Vision is one of the most important sensory modalities in humans, and people rely on vision as the primary sensing modality. Visual information seems to be transferred through the visual streams differently based on the location of an object in the visual field rather than on characteristics of an object alone (31). Visual field, the area perceived by the eyes while people fixate on a point, is composed of central and peripheral visual fields. Visual resolution decreases toward the periphery of the visual field. People usually are unaware of this because they direct their gaze to objects in the center of the visual field. However, in sports such as football or basketball, players gather visual information from the periphery of the visual field to see other players and objects beyond the central visual field. Hence, peripheral visual perception may be relevant to performance in sports where peripheral vision plays an important role.
Many sports require high-level visual perceptual skills that are performed under conditions of physiological stress. Recent studies have reported that strenuous exercise impairs peripheral visual perception (1–3,5,6). During strenuous exercise, hyperventilation-induced hypocapnia causes constriction of the arterioles in the brain (25) and leads to a decrease in cerebral oxygenation (4,7). The finding that central neurons sense reduced oxygen delivery and change their activities in response to decreased oxygen availability (21) suggests that a decrease in oxygen availability has the potential to impair visual perceptual performance during exercise. Therefore, the working hypothesis of this review is that a decrease in cerebral oxygenation leads to impairment in peripheral visual perception. Behavioral and physiological data will be presented that support this hypothesis.
ASSESSMENT OF VISUAL PERCEPTION
Visual perception is evaluated by measuring visual reaction time (RT). Visual RT is the time from the appearance of a visual stimulus to the onset of motor output. Visual RT reflects the duration of time necessary to perceive the visual stimulus, select the appropriate response, and select the subsequent programming of the motor response. In a number of studies, RT was fractionated into premotor and motor components based on the onset of electromyogram recordings from a responding muscle (8). The premotor component of RT is called the premotor time and is defined as the time from appearance of a visual stimulus to the onset of muscle activity. The premotor time also can be used to evaluate visual perceptual ability in the central nervous system. In a simple visual RT task, only one visual stimulus is presented, and only one response is required. No irrelevant distractors are presented. In a simple motor response (e.g., press a button with a thumb), there exists no response selection, and the response programming process is considered to be minimal. Therefore, a simple visual RT task using a simple motor response is classified as a visual perceptual task. In a visual perceptual task, changes in RT or premotor time are attributable primarily to changes in visual perception. For these reasons, simple visual RT and premotor time to visual stimuli have been used to assess the effects of acute exercise on visual perception (1–3,5,6).
FACTORS THAT AFFECT VISUAL PERCEPTION
The visual pathway begins with the retina, where photoreceptor cells are distributed nonuniformly (11). Then, visual information is relayed, via thalamus, to the primary visual cortex (35). Thus, the visual pathway from the retina to the visual cortex, which is driven by properties inherent in visual stimulus, is important for visual perception. However, the visual pathway from the retina to the visual cortex is not the sole factor that determines visual perception. Visual attention can be controlled voluntarily by top-down signals derived from task demands (10). Higher cortical areas are known to be involved in the control of visual attention in a top-down manner (10,24), and the control of visual attention affects the neural activity at many stages throughout the visual system (24). Voluntary control of visual attention allows us to orient visual attention to an object in the absence of eye movement, and orienting of visual attention enhances visual perception (e.g. 27). Therefore, visual perception also is influenced by the orienting of visual attention.
ARE EFFECTS OF EXERCISE DIFFERENT BETWEEN CENTRAL AND PERIPHERAL VISUAL PERCEPTION?
The anatomical and functional difference between central and peripheral vision led us to hypothesize that the effects of exercise may be different between central and peripheral visual perception. We performed behavioral studies that examined whether the effects of acute exercise on visual perception are different between the central and peripheral visual fields (2,3). In one study (2), the central visual perception was not affected by exercise at 65% peak oxygen uptake (V˙O2), whereas peripheral visual perception was impaired during exercise at the same workload. These results suggested that peripheral visual perception may be vulnerable to acute exercise compared with central visual perception (2). The finding that visual resolution decreases toward the periphery of the visual field suggests that the vulnerability to exercise may be because of differences in visual resolution between central and peripheral vision. However, in the study (2), visual stimulus was presented exclusively in either the central or peripheral visual field. The participants oriented their visual attention to a narrow area of the visual field when the visual stimulus was presented in the central visual field. In contrast, the participants were required to orient their visual attention to a large area when the visual stimulus was presented in the peripheral visual field. A limitation of the study was that we could not rule out the possibility that the difference in vulnerability to exercise may be because the participants oriented their visual attention in a different area. Therefore, in a follow-up study (3), we tested whether the vulnerability to exercise could be ascribed to low visual resolution.
We hypothesized that if the vulnerability to exercise is associated with visual resolution, the detrimental effects of strenuous exercise on visual perception may be exaggerated toward the periphery of the visual field (3). Visual stimuli were randomly presented at 2, 10, 30, and 50 degrees to either the right or left with equal probability in a within-block manner. Simple visual RT was measured at rest and during cycling at 40% and 75% peak V˙O2. Exercise at 40% peak V˙O2 did not affect visual perception. In contrast, exercise at 75% peak V˙O2 had detrimental effects on both central and peripheral visual perception. However, the detrimental effects on visual perception were not exaggerated toward the periphery of the visual field. This result suggested that the detrimental effects of strenuous exercise were independent of visual resolution (3). In this study, the participants were required to deploy visual attention to a large area of the visual field because visual stimuli were presented within the large area with equal probability. Therefore, the finding that the detrimental effects on visual perception were observed independently of visual resolution raised the possibility that strenuous exercise impairs orienting of visual attention (3). Although differences in visual stimulus, exercise intensity, and duration between the previous studies (2,3) prevented us from concluding that strenuous exercise impairs orienting of visual attention exclusively, strenuous exercise has the potential to impair higher brain activation associated with orienting of visual attention. Physiological factors that are likely to affect peripheral visual perception during strenuous exercise will be discussed later in this article.
PERIPHERAL VISUAL PERCEPTION DURING GRADED EXERCISE
Exercise seems to affect peripheral visual perception. However, exercise intensity where peripheral visual perception is impaired is unclear. The ventilatory threshold (VT) is the point at which ventilation increases disproportionately to oxygen consumption during graded exercise (34). Hyperventilation induced by exercise above the VT leads to a decrease in cerebral oxygenation (4,7). We examined whether peripheral visual perception was impaired at exercise intensities above the VT. Reaction time to peripheral visual stimuli was measured at rest, during graded exercise on a cycle ergometer, and immediately after exercise (1). Peripheral visual perception was not affected during exercise at a low and moderate workload compared with rest. However, exercise at high workloads had detrimental effects on peripheral visual perception (Fig. 1). Further analysis found that peripheral visual perception was impaired at workloads above the VT (1) but not at the VT. This result suggested that a decrease in cerebral oxygenation induced by exercise above the VT could be responsible for the impairment in peripheral visual perception. In addition, impairment in peripheral visual perception was not observed immediately after exercise, which demonstrates that the detrimental effects on peripheral visual perception were observed only during exercise.
Physically fit individuals, who have high oxygen carrying capacity, may be able to compensate for the negative effects of strenuous exercise. Therefore, we examined the relationship between aerobic capacity and impairment in peripheral visual perception (Fig. 2) (1). Delta RT during strenuous exercise was correlated negatively with peak V˙O2 (r2 = 0.54, P < 0.05), indicating that high aerobic capacity attenuated impairment in peripheral visual perception during strenuous exercise. This result suggested that oxygen availability was associated possibly with peripheral visual perception during strenuous exercise.
PERIPHERAL VISUAL PERCEPTION UNDER HYPOXIA
Oxygen delivery to the body tissues is compromised under hypoxic environment. Hypoxia is known to affect the central nervous system (21). Hence, visual perception may be impaired under hypoxia. A few research groups have shown that hypoxia influences visual perceptual performance. In an early study, Fowler and Nathoo (14) reported that severe hypoxia slowed early visual processing at rest. Kobrick and Dusek (17) showed that severe hypoxia had detrimental effects on peripheral visual perception at rest. In contrast, mild hypoxia did not impair peripheral visual perception at rest (5). This may be because of a compensatory increase in cerebral blood flow that maintained oxygen delivery to the brain (18). However, cerebral oxygenation substantially decreased at rest under severe hypoxia despite an increase in cerebral blood flow (16,18). The discrepancy between studies may arise from differences in the severity of hypoxia. In addition, the discrepancy also could be associated with the differences in the presentation locations of the peripheral visual stimuli.
Exercise under hypoxia decreases cerebral oxygenation compared with normoxia (5,16,32). It was hypothesized that if a decrease in cerebral oxygenation compromises peripheral visual perception, peripheral visual perception may be impaired during exercise under hypoxia. The premotor time to peripheral visual stimuli increased to some extent during exercise under hypoxia relative to normoxia, although the differences between normoxia and hypoxia statistically were not significant (Fig. 3) (5). Further analysis was performed to examine the relationship between the decrease in cerebral oxygenation and impairment in peripheral visual perception. Figure 4 represents the relationship between delta premotor time and delta cerebral oxygenation during exercise. Delta premotor time during exercise was negatively correlated with delta cerebral oxygenation during exercise (r2 = 0.89, P < 0.01). This finding suggested that impairment in peripheral visual perception during exercise was associated closely with the decrease in cerebral oxygenation (5).
PERIPHERAL VISUAL PERCEPTION UNDER HYPEROXIA
In contrast to hypoxia, the elevated fraction of inspired oxygen under hyperoxia prevents a decrease in arterial pressure of oxygen and arterial desaturation of oxygen during exercise. Thus, the brain may benefit from enhanced oxygen availability (22). An increase in oxygen availability under hyperoxia seemed to maintain cerebral oxygenation during strenuous exercise (23). This led us to hypothesize that increased oxygen availability prevents the impairment in peripheral visual perception during strenuous exercise. In one study, peripheral visual perception was measured at rest and during and after exercise under normoxia and hyperoxia (Fig. 5). At rest, there was no difference in peripheral visual perception between normoxia and hyperoxia. This result indicated that hyperoxia per se did not affect peripheral visual perception. Notably, strenuous exercise did not have detrimental effects on peripheral visual perception under hyperoxia. In contrast, consistent with previous studies, peripheral visual perception was impaired during strenuous exercise under normoxia. There were no differences in exercise heart rate, V˙O2, ventilation, or ratings of perceived exertion between the normoxia and hyperoxia conditions. These findings suggested that hyperoxia ameliorated the detrimental effects of strenuous exercise on peripheral visual perception (6). The study also found an improvement in peripheral visual perception during moderate exercise under hyperoxia (6). There is limited research in this area, and, therefore, it is difficult to explain why this improvement occurred. Future research should examine underlying mechanisms during exercise under hyperoxia on peripheral visual perception.
DOES CEREBRAL OXYGENATION AFFECT PERIPHERAL VISUAL PERCEPTION DURING EXERCISE?
The Reticular-Activating Hypofrontality Model
Recently, Dietrich and Audiffren (13) proposed a reticular-activating hypofrontality model to account for the psychological consequences of acute exercise. According to this model, exercise facilitates implicit information by enhancing noradrenergic and dopaminergic systems. However, increased activation of motor and sensory systems during strenuous exercise causes higher-order functions of the prefrontal cortex to be disengaged to conserve finite metabolic resources. Therefore, strenuous exercise may cause a downregulation in the brain regions that are not required critically during exercise because metabolic demands become higher in the brain regions associated with exercise. Indeed, the prefrontal cortex seems to be the first region affected by the heavy metabolic burden of exercise (13). Given that higher cortical areas, including the prefrontal cortex, are involved in the control of visual attention (10,24), it is plausible that strenuous exercise impairs orienting of visual attention to a large area of the visual field.
We found that a decrease in cerebral oxygenation was associated with the impairment in peripheral visual perception (5). This notion was supported indirectly by our finding that peripheral visual perception was maintained, even during strenuous exercise, when oxygen availability was increased under hyperoxia (6). Because cerebral oxygenation decreases during strenuous exercise above the VT (4,7), impaired peripheral visual perception during exercise above the VT is aligned with the findings. Furthermore, the finding that peripheral visual perception was not affected after exercise is compatible with the rapid recovery of cerebral oxygenation immediately after exercise (5).
When the brain is activated during exercise, an increase in cerebral oxygen supply is required to match the enhanced level of neuronal metabolism (29). Cerebral oxygenation reflects the balance between oxygen availability and utilization (9). The decrease in cerebral oxygenation during exercise suggests that oxygen availability may be insufficient to meet the metabolic demands of the brain. Recent studies suggest that a decrease in cerebral oxygenation could limit the central motor output during exercise under hypoxia (33) or after administration of beta-blocker propranolol (30). Only a few studies have examined the relationship between cerebral oxygenation and visual perceptual performance during exercise. Therefore, it may be premature to conclude that a decrease in cerebral oxygenation is the primary mechanism that limits peripheral visual perception. However, because central neurons sense reduced oxygen delivery and change their activities in response to decreased oxygen availability (21), it is tentatively suggested that a decrease in cerebral oxygenation during strenuous exercise has the potential to compromise brain metabolism associated with peripheral visual perception.
Alternatively, a decrease in oxygen availability may affect the level of neurotransmitters in the brain. Neurotransmitters play a crucial role in the maintenance of physiological function at cellular and organ levels. The turnover of several neurotransmitters seems to be altered under hypoxia, despite the preserved state of brain energy stores (28). For example, the synthesis of acetylcholine (15) and serotonin (12) is sensitive to oxygen availability. Therefore, hypoxia-induced changes in the levels of neurotransmitters also could underlie the detrimental effects of exercise on peripheral visual perception. Figure 6 summarizes the proposed hypothesis that explains why exercise above the VT or under hypoxia affects peripheral visual perception. This hypothesis is tentative still, and whether this is cause and effect or merely association has not been determined. Future studies are necessary to clarify the causal links between physiological changes during exercise and impaired peripheral visual perception.
Exercise has been shown to induce several physiological changes in the central nervous system, including circulatory, metabolic, and neurohormonal effects (19,20,26). This suggests that multiple factors are likely to be associated with impairment in peripheral visual perception during exercise. Therefore, to understand the way in which strenuous exercise affects peripheral visual perception, it is necessary to use various research techniques to explore how strenuous exercise affects peripheral visual perception. The combination of different neuroimaging methods may be a powerful approach to identify physiological mechanisms that affect peripheral visual perception during strenuous exercise. Specifically, multi-channel near-infrared spectroscopy would provide information on regional oxygenation in discrete brain areas, whereas neuroimaging would allow us to examine how cortical and subcortical areas are influenced during strenuous exercise. Electrophysiological and neuroendocrinological studies using both human and animal models also will help us elucidate the mechanism(s) involved in the association between strenuous exercise and decreased peripheral visual perception. Finally, because this review focused exclusively on the association between cerebral oxygenation and peripheral visual perception, the effects of acute exercise on visual information processing at early visual processing stages (e.g., retina) should be investigated.
The present review addressed how acute exercise affects peripheral visual perception. Recent findings demonstrated that strenuous exercise has detrimental effects on peripheral visual perception. Peripheral visual perception was impaired during exercise and was associated with a decrease in cerebral oxygenation. In contrast, peripheral visual perception was not impaired during strenuous exercise when oxygen availability was increased under hyperoxia. Irrespective of the underlying mechanisms, a decrease in cerebral oxygenation is likely to be associated with impairment in peripheral visual perception during strenuous exercise. Future studies will allow us to determine potential physiological mechanisms that explain the impairment of peripheral visual perception during strenuous exercise.
The author is grateful to the collaborators who contributed to the studies discussed in this article, especially to Dr. Kokubu M. and Prof. Oda S. for valuable comments and support. The author thanks Grants-in-Aid for JSPS Fellows and Young Scientists (B) for support of the research discussed herein. The author recognizes the work of many other researchers that could not be cited because of the reference limitations.
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Keywords:©2013 The American College of Sports Medicine
peripheral vision; cerebral oxygenation; near-infrared spectroscopy; hyperventilation; hypoxia; hyperoxia