Role of muscle pulleys in producing eye position-dependence in the angularvestibuloocular reflex: A model-based study

It is well established that the head and eye velocity axes do not always al ign during compensatory vestibular slow phases. It has been shown that the eye velocity axis systematically tilts away from the head velocity axis in a manner that is dependent on eye-in-head position. The mechanisms responsi ble for producing these axis tilts are unclear. In this model-based study, we aimed to determine whether muscle pulleys could be involved in bringing about these phenomena. The model presented incorporates semicircular canals , central vestibular pathways, and an ocular motor plant with pulleys. The pulleys were modeled so that they brought about a rotation of the torque ax es of the extraocular muscles that was a fraction of the angle of eye devia tion from primary position. The degree to which the pulleys rotated the tor que axes was altered by means of a pulley coefficient. Model input was head velocity and initial eye position data from passive and active yaw head im pulses with fixation at 0 degrees, 20 degrees up and 20 degrees down, obtai ned from a previous experiment. The optimal pulley coefficient required to fit the data was determined by calculating the mean square error between da ta and model predictions of torsional eye velocity. For active head impulse s, the optimal pulley coefficient varied considerably between subjects. The median optimal pulley coefficient was found to be 0.5, the pulley coeffici ent required for producing saccades that perfectly obey Listing's law when using a two-dimensional saccadic pulse signal. The model predicted the dire ction of the axis tilts observed in response to passive head impulses from 50 ms after onset. During passive head impulses, the median optimal pulley coefficient was found to be 0.21, when roll gain was fixed at 0.7. The mode l did not accurately predict the alignment of the eye and head velocity axe s that was observed early in the response to passive head impulses. We foun d that this alignment could be well predicted if the roll gain of the angul ar vestibuloocular reflex was modified during the initial period of the res ponse, while pulley coefficient was maintained at 0.5. Hence a roll gain mo dification allows stabilization of the retinal image without requiring a ch ange in the pulley effect. Our results therefore indicate that the eye posi tion-dependent velocity axis tilts could arise due to the effects of the pu lleys and that a roll gain modification in the central vestibular structure s may be responsible for countering the pulley effect.