How breathing disrupts vision: hyperventilation-induced hypocapnia impairs oculomotor responses in resting humans.

Eye movements are precisely controlled by the brain to acquire clear and stable visual information, and eye movement measurements are also used as neurophysiological biomarkers. Hyperventilation, which reduces arterial carbon dioxide partial pressure (hypocapnia) and cerebral perfusion, can be triggered by environmental or psychological stress or by chronic disease conditions. Here, we hypothesized that hyperventilation-induced hypocapnia would impair oculomotor responses in resting humans. Thirteen healthy young adults (eight females) performed a free-viewing task and an anti-saccade task under three breathing conditions: spontaneous breathing, voluntary hypocapnic hyperventilation and voluntary normocapnic hyperventilation. Eye movements were recorded using video-based eye tracking, whilst end-tidal carbon dioxide partial pressure and middle cerebral artery mean blood velocity were continuously monitored via a metabolic cart and transcranial Doppler ultrasound, respectively. Hypocapnic hyperventilation reduced end-tidal carbon dioxide partial pressure to ∼20 mmHg, with a concurrent 24 ± 10 cm/s reduction in middle cerebral artery blood flow (both P < 0.001). Hypocapnic hyperventilation also reduced the number of fixations and saccades, and scanpath length, whereas it increased fixation duration in the free-viewing task (all P < 0.01). The aforementioned responses mediated by hypocapnic hyperventilation were not observed under spontaneous breathing or normocapnic hyperventilation conditions (all P > 0.11). In the anti-saccade task, both normocapnic and hypocapnic hyperventilation prolonged latency (both P < 0.01), with hypocapnic hyperventilation exhibiting greater impairment (P < 0.001). We show that hyperventilation-mediated hypocapnia impairs oculomotor responses by attenuating visual fixation and saccadic control in resting humans. Also, hyperventilation per se independently of hypocapnia impairs saccadic control. KEY POINTS: Eye movements, such as fixations and saccades, are essential for visual stability and object tracking in daily life. Hyperventilation, which causes hypocapnia and cerebral hypoperfusion, can occur during physiological or psychological stress or in individuals with chronic disease. In this study we demonstrated that acute voluntary hypocapnic, but not normocapnic, hyperventilation impaired visual fixation variables, including the number of fixations and saccades, fixation duration and scanpath length. Both hypocapnic and normocapnic hyperventilation impaired the latency of anti-saccades, with hypocapnic hyperventilation causing a more pronounced impairment. We conclude that (1) hypocapnia induced by hyperventilation may impair oculomotor responses by weakening visual fixation and saccadic control, and (2) hyperventilation itself can also impair saccadic control. These oculomotor impairments associated with hypocapnic hyperventilation might increase the risk of injury or death in tasks that require precise visuomotor coordination.