Ocular Responses and Visual Performance after High-Acceleration Force Exposure

Abstract

purpose. To evaluate ocular responses and visual performance after high-acceleration force exposure.

methods. Fourteen men were enrolled in the study. A human centrifuge was used to induce nine times the acceleration force in the head-to-toe (z-axis) direction (+9 Gz force). Visual performance was evaluated using the ETDRS (Early Treatment of Diabetic Retinopathy Study) visual chart, and contrast sensitivity (CS) was examined before and after centrifugation. Ocular responses were assessed with biomicroscopy and topographic mapping after gravitational stress.

results. Transient visual acuity reduction (0.02 ± 0.04 logMar vs. 0.19 ± 0.07 logMar VA; P < 0.05) and temporary ocular anterior segment reactions were observed immediately after centrifugation. These reactions included changes in corneal thickening (553.7 ± 21.7 μm vs. 591.2 ± 20.6 μm; P < 0.05), increasing anterior chamber depth (ACD; 3.19 ± 0.26 mm vs. 4.53 ± 0.34 mm; P < 0.05), and pupillary enlargement (3.54 ± 0.73 mm vs. 5.76 ± 0.61 mm; P < 0.05). The increase in ACD continued for 15 minutes after exposure to acceleration (3.19 ± 0.26 mm vs. 4.39 ± 0.27 mm; P < 0.05). Pupillary dilation was noted both 15 (3.54 ± 0.73 mm vs. 5.56 ± 0.67 mm; P < 0.05) and 30 (5.47 ± 0.59 mm, P < 0.05) minutes after the gravitational stress. CS decreased significantly at low and medium spatial frequencies (1.5, 3, and 6 cyc/deg) and did not return to the baseline level by 30 minutes.

conclusions. High-acceleration force may induce transient visual acuity reduction and temporary corneal thickening. Prolonged increase in ACD and pupillary dilation were also observed. The decrease in CS persisted for 30 minutes after centrifugation. The mechanisms underlying these observations are not clear, because there are no previous reports on this topic. Further studies are needed.

Vision plays a critical role in humans undergoing high-acceleration movement. With increases in modern vehicle performance, problems associated with acceleration are becoming important. ^{1 2} When an emergency occurs at high speed, visual performance is important to preventing further catastrophe because the response time is relatively short. ^{1 2} Investigators in prior studies have reported that positive acceleration can cause grayout, blackout, and loss of peripheral vision. ^{1 3 4} Many ocular reactions may also occur when the head is suddenly forced to stop or start moving or to turn rapidly. As the eye is forced to follow the movements of the head, this acceleration-deceleration–induced shearing force may induce ocular structure changes and even injuries. ^{5 6} Because previous data are usually based on subjective descriptions and are not quantitative, it is important to clarify the influence of acceleration force on visual performance and ocular reactions. However, this issue has not been explored thoroughly because of the difficulty in designing experiments. 

Recent advances in technology allow the human centrifuge to be used to elicit high-acceleration forces. ^{4 7} The centrifuge is designed to improve the trainee’s learning experience during high G-forces. The desired G-forces recommended for optimal training can be adjusted accurately by the instructor according to the trainee’s weight, which allows each subject to train under the same G-force influence. ^{2 8}  

A corneal topography system (Orbscan II; Bausch & Lomb, Rochester, NY) can be used to evaluate objectively the ocular reaction after high G-force exposure. The system is a reliable ocular structure analyzer that uses a calibrated and scanning slit beam to access ocular anterior segment-related structures such as the cornea and to measure pupil size and anterior chamber depth (ACD) at the same time. It does not contact the ocular surface and thus avoids touching the corneal surface and disturbing the detected reading. ^{9 10}  

The goal of this study was to investigate the influence of high-acceleration force on visual performance and ocular reactions. In this study, a human centrifuge was used to elicit an acceleration force set at nine times G-force in the head-to-toe z-axis direction (+9 Gz force). The influence of acceleration force on visual performance was evaluated by measuring visual acuity and contrast sensitivity (CS). The changes in ocular reactions were assessed by biomicroscopy, physical examinations, and corneal topography (Orbscan II; Bausch & Lomb). 

Materials and Methods

Fifteen men (mean age, 21.1 years) were enrolled in the study. Informed consent was obtained from each subject before participation. All experimental protocols were conducted in accordance with the Declaration of Helsinki. Ethical approval for this study was obtained from the institution review board. Subjects with any history of ocular or systemic disease, such as hypertension, diabetes, glaucoma, cataract, or uveitis, were excluded from the investigation. 

All examinations were performed at the Air Force Health Examination and Physiological Training Center, Kan-Shan Armed Forces Hospital, Taiwan. All subjects had remained at sea level for the previous month. Before centrifugation, each subject underwent a complete ocular examination that included tests of visual acuity (Early Treatment of Diabetic Retinopathy [ETDRS] logMAR chart) and refraction (AR310; Nidek, Tokyo, Japan) and examination with the biomicroscope. The letter stimuli of the ETDRS logMAR chart in this study are printed on an illuminated cabinet (background luminance, 350 cd/ m²). The chart has five letters per row ranging in size from +1.0 to −0.30 logMAR. Visual acuity was tested at 4 m distance. The corneal topography system (Orbscan II; Bausch & Lomb) was used to assess the various ocular responses including Sim K (maximum K and minimum K values), anterior best-fit sphere (BFS), posterior BSF, ACD, pupillary diameter (PD), and central corneal thickness (CCT). Macular responses such as metamorphopsia were detected by using the Amsler grid test, and visual performance was assessed further by testing CS with the CS was tested monocularly before and after +9-Gz exposure by a CS test chart (VCTS 6500; Vistech Consultants, Inc., Dayton, OH). The chart consists of 45 circular targets with gratings of different size and contrast. The target size in the distance test is 7.5 cm. The gratings in the targets are vertical or 15° left or right from the vertical direction. In the test chart, the contrast decreases horizontally from left to right, and gratings become smaller vertically from top to bottom (from 1.5 to 18 cyc/deg; from target A to target E). The subject began at the top horizontal line A and stated whether the gratings in targets 1 to 9 are vertical, left, or right. The last target that the subject reported correctly was marked down on a result paper provided by the test. The same procedure was repeated in all the other horizontal test lines from B to E. At measurement time, the room luminance was approximately 200 cd/m² and the test distance, 3 m. 

After these examinations, the subject entered the human centrifuge and donned an aviation helmet with a microphone attached so that he could communicate with the aerospace physician outside. A TV monitor was mounted outside the human centrifuge to monitor the status of each subject. When the setting was complete, a gravitational stress of +9-Gz force was established with a human centrifuge which also applied G-forces parallel to the subject’s body. The technician outside the centrifuge accelerated the speed until it reached +9 Gz and held this constant for 15 seconds. The operating protocol to induced +9 Gz in this experiment was as follows. The centrifuge was accelerated to 2 G/s from 1 to 1.4 G for 15 seconds, then accelerated to 2 G/s from 1.4 to 4 G and held constant for 20 seconds, and then reduced to 1.4 G for 30 seconds. The centrifuge was then accelerated rapidly to 6 G/s and then to 9 G for 15 seconds before slowing to 2 G/s and finally to 1 G. ^{4 11}  

Visual acuity was checked and the corneal topographer was applied again immediately, 15 minutes, and 30 minutes after the centrifugation. Refraction and CS were measured 30 minutes after the gravitational stress. All data were collected and analyzed. Fundus examination was performed 2 hours after centrifugation. Throughout the experiment, blood pressure (BP) and pulse rate were monitored by a digital BP monitor (HDM 704 cm; Omron, Tokyo, Japan). All results are expressed as the mean ± SD. A paired t-test was used to compare the physiological parameters before and after centrifugation. P < 0.05 was accepted as significant. 

Results

One subject withdrew from the study because of nausea after the centrifugation. All data were collected from 14 eyes. Most of the ocular-related parameters, such as anterior BFS, posterior BFS, and Sim K, did not change significantly from before to after centrifugation. However, the CCT increased significantly immediately after centrifugation compared with the value before centrifugation (553.7 ± 21.7 vs. 591.2 ± 20.6, P < 0.05), but this was not maintained beyond 15 minutes after high gravitational stress (Table 1) . 

ACD increased considerably immediately after (3.19 ± 0.26 mm vs. 4.53 ± 0.34 mm, P < 0.05) and 15 minutes after (4.39 ± 0.27, P < 0.05) +9-Gz force stress. ACD returned to the pretest value by 30 minutes after exposure to acceleration (3.24 ± 0.29, P > 0.05; Table 2 ). 

PD enlarged significantly immediately after (3.54 ± 0.73 mm vs. 5.76 ± 0.61 mm; P < 0.05) and 15 minutes (5.56 ± 0.67 mm; P < 0.05) after centrifugation. PD remained enlarged 30 minutes after exposure to acceleration (5.47 ± 0.59 mm; P < 0.05; Table 3 ). 

In the tests of visual performance, transient visual acuity decreased immediately after the gravitational stress (0.02 ± 0.04 vs. 0.19 ± 0.07, P < 0.05; Table 4 ). CS reduction was also observed at 30 minutes after exposure to acceleration, and significant depression of CS was found at low and medium frequencies. CS in the right eye decreased at 1.5 (P < 0.05), 3.0 (P < 0.05), and 6.0 cyc/deg (P < 0.05; Fig. 1 ). Refraction remained stable at 30 minutes after gravitational stress (Table 4) . The Amsler grid examination revealed no particular finding such as metamorphopsia in any subject. 

Throughout the experiment, ocular posterior segment revealed no specific observations. In addition, no particular ocular finding was noted such as hyphema, lens dislocation, or retinal hemorrhage. 

Discussion

In this study, we observed a 10% increase in CCT after +9-Gz force exposure. We assume that the transient hydrostatic pressure increase may explain this finding. The ocular anterior chamber in the eye is full of aqueous humor. ^{12 13} An exposure to high gravity may increase hydrostatic pressure in the anterior chamber and increase the tendency for fluid to flow across the corneal endothelium into the stroma, which would increase the corneal thickness. ¹⁴ The CCT returned to its initial value within 15 minutes, suggesting that the corneal endothelium was not compromised by high gravitational exposure, even at +9-Gz force. An interesting observation was that a 10% increase in CCT occurred without significant concomitant changes in the corneal curvature. Our data are consistent with those of Rom et al., ¹⁵ who found no significant correlation between corneal thickness and curvature, even when the corneal thickness increases up to 16%. 

PD increased significantly after high G-force exposure in our study. Before the stress, PD was 3.54 ± 0.73 mm, and the marked pupillary dilation persisted for 30 minutes after the stress. The size of the pupil is regulated by the autonomic nervous system, which is influenced by many environmental, physiological, and psychological factors. Previous studies show that gravitational stress can increase sympathetic tone to prevent body fluid shifting downward with gravity. ¹⁶ This transient sympathetic tone elevation may account for the early pupil dilation immediately after centrifugation. However, an increase in sympathetic activity cannot clarify completely why the pupil enlargement persisted for 30 minutes. Tran et al. ¹⁷ reported that high G-force exposure causes a persistent reduction in parasympathetic activity. This prolonged reduction in parasympathetic activity may also explain the persistent pupil enlargement after gravitational stress. Neurohormonal regulation is another possible explanation for this persistent pupil dilation. Gravitational stress increases the blood somatostatin concentration. Yamaji et al. ¹⁸ found that somatostatin may induce mydriasis by attenuating cholinergic neurotransmitter release. Therefore, neurohormonal regulation may also be involved in this prolonged pupil enlargement. 

In our experiment, the ACD increased immediately and 15 minutes after +9-Gz force exposure but returned to baseline within 30 minutes after gravitational stress. Pupil enlargement may explain the increase in ACD at 15 minutes after gravitational stress, but it cannot explain why the ACD returned to baseline when mydriasis persisted 30 minutes after centrifugation. We believe that the increase in hydrostatic pressure caused by the +9-Gz force explains this finding. The aqueous humor in the eye may shift toward the gravity direction under gravitational stress. ^{12 13} When subjects are under high-gravity stress, the aqueous hydrostatic pressure in the anterior and posterior chambers may increase toward the gravity direction. Because the volume is greater in the anterior chamber than in the posterior chamber, the aqueous humor pressure is also greater in the anterior chamber during high G-force exposure. ^{12 13} The greater hydrostatic pressure in the anterior chamber may push the iris toward the posterior chamber and cause the ACD to increase. At the same time, this iris diaphragm may rest on the lens surface and trap fluid in the anterior chamber. When the hydrostatic pressure is relieved, the trapped aqueous humor maintains the ACD, which may explain the prolonged deepening of the anterior chamber. The trapped aqueous humor drains with time, and the ACD returns to baseline. ^{12 13 19} We also observed that the refractive power did not reveal a significant finding at 30 minutes after +9-Gz exposure. This observation suggests that axial length did not change at 30 minutes after gravitational stress. However, further research is necessary to confirm this finding. 

In our study, visual acuity showed a transient reduction immediately after centrifugation and returned to baseline at 15 minutes. We assume that temporary corneal edema plays a role, because a study has shown that corneal edema can disturb visual acuity. ²⁰ However, the Amsler grid examination revealed no specific findings in our study, suggesting that the macular structure was not compromised even after the high G-force exposure. For clarification of our supposition, further study may be helpful, such as pinhole, potential acuity testing, and laser interferometry. Visual acuity is usually evaluated with the ETDRS visual chart, a basic method of evaluating visual performance by estimating the visual response to black-and-white contrast. However, performance on the ETDRS chart represents one extreme of CS, and in reality, objects and their surroundings are of varying contrasts. The CS test was developed based on the measurement of visual resolution for a wide range of contrasts. The CS test is useful for evaluating visual quality more precisely, by plotting the reciprocal of the threshold contrast for sinusoidal gratings as a function of their spatial frequency. It thus gives information on visual performance for a range of object scales. ²¹  

In this investigation, we observed remarkable CS loss after gravitational stress and that more than 30 minutes was needed for recovery. Several ocular anterior chamber reactions observed in the study may account for this finding, including corneal clarity and pupillary mydriasis. Hess and Garner ²¹ reported that corneal edema leads to depression of CS. Other researchers have also demonstrated that pupil mydriasis may compromise CS function. ^{22 23} However, the changes of ocular anterior segment reaction cannot fully elucidate why the CS was significantly reduced at low and medium but not at high spatial frequency at 30 minutes after gravitational stress. Factors other than ocular anterior segment response are thought to explain this observation. We assume that the changes in neuroretinal function may play a role in this phenomenon. Ossard et al. ²⁴ have demonstrated that gravitational stress can cause body fluid to shift toward the lower body, which decreases ocular blood flow and leads to hypoxia. Several studies have reported that hypoxia may compromise neuroretinal function and lead to prolonged CS reduction. ^{25 26 27} Visual acuity was coupled to changes in microcirculation in the retina such as retinal capillary density and the size of the free avascular zone (FAZ). In a past study, Arend et al. ²⁶ showed that CS is a more sensitive examination for detecting the change of microcirculation in retina. DiLeo et al. ²⁸ reported that hypoxia may affect magnocellular ganglion cells more severely than parvocellular ganglion cells. The magnocellular ganglion cells are more sensitive to low-contrast stimuli, whereas parvocellular ganglion cells are more sensitive to high-contrast stimuli. ²⁹ Therefore, they also reported that hypoxia may result in contrast losses, particularly at low and medium spatial frequency. ²⁸ Because parvocellular ganglion cells were affected less severely than magnocellular ganglion cells, Harris et al. ³⁰ showed that CS in a patient with minimal diabetic changes in the retina improved significantly, especially at high spatial frequencies, when the patient was subjected to hyperoxia. In our study, the CS examination was performed at 30 minutes after gravitational stress. CS still was significantly reduced at low and medium spatial frequency at 30 minutes, perhaps because magnocellular ganglion cells are affected more severely than parvocellular ganglion cells during gravitational stress. Simultaneously, we observed that differences in CS were unremarkable high special frequency, perhaps because parvocellular ganglion cells are affected less severely than magnocellular ganglion cells during gravitational stress. 

In this study, we observed that high-acceleration force induces noteworthy ocular anterior segment reactions and compromises visual performance. There observations may assist individuals on flight or space missions in preparing for such visual phenomenon. However, these phenomena have not been studied thoroughly to date. Moreover, the effect of gravitational stress on neuroretinal structure and function, such as retinal thickness and cone cell function, has not been completely clarified. Further research is necessary. 

 Supported by grants from the 2007 Research and Development Fund of Kaohsiung Military General Hospital, Grants TSGH-C97-69 and TSGH-C98-69 from the Tri-Service General Hospital, the Chen-Han Foundation, and Grants 92-2314-B-016-065 and 93-2314-B-016-016 from the National Science Council.

 Submitted for publication February 15, 2009; revised April 17, 2009; accepted July 23, 2009.

 Disclosure: M.-L. Tsai, None; C.-C. Liu, None; Y.-C. Wu, None; C.-H. Wang, None; P. Shieh, None; D.-W. Lu, None; J.-T. Chen, None; C.-T. Horng, None

 The publication costs of this article were defrayed in part by page charge payment. This article must therefore be marked “advertisement” in accordance with 18 U.S.C. §1734 solely to indicate this fact.

 

Table 1.

 

The Cornea-Related Parameters before and after Gravitational Stress

	Before	Immediately After	After 15 min	After 30 min
Sim K
Maximum	44.52 ± 0.43	45.08 ± 0.63	45.21 ± 1.17	44.89 ± 1.31
Minimum	43.91 ± 0.67	44.57 ± 0.81	44.32 ± 0.61	44.21 ± 0.87
Anterior BFS (D)	43.23 ± 1.51	42.94 ± 1.32	42.98 ± 0.94	43.11 ± 1.34
Posterior BFS (D)	52.37 ± 2.03	52.02 ± 2.21	52.11 ± 0.97	52.29 ± 1.47
CCT (μm)	553.7 ± 21.7	591.2 ± 20.6*	567.4 ± 21.6	556.2 ± 23.6

  n = 14 eyes.

*  Statistically significant difference (P < 0.05).

Table 2.

 

Anterior Chamber Depth before and after Gravitational Stress

	Before	Immediately After	After 15 min	After 30 min
ACD (mm)	3.19 ± 0.26	4.53 ± 0.34*	4.39 ± 0.27*	3.24 ± 0.29

  n = 14 eyes.

*  Statistically significant difference (P < 0.05).

Table 3.

 

Pupillary Diameter before and after Gravitational Stress

	Before	Immediately After	After 15 min	After 30 min
PD (mm)	3.54 ± 0.73	5.76 ± 0.61*	5.56 ± 0.67*	5.47 ± 0.59*

  n = 14 eyes.

*  Statistically significant difference (P < 0.05).

Table 4.

 

Visual Acuity and Refraction before and after Gravitational Stress

	Before	Immediately After	After 15 min	After 30 min
VA (logMAR)	0.02 ± 0.04	0.19 ± 0.07*	0.05 ± 0.06	0.04 ± 0.07
Refraction (D)	−0.37 ± 0.47			−0.23 ± 0.51

  n = 14 eyes.

*  Statistically significant difference (P < 0.05).

Figure 1.

 

Mean CS before and after +9-Gz force exposure. *Significant differences at P < 0.05.