Baseline Unrestricted Viewing Restricted Viewing Reward Manipulation
A JL JR DJR DJR
D JL JL JL & LPC JL & LPC
E JL PPfs & BDJL PPfs & BDJL PPfs & BDJL
J JRef JRef JR JR
K JRef JRef JR JRef
L JR & RPC JR JR JR & BDJR
P JR JR JR JL
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