Evidence for a retinal velocity memory underlying the direction of anticipatory smooth pursuit eye movements

To compute spatially correct smooth pursuit eye movements, the brain uses both retinal motion and extraretinal signals about the eyes and head in space ( Blohm and Lefèvre 2010 ). However, when smooth eye movements rely solely on memorized target velocity, such as during anticipatory pursuit, it is unknown if this velocity memory also accounts for extraretinal information, such as head roll and ocular torsion. To answer this question, we used a novel behavioral updating paradigm in which participants pursued a repetitive, spatially constant fixation-gap-ramp stimulus in series of five trials. During the first four trials, participants' heads were rolled toward one shoulder, inducing ocular counterroll (OCR). With each repetition, participants increased their anticipatory pursuit gain, indicating a robust encoding of velocity memory. On the fifth trial, they rolled their heads to the opposite shoulder before pursuit, also inducing changes in ocular torsion. Consequently, for spatially accurate anticipatory pursuit, the velocity memory had to be updated across changes in head roll and ocular torsion. We tested how the velocity memory accounted for head roll and OCR by observing the effects of changes to these signals on anticipatory trajectories of the memory decoding (fifth) trials. We found that anticipatory pursuit was updated for changes in head roll; however, we observed no evidence of compensation for OCR, representing the absence of ocular torsion signals within the velocity memory. This indicated that the directional component of the memory must be coded retinally and updated to account for changes in head roll, but not OCR.

Revealing the Kinematics of the Oculomotor Plant With Tertiary Eye Positions and Ocular Counterroll

Retinal information is two-dimensional, whereas eye movements are three-dimensional. The oculomotor system solves this degrees-of-freedom problem by constraining eye positions to zero torsion (Listing's law) and determining how eye velocities change with eye position (half-angle rule). Here we test whether the oculomotor plant, in the absence of well-defined neural commands, can implement these constrains mechanically, not just in a primary position but for all eye and head orientations. We stimulated the abducens nerve at tertiary eye positions and when ocular counterroll was induced at tilted head orientations. Stimulation-induced eye velocities follow the half-angle rule, even for tertiary eye positions, and microstimulation at tilted head orientations elicits eye positions that adhere to torsionally shifted planes, similar to naturally occurring eye movements. These results support the notion that oculomotor plant can continuously apply these three-dimensional rules correctly and appropriately for all eye and head orientations that obey Listing's law, demonstrating a major role of peripheral biomechanics in motor control.