Ocular Responses and Visual Performance after Emergent Acceleration Stress

Abstract

Purpose.: To evaluate visual function after emergent acceleration stress.

Methods.: Sixteen subjects were enrolled in this study. Human ejection seat trainer was used to induce six times gravitational force in the head-to-toe (z-axis) direction (+6 Gz). Visual performance was evaluated using the visual chart and contrast sensitivity (CS) at indicated times. Ocular reactions were assessed with biomicroscopy and topographic mapping.

Results.: Temporary visual acuity reduction (0.02 ± 0.05 vs. 0.18 ± 0.08 logMAR visual acuity [VA]; P < 0.05) and ocular reactions were observed after ejection. These reactions included changes in increasing anterior chamber depth (ACD; 3.18 ± 0.29 vs. 4.48 ± 0.32 mm; P < 0.05) and pupillary dilation (PD; 3.56 ± 0.72 vs. 5.64 ± 0.56 mm; P < 0.05). The ACD deepening continued at 15 minutes (4.37 ± 0.26 mm; P < 0.05), and PD persisted at 30 minutes after the gravitational stress (5.42 ± 0.54 mm, P < 0.05). CS decreased significantly at all spatial frequencies immediately after ejection. However, CS returned to the initial range at high spatial frequency by 30 minutes.

Conclusions.: Emergent acceleration force induces significant ocular responses and visual fluctuation. Prolonged ACD deepening (>15 minutes) and PD (>30 minutes) were noted, but cornea and refraction remain stable. CS at all spatial frequencies revealed remarkable reduction immediately after ejection, and recovered to baseline levels within 30 minutes only at high spatial frequency. Neuroretinal function may involve visual fluctuation after acceleration stress, because visual fluctuation corresponds with the characters of neuroretinal function. However, further studies are necessary.

Human exposure to emergent acceleration stress in daily real-life activities (e.g., traffic, sports, accidental events) and its effects on visual function is the subject of this study. When humans undergo an emergency at high acceleration stress, vision plays a key part in preventing further catastrophe, as the response time is relatively short. ^{1 –3} With increases in acceleration-related events, understanding of visual performance and ocular response may enhance the safety and survival of individuals who undergo an emergent acceleration event in real life. 

Although the effect of the acceleration force on the ocular responses and visual performance have been studied previously, more research work is still needed. In particular, past studies have reported that high gravitational exposure can lead to visual impairment, such as gray out, blackout, and loss of peripheral vision. ^4,5 However, the preceding results are usually based on subjective descriptions and are not quantitative due to the difficulty in designing experiments. 

In our past investigation, we observed that subjects developed persistent ocular structure responses and contrast sensitivity impairment at low and medium spatial frequency at 30 minutes after centrifugation (+9 Gz). ⁶ However, the amount of contrast sensitivity (CS) changes, at all spatial frequencies and immediately after centrifugation, remained unknown. Moreover, centrifugation-induced gravitational exposure did not fully reveal the real condition of the emergent acceleration events in real life due to its gradual onset and long duration. Crises at high gravitational stress that happened to individuals in daily activity are usually sudden and transient such as sport, traffic, and accidental events. However, the gravitational stress induced in a human centrifuge at +9 Gz force is gradual in onset (65 seconds). Moreover, the persistence in duration is not transient but long (15 seconds). ⁶ Furthermore, antigravity (anti-G) force equipment is necessary for individuals exposed to centrifugation gravitational stress such as oxygenation or an anti-G suit. ^5,6 Nevertheless, individuals are usually not equipped with anti-G force preparation in real life. Therefore, it is required to develop another model to simulate a real emergent acceleration event and to further clarify the ocular responses and visual performance in an individual undergoing an emergent gravitational stress. 

With advances in technology, the human ejection seat trainer was developed to simulate sudden and transient acceleration stress. ⁷ The trainer is designed to improve the pilots' learning experience during escape ejection under emergent gravitational exposure. The desired acceleration force recommended for optimal training can be accurately adjusted according to the trainee's weight. ^7,8  

In this study, a human ejection seat trainer was used to elicit an acceleration force set at six times G-force in the head-to-toe z-axis direction (+6 Gz force). The influence of G-force on visual performance was assessed by measuring visual acuity and CS at all spatial frequencies. The changes in ocular responses were evaluated by biomicroscopy, physical examinations, and corneal topography. The effects of ocular responses on visual performance were investigated as well. 

Materials and Methods

Sixteen healthy males, aged 22–24 years (mean age 23.3 ± 0.8), were enrolled in the study. All subjects before simulated ejection had normal vision (6/6 or better), clear ocular media, and no ocular disease. They were in good general health as assessed by an ophthalmologist (C-TH). The investigation was conducted in accordance with the requirements of the ARVO statement and the tenets of the Declaration of Helsinki. Ethical approval for this study was obtained from the institutional review board. 

Before ejection, each subject underwent a complete ocular examination that included tests of visual acuity (early treatment of diabetic retinopathy [ETDRS], logMAR chart), refraction (AR310; Nidek, Tokyo, Japan), and examination with a biomicroscope. The letter stimuli of the ETDRS logMAR chart in this study were printed on an illuminated cabinet (background luminance, 350 cd/m²). The chart had five letters per row ranging in size from 1.0 to −0.30 logMAR. Visual acuity was tested at 4 m distance. A corneal topograph (Orbscan II; Bausch & Lomb, Rochester, NY) was used to assess the various ocular responses including maximum K and minimum K values (Sim K), anterior best-fit sphere (BFS), posterior BFS, anterior chamber depth (ACD), pupillary diameter (PD), and central corneal thickness (CCT). Macular responses such as metamorphopsia were detected using the Amsler grid test, and visual performance was assessed further by testing CS. CS was tested monocularly before and after +6 Gz exposure with a contrast sensitivity test chart (VCTS 6500; Vistech Consultants, Inc., Dayton, Ohio). The test chart consisted of 45 circular targets with gratings of different sizes and contrast. The target size in the distance test was 7.5 cm. The gratings in the targets were vertical or 15° left or right from the vertical direction. In the test chart, the contrast decreased horizontally from left to right and the gratings became smaller vertically from top to bottom (from 1.5 to 18 cycles per degree [CPD]; from target A to target E). The testee began at the top horizontal line A and stated whether the gratings in targets 1 through 9 were vertical, left, or right. The last target that the testee reported correctly was marked down on a result paper provided for the test. The same procedure was repeated in all other horizontal test lines from B to E. During the measurement, the room luminance was approximately 200 cd/m² and the test distance was 3 m. 

After these examinations, experiments were conducted on an ejection seat trainer (EST; Aviation Psychological Research Laboratory, Gangshan Armed Forces Hospital, Kaohsiung, Taiwan) where the subjects received ejection simulation at ground level. The EST in this study included a simulated cockpit equipped with a catapult system, an ejection seat, and a vertical rail (Fig. 1). The ejection seat was engaged on the vertical rail tract. Safety interlocks were set at the distal end of the vertical rail to ensure the subject's safety. The EST could simulate a sudden and transient acceleration stress from 1g to 7g. Before ejection, the ejection seat was mounted in the cockpit and fixed to the vertical rail. The subject sat in upright position and fastened the seatbelt on the ejection seat. After that, the subject pulled the catapult switch up in the EST by himself, and then the catapult system in the simulated cockpit catapulted the subject up along the vertical rail to simulate an emergent acceleration stress. 

Figure 1.

 

Schematic drawing of the ejection seat system. The EST includes an ejection seat, a vertical rail, and a simulated cockpit-equipped catapult system.

In this experiment, the ejection seat was set to eject at +6 Gz force for 0.2 seconds duration by aviation physicians according to the body weight of each subject. There was no decelerator or brake system present in the vertical rail. The subject was ejected upwards about 8 meters in approximately 1.4 seconds, and stopped only by the gravity. After ejection, the delivery system sent the subject and seat to the initial position via a vertical rail without minus gravitational force. 

Visual acuity as well as refraction was checked and the corneal topograph (Orbscan II; Bausch & Lomb) was applied again immediately, 15 minutes, and 30 minutes after the ejection. CS was measured immediately after and 30 minutes after the gravitational stress. Fundus examination was performed at 2 hours after ejection. All data were collected and analyzed. All results are expressed as the mean ± SD. A paired t-test was used to compare the related parameters before and after simulated ejection; a P value < 0.05 was accepted as significant. 

Results

All data were collected from 16 eyes. We observed that cornea-related parameters such as anterior BFS, posterior BFS, Sim K, and CCT did not change significantly from before to after ejection (Table 1). 

Table 1.

 

Changes of Cornea-Related Parameters before and after Simulated Ejection

	Before Ejection	Just after Ejection	15 Min after Ejection	30 Min after Ejection
Sim K
Maximum	44.24 ± 0.41	45.20 ± 0.85	45.00 ± 1.25	44.68 ± 1.50
Minimum	43.38 ± 1.66	44.82 ± 0.58	44.24 ± 0.41	44.32 ± 0.98
Anterior BFS, D	43.04 ± 1.37	42.82 ± 1.24	42.89 ± 0.67	43.05 ± 1.24
Posterior BFS, D	52.43 ± 2.05	52.00 ± 2.25	52.06 ± 0.93	52.38 ± 1.44
Central corneal depth, μm	553.5 ± 21.7	561.5 ± 17.7	560.3 ± 20.5	557.1 ± 24.5

 D, diopter.

ACD deepened considerably immediately after (3.18 ± 0.29 vs. 4.48 ± 0.32 mm, P < 0.05) and 15 minutes after (4.37 ± 0.26; P < 0.05) +6 Gz force stress. ACD returned to the pretest value by 30 minutes after acceleration exposure (3.23 ± 0.31 mm; P > 0.05) (Table 2). 

Table 2.

 

Anterior Chamber Depth before and after Simulated Ejection

Examination Time	Before Ejection	Just after Ejection	15 Min after Ejection	30 Min after Ejection
ACD, mm	3.18 ± 0.29	4.48 ± 0.32*	4.37 ± 0.26*	3.23 ± 0.31

  n = 16 eyes.

*  Statistically significant differences when P < 0.05.

PD enlarged significantly immediately after (3.56 ± 0.72 vs. 5.64 ± 0.56 mm; P < 0.05) and 15 minutes (5.47 ± 0.64 mm; P < 0.05) after ejection. PD remained enlarged 30 minutes after acceleration exposure (5.42 ± 0.54 mm; P < 0.05) (Table 3). Refraction remained stable before, immediately after, 15 minutes after, and 30 minutes after gravitational stress (Table 4). 

Table 3.

 

Papillary Diameter before and after Simulated Ejection

Examination Time	Before Ejection	Just after Ejection	15 Min after Ejection	30 Min after Ejection
Papillary diameter (mm)	3.56 ± 0.72	5.64 ± 0.56*	5.47 ± 0.64*	5.42 ± 0.54*

  n = 16 eyes.

*  Statistically significant differences when P < 0.05.

Table 4.

 

Visual Acuity and Refraction before and after Simulated Ejection

	Before Ejection	Just after Ejection	15 Min after Ejection	30 Min after Ejection
VA LogMAR	0.02 ± 0.05	0.18 ± 0.08*	0.04 ± 0.09	0.04 ± 0.06
Refraction, D	−0.35 ± 0.46	−0.27 ± 0.50	−0.28 ± 0.43	−0.24 ± 0.49

*  Statistically significant differences when P < 0.05.

In the visual performance test, transient visual acuity decreased immediately after the gravitational stress (0.02 ± 0.05 vs. 0.18 ± 0.07 logMAR VA; P < 0.05) (Table 4). CS reduction was also observed immediately after acceleration exposure, and a significant depression of CS was found at all spatial frequencies. CS in the right eye decreased at 1.5 CPD (P < 0.05), 3.0 CPD (P < 0.05), 6.0 CPD (P < 0.05), 12.0 CPD (P < 0.05), and 18.0 CPD (P < 0.05) (Fig. 2). CS reduction was also observed at 30 minutes after acceleration exposure, and significant depression of CS was found at low and medium frequencies. CS in the right eye decreased at 1.5 CPD (P < 0.05), 3.0 CPD (P < 0.05), and 6.0 CPD (P < 0.05) (Fig. 3). The Amsler grid examination revealed no particular finding, such as metamorphopsia, in any subject. 

Figure 2.

 

Mean CS before and immediately after simulated ejection (+6 Gz force exposure). *Significant differences at P < 0.05.

Figure 3.

 

Mean CS before and at 30 minutes after simulated ejection (+6 Gz force exposure). *Significant differences at P < 0.05.

Throughout the experiment, the 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, the maps of the anterior and posterior BFS did not show significant changes. This finding suggests that the corneal curvature remained stable before and after + 6 G-force exposure. Our studies also discovered that no remarkable pachymetric changes occurred. However, this observation was different from our past finding where we observed a 10% increase in CCT after +9 Gz force exposure. ⁶ In our previous study, the acceleration force induced by centrifuge was slow, at higher magnitude (+9 Gz), and sustained for 15 seconds, whereas the gravitational stress induced by the ejection seat was sudden and transient. Moreover, this acceleration force in the present study is less in magnitude (+6 Gz) than that in the previous study. Therefore, we observed unremarkable pachymetric results. Furthermore, previous studies have shown that when corneal edema occurred, the posterior aspect of the cornea thickens more than the anterior aspect because the anterior corneal stroma has less capacity to thicken than does the posterior stroma. ^{9 –12} In this study, anterior BFS remained constant at immediately, 15 minutes, and 30 minutes after simulated ejection. Furthermore, posterior BFS showed no specific changes at all above the indicated time. This finding further confirmed that the cornea did not show any associated change in corneal thickness before or after sudden and transient gravitational stress (+6 Gz). In addition, our current and previous observations also suggest that magnitude and exposure time of acceleration force may play a role in the maintenance of corneal clarity and curvature after acceleration exposure. 

In this investigation, a significantly prolonged PD increase was noted for 30 minutes after high G-force exposure. Prolonged autonomic nervous systemic activity and neurohormonal regulation may account for this finding. Previous studies showed that gravitational stress can increase sympathetic tone to prevent body fluid from shifting downward with gravity. ¹³ Nevertheless, this transient sympathetic tone elevation only explains the early pupil dilation immediately after simulated ejection. Tran et al. ¹⁴ reported that high G-force exposure causes a persistent reduction in parasympathetic activity. This prolonged autonomic nervous activity may take part in persistent pupil enlargement after gravitational stress. Besides, neurohormonal regulation may also be involved in persistent pupil dilation. A previous study revealed that gravitational stress increases somatostatin concentration in blood. Yamaji et al. ¹⁵ found that somatostatin may induce persistent mydriasis by attenuating cholinergic neurotransmitter release. Therefore, neurohormonal regulation may also play a role in this prolonged pupil enlargement. 

In our experiment, the ACD became deeper immediately and 15 minutes after +6 Gz force exposure but returned to the baseline value within 30 minutes after gravitational stress. Pupil enlargement might explain the ACD deepening at 15 minutes after gravitational stress, but it cannot explain why the ACD returned to the initial value when mydriasis persisted 30 minutes after simulated ejection. Moreover, ACD deepening (4.48–4.37 mm) found in this study is even deeper than the pharmacologic mydriasis-induced ACD deepening (<3.36 mm) in a previous report. ¹⁶ In addition to pupillary mydriasis, we assumed that iris root rotation resulting from ejection-induced deformation of corneoscleral shell may play a role in prolonged ACD deepening. It has been previously reported that localized ocular indentation could lead to ocular globe deformation. ¹⁷ Patel et al. ¹⁸ reported that regional scleral deformation could be induced by focal scleral indentation with fixed force (approximately 0.055 N). Delori et al. ¹⁹ showed that high-speed impact may lead to globe deformation. Because of different bulk modulus between eyeball and its surrounding tissues, Cirovic et al. ²⁰ reported that deformation of ocular globe may be caused by the forces (approximately 5 N) from the surrounding tissues after exposure to high acceleration or deceleration. Besides, many experimental and computational studies have shown that globe deformation may lead to changes in the iris profile. Amini and Barocas ¹⁷ found that corneoscleral indentation might result in posterior rotation of the iris root and cause posterior bowing of the iris. Therefore, Takanashi et al. ²¹ reported that scleral indentation could open the anterior chamber angle and consequently improve angle visualization. It has also been shown that after globe-deformation-induced iris root rotation, the aqueous humor could be trapped in the anterior chamber and cause reverse pupillary block. ²² In this study, the eyeball might have been deformed by the ejection-induced forces (approximately 4.5 N, where eyeball mass was 7.5g and acceleration stress was +6 Gz). This ejection-induced eyeball deformation could have led to aqueous trapped in anterior chamber and a reverse pupillary block status. Because aqueous humor was trapped in the anterior chamber due to a flap-valve-like effect (reverse pupillary block) caused by higher pressure in the anterior chamber, ²³ a prolonged ACD deepening was observed after +6 Gz gravitation stress. 

With time, the trapped aqueous humor in the anterior chamber was drained and the new aqueous formed in the posterior chamber. We detected the ACD gradually returned to its baseline level within 30 minutes. In this study, the ACD changed from 3.2 mm up to 4.8 mm (4.48 ± 0.32) immediately after the ejection. We estimated the amount of aqueous humor transferred to the anterior chamber would be roughly approximately 25 to 100 μL (shifted aqueous = πr ² × [4.8–3.2]; where πr ² = base area; minimum r approximately 2.5 mm, minimum r approximately [dilated pupil diameter]/2; maximum r approximately 5 mm, maximum r approximately [cornea diameter[/2; height difference = [4.8–3.2]). If aqueous humor drains via the trabecular meshwork with the rate of 2.5 μL per minute, ²⁴ it will takes approximately 10 to 40 minutes (25/2.5; 100/2.5) for the system to reach equilibrium. Hence, we observed the ACD deepening at 15 minutes and back to its initial range at 30 minutes after ejection. In addition, we also observed that the refractive power did not change significantly throughout the experiment. Based on the physical laws of optics, increasing ACD should lead to changes in the refractive index of the eye. In this study, the ACD revealed varied values at different time points but refraction remained stable. These observations suggest that sudden and transit acceleration force (+6 Gz) is not enough to fully disturb accommodation function. However, we did not evaluate any quantitative measurements of the anterior and posterior lens diameter or lens thickness due to limited facilitation. Additional research is required to elucidate on these findings, as there are no previous reports on this issue. 

Although much work has been done, ^5,6 the effects of G-force stress on visual performance has not been fully studied. In this work, visual acuity showed a transient VA reduction immediately after ejection and returned to baseline 15 minutes after +6 Gz force exposure. However, the ocular anterior chamber changes we observed in this study are not enough to explain this finding, because ACD deepening persisted for 15 minutes and mydriasis persisted for 30 minutes. Furthermore, the Amsler grid examination revealed unremarkable results, suggesting that the macular function was not compromised even after the urgent acceleration exposure. Therefore, CS was applied to evaluate the possible mechanism to explore this transient visual impairment because we assumed that the changes in the neuroretinal function might play a role in this observation. Previous studies have reported that magno- and parvocellular ganglion cells make different contributions to visual performance. ²⁵ Damage to the magnocellular pathway has little effect on visual acuity, but it significantly reduces motion vision and contrast sensitivity at low spatial frequency. In contrast, damage to the parvocellular pathway has no effect on motion perception but it severely impairs visual acuity and contrast sensitivity at high spatial frequency. ^{25 –28}  

In this study, we observed that CS reduction persists for > 30 minutes at low and medium frequency but remains stable at high spatial frequency. Because the magnocellular pathway contributes to contrast sensitivity at low spatial frequency, our observation suggests that acute gravitational stress may compromise magnocellular function for 30 minutes and lead to CS reduction at low spatial frequency at 30 minutes after gravitational stress. Kawai et al. ²⁹ have demonstrated that gravitational stress can cause body fluid to shift toward the lower body, which decreases ocular blood flow and leads to hypoxia. ³⁰ Previous studies have reported that hypoxia may compromise neuroretinal function and result in prolonged CS reduction. ^25,27,31,32 Chou et al. ⁵ report that centrifugation-induced gravitational stress can lead to prolonged CS loss at low and medium spatial frequency for 30 minutes. Our results parallel with previous reports. ^5,6 However, many issues about visual fluctuation after gravitational stress were still undetermined because the CS changes right after gravitational stress remained unknown in our past study. CS at low and medium spatial frequency revealed significant reduction at 30 minutes after ejection, which may be because, at low and medium spatial frequency, it decreased progressively within 30 minutes or immediately after ejection. Moreover, CS at high spatial frequency revealed insignificant changes at 30 minutes after ejection, which may result from CS at high spatial frequency recovering progressively within 30 minutes or remaining steady after ejection. To clarify our previous findings further, we evaluated CS not only at 30 minutes but also immediately after ejection in this study. 

In this investigation, we found remarkable CS impairment not only at low spatial frequency but also at high spatial frequency immediately after ejection. This result demonstrated that CS at low spatial frequency was compromised immediately and did not recovery within 30 minutes after ejection. Besides, this finding also indicated that CS at high spatial frequency was compromised immediately but returned to baseline at 30 minutes after acceleration exposure. Because parvocellular function mainly contributed to CS at high spatial frequency, this observation suggested that parvocellular function was also impaired immediately after ejection but recovered within 30 minutes. Previous research has also reported that oxygen demand in the affected magnocellular and parvocellular pathways is different. ³³ Moreover, DiLeo et al. ³⁴ reported that hypoxia may affect parvocellular ganglion cells less severely than magnocellular ganglion cells. Harris et al. ³⁵ showed that hyperoxic conditions significantly improve CS, especially at high spatial frequency in the patient with minimal diabetic change retina. Therefore, we found that CS at low and medium spatial frequency decreased constantly, but at high spatial frequency it recovered within 30 minutes after ejection. Because visual acuity is mainly contributed by parvocellular function, we herein observed a temporary but not prolonged visual acuity reduction on the ETDRS chart in this study. 

To sum up this investigation, we found that emergent acceleration force can induce notable ocular anterior segment reactions, such as prolonged ACD deepening and pupil mydriasis. However, corneal curvature and thickness remained unchanged. We also observed that CS at all spatial frequencies revealed remarkable reduction right after acceleration stress, and recovered to baseline levels within 30 minutes only at low spatial frequency. Our observations provide valuable information for the developments of sport visual science and aviation medicine. These findings also offer practical information for individuals in acceleration missions, events, or accidents to be prepared and to prevent further injury in real life. Moreover, the visual fluctuation that we observed in this study corresponds with the characteristics of parvocellular and magnocellular function. We suggest that neuroretinal function may play a role in the pathogenesis of visual fluctuation after gravitational stress in addition to ocular responses. However, further research is necessary to fully elucidate the mechanism of visual fluctuation after emergent gravitational stress. 

Footnotes

 Supported by grants from the 2006 Research and Development Fund of Kaohsiung Military General Hospital, the Tri-Service General Hospital (TSGH-C98-69; TSGH-C99-88; TSGH-C101-103), and Teh-Tzer Foundation.

Footnotes

 Disclosure: M.-L. Tsai, None; C.-T. Horng, None; C.-C. Liu, None; P. Shieh, None; C.-L. Hung, None; D.-W. Lu, None; S.-Y. Chiang, None; Y.-C. Wu, None; W.-Y. Chiou, None