Abstract
Background The risk of traumatic brain injury (TBI) and comorbid posttraumatic dizziness is elevated in military operational environments. Sleep deprivation is known to affect a service member's performance while deployed, although little is known about its effects on vestibular function. Recent findings suggest that moderate acceleration step rotational stimuli may elicit a heightened angular vestibulo-ocular reflex (aVOR) response relative to low-frequency sinusoidal stimuli after 26 hours of sleep deprivation. There is concern that a sleep deprivation–mediated elevation in aVOR function could confound detection of comorbid vestibular pathology in service members with TBI. The term “dynamic visual acuity” (DVA) refers to an individual's ability to see clearly during head movement and is a behavioral measure of aVOR function. The Dynamic Visual Acuity Test (DVAT) assesses gaze instability by measuring the difference between head-stationary and head-moving visual acuity.
Objective The purpose of this study was to investigate the effects of 26 hours of sleep deprivation on DVA as a surrogate for aVOR function.
Design This observational study utilized a repeated-measures design.
Methods Twenty soldiers with no history of vestibular insult or head trauma were assessed by means of the DVAT at angular head velocities of 120 to 180°/s. Active and passive yaw and pitch impulses were obtained before and after sleep deprivation.
Results Yaw DVA remained unchanged as the result of sleep deprivation. Active pitch DVA diminished by −0.005 LogMAR (down) and −0.055 LogMAR (up); passive pitch DVA was degraded by −0.06 LogMAR (down) and −0.045 LogMAR (up).
Limitations Sample homogeneity largely confounded accurate assessment of test-retest reliability in this study, resulting in intraclass correlation coefficients lower than those previously reported.
Conclusions Dynamic visual acuity testing in soldiers who are healthy revealed no change in gaze stability after rapid yaw impulses and subclinical changes in pitch DVA after sleep deprivation. Findings suggest that DVA is not affected by short-term sleep deprivation under clinical conditions.
The human vestibular system consists of a peripheral sensory apparatus, central processing centers, and efferent pathways that mediate numerous functional motor outputs.1 Among these, the angular vestibulo-ocular reflex (aVOR) maintains stable gaze (ie, eye position in space) by generating compensatory eye movement responses that are opposite in direction but equal in magnitude to head movement stimuli.2,3 Additionally, cortical vestibular processing centers within the insular and temporoparietal brain regions integrate vestibular, visual, and somatosensory signals constructing neural representations of the individual's environment to accurately guide behavior.1,3,4
A growing body of evidence supports an association between vestibular pathology and posttraumatic dizziness in service members who sustain mild traumatic brain injury (mTBI) in the deployed environment.2,5–7 According to official Department of Defense sources, more than 220,000 service members have been diagnosed with TBI within the last decade, leading some to describe this condition as the “signature injury” of modern conflicts.8–10 Epidemiological findings for a returning Brigade Combat Team indicated that 22.8% of soldiers in the unit had at least 1 clinician-confirmed TBI over the course of a year-long deployment. Among symptoms experienced in this subgroup of injured personnel, posttraumatic dizziness (59.3%) and balance problems (25.9%) were exceeded in prevalence only by headache.11 Similar findings have been documented elsewhere in the literature.12–14
Like other sensorimotor sequelae associated with mTBI, vestibular dysfunction can be challenging to assess in the deployed environment, where sophisticated measurement techniques typically are not available. Accurate assessment may be further complicated by situational or environmental stressors that are known to affect performance in military operational settings.15 Sleep disturbances in deployed environments have been shown to contribute to battle fatigue, degraded operational performance, and potentially insidious (and dangerous) lapses in vigilance or “situational awareness” in military parlance.15–18 Although the effects of sleep deprivation on executive function, memory, and reaction time are well established, little is known about the effects of sleep deprivation on vestibular function, a sensory modality also critical for perceptual stability in military operational environments.4,19–21
Few studies have investigated the effects of sleep deprivation on aVOR function, and early work did not identify significant changes in eye movement responses to rotational stimuli after short-term (24–28 hours) sleep deprivation protocols.22,23 There is, however, one notable exception to this trend. Quarck et al24 explored the effects of 26 hours of supervised sleep deprivation on aVOR function through the use of 2 distinct rotational chair testing paradigms. In one of these paradigms, participants were rotated with a velocity step from 0 to 60°/s (angular acceleration 100°/s2) in clockwise and counterclockwise directions. Eye movements were recorded by means of electronystagmography. In a second, independently administered condition, participants were sinusoidally rotated at a velocity of ±25°/s and a frequency of 0.2 Hz (maximum chair acceleration was 0.32°/s2). Findings from these experiments revealed a significant post–sleep deprivation elevation in aVOR gain (eye/chair velocity) relative to a baseline (well-rested) condition for step rotations but not sinusoidal testing. The authors of this study proposed that the abrupt onset of rotation during step testing in conjunction with sleep deprivation–induced modulation of the temporoparietal junction resulted in the enhanced vestibular response.24 This theory is plausible because the temporoparietal junction is an area of known importance both for regulating the vestibulo-ocular reflex (VOR) and for detecting unexpected, potentially destabilizing, or novel stimuli.24–26 To our knowledge, the effects of sleep deprivation on behavioral measures of gaze stability have not been investigated elsewhere. If it holds true, however, that sleep deprivation consistently elevates aVOR responses to moderate and high-acceleration rotational stimuli, such a finding could represent a significant diagnostic impediment to accurate vestibular assessment in deployed clinical environments in which sleep disturbances are commonplace.18 As such, there is a need to identify the effects of sleep deprivation on gaze stability in service members.
The most commonly used clinical measure of gaze stability is dynamic visual acuity (DVA), which refers to a person's ability to see clearly during head movement.27 The dynamic visual acuity test (DVAT) is a behavioral measure of aVOR function used to characterize gaze instability under functional (ie, high velocity and acceleration) conditions by measuring the difference between head stationary and head moving visual acuity.27 Although limited research has been performed exploring the psychometrics of this measure,27–29 the instrumented DVAT is known to be both sensitive (94.5%) and specific (95.2%) for detecting vestibular asymmetry in people with vestibular dysfunction and has been shown to have excellent test-retest reliability for both yaw-plane assessments (r=.87, control participants who were healthy; r=.83, patients with dizziness) and pitch-plane assessments (r=.89, participants who were healthy; r=.94, patients with dizziness).27,28 Reliability testing in study participants who are healthy typically is conducted over 1-week time frames to reflect common clinical practice patterns for reassessment. These same studies, however, have measured reliability in patient participants within the same day to control for the effects of compensation over time.27,28 Reliability testing over periods of 24 to 72 hours (consistent with practice patterns in an operational environment) has not yet been reported in the literature.
Recently, in a study focused specifically on the reliability of commonly used clinical measures of gaze stability, Mohammad et al29 found improved DVAT test-retest reliability when patients with vestibular disorders were tested twice within 1 testing session (with 30 minutes of rest between measurements) relative to subsequent assessment 7 to 10 days later. These findings suggest that the timing of DVA reassessment could affect test reliability if administered at intervals less than 1 week from baseline. Timing of DVAT administration also may be relevant in operational environments in which the opportunity for repeat assessment over a 1-week time frame is not always feasible.30 Given the necessity for objective outcomes to help guide return-to-duty decision making after TBI/traumatic dizziness, the known utility of the DVAT for identifying vestibular asymmetry and the relative dearth of published studies reporting DVAT reliability data for short-term reassessment, further investigation of test-retest reliability within operationally relevant time parameters is appropriate.
The DVAT typically is administered under active (ie, participant-generated) head movement conditions thought to assess vestibular function in concert with descending efference copy signals from the cortex.31 Active head impulses are known to speed the latency of the aVOR response, although gain values typically are augmented only in the presence of vestibular pathology.32 The DVAT also may be administered passively with clinician-administered, high-acceleration, high-velocity, low-amplitude head impulses that are unpredictable in timing and direction.33 Unlike the active or “predictable” DVAT, passive DVA assessment is theorized to isolate peripheral vestibular contributions to gaze stability by eliminating efference copy-mediated effects and resultant preprogrammed eye movements.31 Assessment of peripheral vestibular function is accomplished through examiner-mediated alteration of the predictability, timing, and magnitude of head movement stimuli.31,33,34 Recent evidence suggests that complementary measurement of both active and passive gaze stability may be useful in assessing posttraumatic dizziness, given the possible co-occurrence of peripheral and central dysfunction.2,7 Although there is a growing body of evidence supporting the use of passive DVA assessment, reliability of this technique has not yet been reported for yaw- or pitch-plane assessment.33,35
Given the strong psychometric properties, clinical feasibility, and demonstrated utility in identifying vestibular asymmetry in vestibulopathic and concussed personnel, the DVAT shows considerable promise for use in forward-deployed environments in which comorbid mTBI, posttraumatic dizziness, and sleep deprivation are prevalent.13,27,36,37 The primary purpose of this study was to investigate the effect of 26 hours of supervised sleep deprivation on DVA in uninjured active duty service members. Additionally, we explored the test-retest reliability of the DVAT for assessing aVOR function during an operationally relevant, 24-hour period during which time participants were rested. We hypothesized that DVA would not be significantly affected by 26 hours of supervised sleep deprivation.
Method
Participants
We studied 20 US Army soldiers (18 male, 2 female; mean age=21.7 years, SD=3.3, range=18–28) with no history of TBI or vestibular pathology in a US-based laboratory environment. Selection criteria for participants excluded those with a history of substance abuse, known neurological disorders, and known psychiatric conditions (including attention deficit disorder and posttraumatic stress disorder). Participation required no gross visual (no worse than 20/30 corrected or uncorrected) or hearing problems and was limited to men and women 18 to 50 years of age who had completed at least 12 years of education.
All participants demonstrated full, pain-free active cervical range of motion (including rotation, flexion, and extension) and underwent prophylactic vertebral artery testing. High-acceleration, high-velocity, low-amplitude head impulse testing also was performed on all volunteers to rule out vestibular hypofunction.34 Screening revealed no abnormalities in this study sample. Informed consent was obtained from all participants in accordance with policies and procedures established by the Institutional Review Board of the US Army Research Institute of Environmental Medicine, which approved the study.
Dynamic Visual Acuity Testing
After a standardized task familiarization period consisting of 4 to 5 nonexperimental trials per participant to ensure consistent activation of the rate-triggered optotype, participant DVA was randomly assessed in response to both active (alternating/self-generated) and passive (unpredictable timing and direction/examiner-administered) head movement stimuli with the use of a commercially available system (Micromedical Technologies, Chatham, Illinois). The DVA testing involved discretely performed (ie, noncontinuous) yaw-pane (left and right) and pitch-plane (up and down) head impulses administered in 4 distinct conditions (ie, active yaw, passive yaw, active pitch, and passive pitch). In each test condition, participants were instructed to actively return to or passively submit to a return to a “neutral” start position (characterized by 0° of cervical rotation) before initiation of the next impulse. Impulse parameters were low in amplitude (∼20°) and high in velocity (120–180°/s); 120°/s was chosen as the minimum threshold for optotype presentation to ensure that gaze stability was driven by the aVOR.27 Passive impulses were administered by a physical therapist with 8 years of experience with this technique. For testing, participants were seated 3.1 m (10 ft) in front of a 50.8-cm (20-in) color monitor that was adjusted to ensure that the visual stimulus was triggered at eye level. Individuals requiring corrective lenses for normal viewing were instructed to wear them during all testing sessions.
Static visual acuity was measured first by repeatedly displaying a single optotype (the letter C), randomly reoriented with each trial to 0, 90, 180, or 270 degrees on a computer monitor. Participants viewed 5 optotypes, starting at the smallest possible font size (corresponding with the greatest possible visual acuity level, 20/10). Static visual acuity was established when a participant could correctly identify all 5 optotype presentations at a given visual acuity level. Each level of visual acuity was measured in 0.1 LogMAR units (logarithm of the minimum angle of resolution, log10 X, where X=the minimum angle resolved, in arcmin, with 1 arcmin=1/60°).25 The better the participant's visual acuity, the lower his or her LogMAR score, with approximate (rounded) LogMAR scores of −0.3, −0.1, 0, 0.2, 0.3, 0.7, and 1.0 corresponding to Snellen visual acuity of 20/10, 20/15, 20/20, 20/30, 20/40, 20/100, and 20/200, respectively. Negative LogMAR scores denote visual acuities better than 20/20 (ie, less than 0.00 LogMAR). The ability to assess participant visual acuity at levels better than 20/20 (in both head-static and head-moving conditions) using the Micromedical DVAT reflects a system capability not available in earlier DVA testing studies.27,28
For the dynamic component of the test, a single-axis rate sensor was positioned on the participant's head so that the sensor's axis of maximum sensitivity was aligned with the axis of rotation for yaw- and pitch-plane head movements: axial and interaural axes, respectively. During each head rotation, an optotype “C” pseudo-randomly oriented in 1 of 4 directions on the monitor when head velocity, sensed by the rate sensor, exceeded 120°/s. For each testing condition (ie, yaw-left, yaw-right, pitch-up, and pitch-down), the optotype would only present (ie, be visible) for head movements in the designated direction and for the duration of the head movement. For example, the optotype in the pitch-up condition only flashed when cervical extension velocity exceeded 120°/s during an upward impulse. Within each testing condition, there also were head impulses directed toward the non-optotype flashing side to decrease predictability during passive impulse conditions.
The size of an optotype was determined by the participant's success at correctly identifying the orientation of all previously displayed optotypes. All participants were initially assessed at their previously established static visual acuity rating. If unable to correctly identify the orientation of 4 of 5 optotypes at that level of visual acuity, the size of the optotype was progressively increased by the investigator in 0.1 LogMAR increments (analogous to moving up 1 line on a Snellen eye chart) until the participant was able to identify 4 of 5 optotypes at a given level of visual acuity. This event (correct identification of 4 of 5 optotypes) marked the conclusion of testing for a specific testing condition (eg, active yaw-left head movement testing). The DVA test score for each condition (ie, active yaw-left, active yaw-right, passive yaw-left, passive yaw-right, active pitch-up, active pitch-down, passive pitch-up, and passive pitch-down) was calculated by subtracting the static visual acuity LogMAR score from the DVA LogMAR score. The difference was expressed in LogMAR and corresponds to the number of lines lost on a standard Snellen eye chart. Additional information about LogMAR computation has been published elsewhere.27 Per accepted clinical standards previously reported in the literature, a loss of 3 or more “lines” of visual acuity (9+ optotypes) during dynamic testing would be considered a clinically significant decrement in DVA.27
Sleep Deprivation Protocol
Participant DVA was assessed during morning duty hours (ie, 8 am) at 3 distinct phases within the context of a larger study. During the first testing phase (T1), well-rested participants were instructed on correct performance of the test, were given the opportunity to practice active and passive head impulses, and were assessed under all aforementioned head movement conditions. During the second testing phase (T2), well-rested participants were brought back 24 hours after baseline testing to investigate short-term stability of the DVAT under similar conditions of alertness as T1 and to assess short-term test-retest reliability. Finally, participant DVA was reassessed at T3 (T2 + 26 hours) after 26 hours of supervised sleep deprivation.
Participation in the sleep deprivation protocol was limited to 4 service members per testing session. This 26-hour period of sustained wakefulness was performed between T2 and T3 and was conducted under the constant supervision of research personnel to ensure participant safety and adherence. During the 26-hour sleep-deprivation phase, participants were co-located in a common living area and were encouraged to go about their normal daily routine, which included exercise, regular meals and nutrition, and entertainment. Study participants were closely supervised throughout the 26-hour period to ensure adherence to wakefulness guidelines and abstinence from caffeinated products.
Study Design and Data Analysis
This prospective, repeated-measures design used sleep deprivation as an environmental perturbation to quantify DVA performance within participants across 3 levels of time. SAS 9.2 software (SAS Institute Inc, Cary, North Carolina) was used to perform a mixed-model analysis with random individual intercept to account for correlation of repeated measurements within participants between conditions. Factors included in the statistical model included independent variables of time (3 levels), head movement condition (2 levels: active versus passive), and impulse direction (2 levels). Yaw and pitch analyses were performed separately. Planned comparisons were established a priori to investigate the effects of time on DVA performance after 24 hours in a rested condition (measure stability) and again after 26 hours of sleep deprivation, with the alpha level of significance established at .05 for each test. Whereas a Bonferroni correction was not prospectively applied to adjust for multiple comparisons, a post hoc correction for the 2 primary pair-wise comparisons (ie, T1 versus T2 and T2 versus T3) would yield a corrected significance level of .025. Post hoc tests were performed to assess for effects of significant 2-way and 3-way interactions between independent variables on the dependent variable (DVA). Time-point comparison calculations for 20 participants yielded 80% power at the 2-sided .05 significance level to detect a difference between time points (ie, 0.66 times the standard deviation in DVA performance, assuming a correlation of .5 between time points, within participants).
Intraclass correlation coefficients (ICC [3,1]) with 95% confidence intervals were used to assess measure agreement and test-retest reliability over the 24-hour time frame among rested participants (T1 and T2) for each permutation of head movement conditions.
Results
24-Hour Test-Retest Reliability
Intraclass correlation coefficient (3,1) analysis from T1 to T2 revealed variable levels of agreement between the 4 head movement conditions. The strength of associations ranged from “poor” to “moderate.”38 Data for yaw and pitch impulses (including 95% confidence intervals) are presented in Tables 1 and 2. The performance data by condition (ie, active and passive yaw and pitch) for the rested reassessment are described in greater detail below. Post hoc between-subjects analysis of variance (ANOVA) was not found to be significant (F=2.02, df=19, P=.171).
Yaw Dynamic Visual Acuity: Intraclass Correlation Coefficients (3,1) (95% Confidence Intervals)a
Pitch Dynamic Visual Acuity: Intraclass Correlation Coefficients (3,1) (95% Confidence Intervals)a
Yaw DVA
24-hour reassessment–rested condition.
Mean static visual acuity in the study sample was −0.29 LogMAR (0.30). Absolute yaw DVA values are presented in Table 3. Although there was a significant time effect (F=7.08, df=2, P<.001), head movement direction (ie, left versus right) (F=0.41, df=1, P=.52) and head movement type (ie, active versus passive) (F=0.18, df=1, P=.78) did not significantly influence DVA performance for yaw-plane impulses (thus, yaw measurements were averaged across these head movement direction and movement type conditions). Yaw impulse analysis revealed a statistically significant improvement in DVA (ie, yaw DVA) from T1 to T2 (t=3.60, df=216, P=.0004), with a mean improvement of −0.04 LogMAR (Log of the minimum angle resolved). This improvement equates to correct identification of 2 to 3 additional optotypes with the second test (with a change of 1 optotype equivalent to 0.018 LogMAR of acuity).28
Absolute Yaw Dynamic Visual Acuity Values
Sleep-deprived condition.
No change in yaw DVA was identified after sleep deprivation (t=0.90, df=216, P=.37). Combined yaw-plane DVA data and variance for each of the 3 time points are shown in Figure 1.
Change in mean group yaw dynamic visual acuity (DVA) values from time 1 to time 2 (test-retest stability) obtained under rested conditions. Change in mean group yaw DVA values from time 2 to time 3 reflect 26 hours of supervised sleep deprivation (sleep deprivation protocol). Solid line represents active DVA values; dashed line represents passive DVA values. Error bars characterize the collective variance (standard deviations) for measurements at each time point. The Snellen eye chart equivalent scores follow the LogMAR score in parentheses. Note visual acuity is better than 20/20 in all cases. Statistical significance of time effect is denoted with open bracket (P=.0004). As a point of reference, note that functional yaw-plane DVA deficits in patients with vestibular hypofunction have been measured in the range of LogMAR=0.3–0.4, per the findings of Herdman et al.36 PY=passive yaw, AY=active yaw.
Pitch DVA
24-hour reassessment–rested condition.
Absolute pitch DVA values are presented in Table 4. Pitch analysis revealed overall statistically significant changes in DVA performance for time (F=7.54, df=2, P=.0007), head movement type (ie, active versus passive) (F=5.30, df=1, P=.04), and head movement direction (ie, up versus down) (F=4.25, df=1, P=.02); however, tests for 2- and 3-way interaction effects were not statistically significant. The DVA differences from T1 to T2 (t=3.56, P=.0005) revealed improvement of 0.025 LogMAR (down) and 0.04 LogMAR (up) under active conditions (the equivalent of 2 additional optotypes correctly identified in each direction). Passive DVA improved 0.04 LogMAR down (average of 2 optotypes) and 0.015 LogMAR up (∼1 optotype). Combined pitch-plane DVA data for each of the 3 time points are shown in Figure 2.
Absolute Pitch Dynamic Visual Acuity Values
Change in mean group dynamic visual acuity (DVA) values from time 1 to time 2 (test-retest stability) obtained under rested conditions. Change in mean group pitch DVA values from time 2 to time 3 reflect 26 hours of supervised sleep deprivation (sleep deprivation protocol). Active, downward-directed (AD) head impulses are depicted with the thin solid line; passive, downward-directed (PD) impulses are depicted with the dashed line; active, upward-directed (AU) impulses are depicted with the bold solid line; and passive, upward-directed (PU) impulses are depicted with the stipple-circle line. Error bars characterize the collective variance (standard deviations) for measurements at each time point. The Snellen Eye Chart equivalent to the LogMAR score is depicted in bold below. Note visual acuity is better than 20/20 in all cases. Statistical significance of time effects is denoted with open brackets. As a point of reference, note that functional yaw-plane DVA deficits in patients with vestibular hypofunction have been measured in the range of LogMAR=0.3–0.4, per the findings of Schubert et al.28
Sleep-deprived condition.
Mean active pitch DVA worsened significantly from T2 to T3 (t=3.12, P=.002). Active pitch DVA diminished by −0.005 LogMAR (down) (<1 optotype) and −0.055 LogMAR (up) (∼3 optotypes missed). Passive pitch DVA was degraded by −0.06 LogMAR (down) (ie, ∼3 optotypes) and −0.045 LogMAR (up) (an average of 2–3 optotypes missed).
Discussion
Short-Term Stability of the DVA Response Under Rested Conditions
Preliminary research supports weekly reassessment of DVA among service members in US-based military treatment facilities to guide return-to-duty decisions after TBI.37 There is currently, however, both an operational need for—and a dearth of—objective, evidence-based measures to inform such decisions in operational environments. Previous studies report test-retest reliability of the DVAT at time intervals ranging from hours (in patient participants) to days (in control participants who are healthy).27–29 To date, however, measurement stability data for 24-hour reassessment of control participants who are healthy is lacking.
Findings from the current study reveal statistically (but not clinically) significant improvement in DVA performance under well-rested conditions that may be consistent with a mild practice effect.38 The magnitude of DVAT improvements in this study (2–3 optotypes) in response to yaw- and pitch-plane impulses are similar to previously reported results in both patient participants and control participants who were healthy.27–29 In separate studies, Herdman et al27 and Schubert et al28 reported enhanced DVA performance for same-day reassessments in patients with mean change magnitudes of 2.3 (SD=0.7) optotypes (yaw) and 2 optotypes (pitch), respectively. Mohammad et al29 reported small but significant yaw DVA improvements in patients with vestibular disorders for same-day and 7-day reassessments. Mean yaw change magnitudes in the study by Mohammad et al29 ranged from 0.04 (SD=0.03) to 0.07 (SD=0.01) LogMAR, although pitch performance remained consistent.
Test-retest reliability estimates of the DVAT in this study were lower than those previously reported by Herdman et al,27 Schubert et al,29 and Mohammad et al.30 This finding is most likely to be a function of the limited variability in the DVA data and a consequent violation of the restriction in range assumption for the ICC model.38 It is well established that a restriction in the range of normally distributed values can reduce correlations in ICC models, causing artificially deflated reliability estimates.38–40 Statistical theory indicates that when within-subject variance in a model is greater than between-subjects variance, as was confirmed by a post hoc ANOVA reported in this study, the reliability estimate may not be considered valid because the actual limits of the ICC do not match the theoretical limits of .00 to 1.00.38,41 The lack of between-subjects variance observed in the model is consistent with sample homogeneity in the 2 key variables known to affect DVA performance: participant age and vestibular function. In contradistinction to significant participant age variability reported by Herdman et al27 and Schubert et al28 (both groups of researchers assessed DVA performance in control and patient participants across multiple decades), these data reflect performance in a sample with a mean age of 21.7 years (SD=3.3). Violation of the restriction in range assumption in this case seems plausible, given the extent to which DVA performance is known to vary with age.27,28
Restricted range also was evident in the DVAT performance data. This finding is not surprising, however, given that participants in the current study showed no history of head trauma or vestibular pathology and demonstrated normal vestibular responses to head impulse testing. Conversely, participants in previous DVA investigations demonstrated significant performance variability, reflecting a much broader range of vestibular function than was observed in this study. Herdman et al,27 for example, reported DVA performance across a diverse sample, with responses ranging from normal (X̅=0.043, SD=0.048) in participants who were healthy aged 19 to 79 years, to subtly impaired (X̅=0.286, SD=0.144, or ∼20/40) in patients with unilateral vestibular loss, to more significantly degraded DVA (X̅=0.397, SD=0.137, or ∼20/50) in patients with bilateral vestibular hypofunction.
The relatively small sample size also may have adversely influenced reliability and ICC confidence interval estimates. Portney and Watkins38 indicated that for cohorts of fewer than 30 participants, sampling distributions tend to be flatter than normal and ICCs tend to be less precise, resulting in wider confidence intervals. The current study showed DVA performance in a cohort of 20 participants—a number far exceeded by sample sizes in the studies by Herdman et al27 (n=97) and Schubert et al28 (n=64).
Although the reliability findings from this study are admittedly suspect, given the homogeneity of the sample, the observation that passive DVA testing seemed to yield superior repeatability to active testing suggests a potentially interesting consideration for gaze stability assessment. It is possible that superior DVA reliability may be achieved under passive testing conditions when impulses are administered by an experienced clinician, given an examiner's superior and consistent control of the magnitude, timing, and velocity of head movement stimuli relative to active DVA testing. Future research should explore potential reliability differences between active and passive testing approaches. In summary, despite the questionable ICC values and confidence intervals reported in these data, the relatively small overall magnitude of DVA change demonstrated by participants in this study and in previous studies suggests that the DVAT is sufficiently stable to serve as an acute screening tool for concussion-related vestibular dysfunction in a deployed environment.
Yaw DVA and Sleep Deprivation
The results of this study yielded no statistically or clinically significant change in yaw DVA after 26 hours of sleep deprivation. These findings suggest that functional gaze stability is preserved after short-term sleep deprivation under head movement and illumination conditions characteristic of daily activities. Consequently, these data provide preliminary support for the use of high-energy, functional techniques such as DVA to assess gaze stability in conditions in which sleep deprivation may confound assessment.
The results from this study reveal potential differences between moderate- and high-velocity assessment techniques that clinicians should consider when selecting and interpreting objective measures for patients with traumatic dizziness. Possible explanations for divergent findings between this study and that performed by Quarck et al24 include differences in rotational stimulus characteristics and experimental lighting conditions.
Head Movement Stimulus Characteristics
Evidence suggests that vestibular responses in human and nonhuman primates are frequency- and velocity-dependent, meaning that aVOR response magnitudes vary depending on the kinematic parameters of the rotational head movement stimuli applied.42,43 Specifically, physiological data in primates support the idea that the vestibular system is capable of generating nonlinear aVOR responses to rapid, high-frequency component angular head movements to stabilize gaze during highly dynamic (ie, high-velocity, high-frequency) activities such as walking or running.43,44 Although peak rotational head velocity and acceleration were not measured in this study, head impulses performed during DVA testing are known to approach 3,500°/s2 and 250°/s, values that greatly exceed the moderate acceleration (100°/s2) and velocity (60°/s) stimuli applied by previous researchers.24,33,45 We suggest that the “high-energy” head movement stimuli applied during DVA testing in this study may have contributed to the well-preserved gaze stability performance observed among study participants.
Other studies measuring aVOR function have yielded similar results.32,46 High velocity, acceleration, and frequency component rotations are known to generate gains at or close to 1.00 (a perfectly compensatory response).32,46 A gain of 1.00 implies that there is precise agreement between head movement and eye movement such that the object of an individual's interest is clear and stable on the fovea.3 Conversely, a gain of greater than 1.00 implies that eye velocity actually overcompensates for head velocity, which can degrade gaze stability.3 In the study by Quarck et al,24 initial (rested) mean VOR gain values were initially measured at 0.77 (SD=0.16) in response to rotational stimuli of 60°/s and 100°/s2 increasing to a mean gain of 0.90 (SD=0.18) after sleep deprivation. One possible explanation for the different responses to sleep deprivation between “high” and “moderate” energy stimuli may be that an optimized system (ie, stable gaze characterized by a gain of ∼1.00 or DVA not significantly different from static visual acuity) may demand little descending drive (from the temporoparietal junction). Conversely, a system not so primed may require a stronger descending signal. Given this explanation, an optimized vestibular system would need to suppress descending inputs to avoid excessive aVOR “augmentation” that would be functionally detrimental to sensory stability.4,43,44 Thus, although it is possible that sleep deprivation affects gaze stability differently with moderate head movement stimulation relative to higher-energy impulses, additional investigation on this topic will be necessary to better characterize the relationship between head movement kinematics and aVOR responses after sleep deprivation.
Experimental Lighting Conditions
Dynamic visual acuity testing in this study was performed under well-lit laboratory conditions to ensure optimal viewing of the visual stimulus. If the enhanced aVOR response to rotational step testing in the study by Quarck et al24 was precipitated solely by the unexpected nature of the stimulus as the authors suggested, we might have anticipated a similar augmentation of DVA in the current study sample after sleep deprivation in response to passive head impulses. The results of this study did not reveal this augmentation of DVA, a finding possibly related to the presence of visual fixation during DVA test conditions. It is possible that because participants were aware of their visual surroundings at all times during the DVA protocol (including passive impulses), there was little or no demand on the temporoparietal junction to reestablish orientation as there presumably was with fixation removed during rotational chair testing in the study by Quarck and colleagues.24 Angular vestibulo-ocular reflex function is known to be enhanced in well-lit conditions relative to performance measured in the dark.3,47
Pitch DVA and Sleep Deprivation
Pitch-plane DVA measurements obtained after 26 hours of sleep deprivation revealed a mean degradation in visual acuity equivalent to less than 1 line on a standard Snellen eye chart. Deterioration of vertical visual acuity was found to be statistically but not clinically significant.28 Although it is unlikely that observed changes reflect disruption of descending cortical influences (given the absence of corresponding significant disruption to yaw-plane responses and common central pathways), the subtle decrement in pitch DVA could be related to increased blink-related impediments to visual acuity.
Increased blink frequency or central perseveration of the blink response caused by central fatigue and decreased attention may account for the subtle degradation in observed vertical DVA. In one study investigating the effect of 20 hours of sleep deprivation on participants who were healthy, the researchers reported that participant blink rate was significantly higher after a night without sleep than before.48 Complementary findings in flight experiments reveal that increases in blink rate are closely associated with degraded performance under conditions that necessitate gaze shifting (ie, saccades) or head movement—behaviors that are both characteristic of DVA testing.45,49 Other authors have suggested that, like blink frequency, blink closure time (ie central perseveration of the blink response) increases with increasing time on task when fatigued. This factor also might have adversely affected pitch DVA performance.49,50
Although the DVA metric used in this study precludes a description of eye movement kinematics or the verification of blink behavior, there is evidence of increased blink frequency in the human factors literature after sleep deprivation through the use of both scleral search coil and infrared camera technology.51,52 Pitch-plane head impulses also have been shown to elicit more frequent blinks than yaw-plane rotations as measured with wireless scleral search coil during a gaze stabilization task.2 Given that accurate performance on the DVAT necessitates visualizing a target to discriminate optotype orientation, the hypothesis for fatigue mediated DVA degradation could describe subtle differences in visual acuity noted in this study. Both increased frequency and longer duration of blinks would account for subtly diminished gaze stability during pitch-plane head movements without implicating “abnormal” VOR performance in a group with no known history of vestibular dysfunction or head injury and better than 20/20 DVA in all tested conditions.
Study Limitations
As discussed, reliability values in this study were lower than those previously reported in the rehabilitation literature.27–29 Although this discrepancy could be related to variability in equipment or possible differences in DVA system resolution, it seems most likely that low ICCs were the result of a restriction in the DVA data range given the lack of variability in our young control sample.38,39 Previous clinical studies using DVA as an outcome measure have consistently demonstrated a broader range of LogMAR scores given the presence of pathologically high DVAT scores from patient participants with unilateral or bilateral vestibular loss.27–29 It is probable that DVAT reliability would have been superior in a more heterogeneous sample; however, the small DVA change magnitudes observed during reliability testing in this study and in earlier studies suggest that this measure is sufficiently stable for use in austere environments to screen concussed service members for vestibular comorbidity and to help guide return-to-duty decision making.27–29
Conclusion
The findings of the present study suggest that 26 hours of sleep deprivation does not have a significant effect on DVA in control service members who are healthy. Data reveal that changes in DVA under both rested and sleep-deprived conditions were within accepted and published ranges of normal variability for this measure. Further well-controlled investigations of head movement stimulus characteristics in patients with vestibular disorders will be essential to better characterize the relationship between sleep deprivation and gaze stability.
Footnotes
Dr Scherer provided concept/idea/research design and project management. All authors provided writing. Dr Scherer and Mr Claro provided data collection and analysis. Dr Heaton provided study participants, facilities/equipment, and consultation (including review of manuscript before submission). The authors thank Elisabeth Kryskow and Alexis Maule in support of this research; Caitlin Dillon for her assistance with figure preparation; and Dr Emily Blood and Dr Steve Allison for insightful recommendations and technical expertise in the statistical treatment of the data.
This study was approved by the Institutional Review Board of the US Army Research Institute of Environmental Medicine.
A platform presentation of this research was given at the Combined Sections Meeting (Neurology Section) of the American Physical Therapy Association; February 10, 2012; Chicago, Illinois.
This work was supported by Congressionally Directed Medical Research Programs (CDMRP) through an Advanced Technology Award (W81XWH-08-2-0,177) to Jamshid Ghajar and by the US Army Medical Research and Materiel Command (USAMRMC) through W81XWH-08-1-0,021 to Dr Heaton.
The opinions and assertions contained herein are the private views of the authors and are not to be construed as official or as reflecting the views of the Department of the Army or the Department of Defense.
- Received March 30, 2012.
- Accepted November 8, 2012.
- © 2013 American Physical Therapy Association
References
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