Long time-constant behavior of the oculomotor plant in barbiturate-anesthetized primate

The mechanics of the extraocular muscles and orbital tissue ("oculomotor plant") can be approximated by a small number of viscoelastic (Voigt) elements in series. Recent analysis of the eye's return from displacement in lightly anesthetized rhesus monkeys has suggested a four-element plant model with time constants (TCs) of approximately 0.01, 0.1, 1, and 10 s. To demonstrate directly the presence of long (1,10 s) TC elements and to assess their contribution quantitatively, horizontal eye displacement was induced in Cynomolgus monkeys under deep barbiturate anesthesia that prevented interference from spontaneous eye movements. The displacement was maintained for either a prolonged (30 s) or brief (0.2 s) period before release. Return to resting position took 20-30 s after prolonged displacement but only 1-2 s after brief displacement, consistent with the presence of long TC elements that would only be substantially stretched in the former condition. Quantitative fitting of the release curves after prolonged displacement indicated that the two long TC elements contribute a substantial proportion (approximately 30%) of the total plant compliance. A model based on the estimated compliance values is shown to account quantitatively both for our release data and for Goldstein and Robinson's data on hysteresis of ocular motoneuron firing rates measured after centripetal saccades following prolonged eccentric fixation. Long time-constant elements in the plant thus make a substantial contribution to some types of eye movement, and their inclusion in plant models can help interpret the firing patterns of single units in the oculomotor system.