Organizational principles of velocity storage in three dimensions. The effect of gravity on cross-coupling of optokinetic after-nystagmus.

1. Optokinetic nystagmus was elicited in alert monkeys by movement of the visual surround in their horizontal or yaw plane, and optokinetic after-nystagmus was recorded in darkness. The animals were upright or were statically tilted at various angles from the upright. While upright, the OKAN was horizontal, and there were no vertical or roll components. When animals were tilted to either side or forward or back, vertical or roll components appeared both in the primary and secondary OKAN. Such components were also observed during nystagmus and after-nystagmus induced by electrical stimulation of the nucleus of the optic tract. The characteristics of the cross-coupled components indicated that they were mediated through the velocity storage mechanism in the vestibulo-ocular reflex. 2. A principle was inferred that explained the appearance of cross-coupled vertical or roll components in the primary and secondary OKAN: With the animal in a tilted position, a vector of eye velocity during OKN along the body-vertical axis was converted during primary OKAN toward a spatial-vertical axis with the same sense by a right hand rule. Thus, slow phase velocity along a vector toward the top of the animal's head during horizontal OKN rotated so that it tended to be directed spatially upward during primary OKAN. The reverse was true for OKN with a velocity vector directed toward the animal's feet. It rotated during primary OKAN so that it tended to be aligned with the direction of gravity. The vector of velocity during secondary OKAN was opposite to the direction of the vector during primary OKAN and was approximately aligned with spatial vertical. 3. OKN and OKAN were elicited about the animal's pitch and roll axes while they were upright and statically tilted at various angles away from the spatial vertical. There was a graded increase in the strength of vertical and roll OKN and OKAN and in the falling time constant of OKAN as the animals were tilted so that the axis of pitch or roll eye movements was moved toward alignment with the spatial vertical. Thus, velocity storage during pure vertical and roll nystagmus was similar to that during yaw OKN and OKAN in tilted positions: it was maximal along the pitch and roll axes when these axes were aligned with gravity. 4. The data indicate that the gravitational field is of fundamental importance in imposing a spatial reference onto the velocity storage integrator.(ABSTRACT TRUNCATED AT 400 WORDS)