Stabilization of gaze during circular locomotion in darkness II. Contribution of velocity storage to compensatory eye and head nystagmus in the running monkey

1. Yaw eye in head (Ė(h)) and head on body velocities (Ḣ(b)) were measured in two monkeys that ran around the perimeter of a circular platform in darkness. The platform was stationary or could be counterrotated to reduce body velocity in space (Ḃ(s)) while increasing gait velocity on the platform (Ḃ(p)). The animals were also rotated while seated in a primate chair at eccentric locations to provide linear and angular accelerations similar to those experienced while running. 2. Both animals had head and eye nystagmus while running in darkness during which slow phase gaze velocity on the body (Ġ(b)) partially compensated for body velocity in space (Ḃ(s)). The eyes, driven by the vestibuloocular reflex (VOR), supplied high-frequency characteristics, bringing Ġ(b) up to compensatory levels at the beginning and end of the slow phases. The head provided substantial gaze compensation during the slow phases, probably through the vestibulocollic reflex (VCR). Synchronous eye and head quick phases moved gaze in the direction of running. Head movements occurred consistently only when animals were running. This indicates that active body and limb motion may be essential for inducing the head-eye gaze synergy. 3. Gaze compensation was good when running in both directions in one animal and in one direction in the other animal. The animals had long VOR time constants in these directions. The VOR time constant was short to one side in one animal, and it had poor gaze compensation in this direction. Postlocomotory nystagmus was weaker after running in directions with a long VOR time constant than when the animals were passively rotated in darkness. We infer that velocity storage in the vestibular system had been activated to produce continuous Ė(h) and Ḣ(b) during running and to counteract postrotatory afterresponses. 4. Continuous compensatory gaze nystagmus was not produced by passive eccentric rotation with the head stabilized or free. This indicates that an aspect of active locomotion, most likely somatosensory feedback, was responsible for activating velocity storage. 5. Nystagmus was compared when an animal ran in darkness and in light. The beat frequency of eye and head nystagmus was lower, and the quick phases were larger in darkness. The duration of head and eye quick phases covaried. Eye quick phases were larger when animals ran in darkness than when they were passively rotated. The maximum velocity and duration of eye quick phases were the same in both conditions. 6. The platform was counterrotated under one monkey in darkness while it ran in the direction of its long vestibular time constant. This raised its rate of locomotion and reduced its Ḃ(s). Head and eye nystagmus was present continuously, and there was after-nystagmus. Gaze gains could be larger than unity during the initial phases of the increased locomotor activity, but as running continued, Ġ(b) was more closely related to Ḃ(s) than to Ḃ(p). This shows that the animal was able to estimate its inertial Ḃ(s) in the absence of vision and with conflicting somatosensory and vestibular cues. It is consistent with the hypothesis that Ġ(b) is driven by a derived estimate of Ḃ(s). 7. We conclude that there is an innate pattern of head-eye coordination that supports gaze compensation in the freely moving animal in the absence of vision. This pattern depends on activation of velocity storage, which might be excited by vision, semicircular canal and somatosensory inputs, inputs related to linear acceleration, pitching the head, and/or efference copy. We infer that an important function of velocity storage is to support gaze compensation during locomotion.