Eye movement deficits following ibotenic acid lesions of the nucleus prepositus hypoglossi in monkeys II. Pursuit, vestibular, and optokinetic responses

The eyes are moved by a combination of neural commands that code eye veloci ty and eye position. The eye position signal is supposed to be derived from velocity-coded command signals by mathematical integration via a single oc ulomotor neural integrator. For horizontal eye movements, the neural integr ator is thought to reside in the rostral nucleus prepositus hypoglossi (nph ) and project directly to the abducens nuclei. In a previous study, permane nt, serial ibotenic acid lesions of the nph in three rhesus macaques compro mised the neural integrator for fixation but saccades were not affected. In the present study, to determine further whether the nph is the neural subs trate for a single oculomotor neural integrator, the effects of those lesio ns on smooth pursuit, the vestibule-ocular reflex (VOR), vestibular nystagm us (VN), and optokinetic nystagmus (OKN) are documented. The lesions were c orrelated with long-lasting deficits in eye movements, indicated most clear ly by the animals' inability to maintain steady gaze in the dark. However, smooth pursuit and sinusoidal VOR in the dark, like the saccades in the pre vious study, were affected minimally. The gain of horizontal smooth pursuit (eye movement/target movement) decreased slightly (<25%) and phase lead in creased slightly for all frequencies (0.3-1.0 Hz, +/-10 degrees target trac king), most noticeably for higher frequencies (0.8-0.7 and similar to 20 de grees for 1.0-Hz tracking). Vertical smooth pursuit was not affected signif icantly. Surprisingly, horizontal sinusoidal VOR gain and phase also were n ot affected significantly. Lesions had Complex effects on both VN and OKN. The plateau of per- and postrotatory VN was shortened substantially (simila r to 50%), whereas the initial response and the time constant of decay decr eased slightly. The initial OKN response also decreased slightly, and the c harging phase was prolonged transiently then recovered to below normal leve ls like the VN time constant. Maximum steady-state, slow eye velocity of OK N decreased progressively by similar to 30% over the course of the lesions. These results support the previous conclusion that the oculomotor neural i ntegrator is not a single neural entity and that the mathematical integrati ve function for different oculomotor subsystems is most likely distributed among a number of nuclei. They also show that the nph apparently is not inv olved in integrating smooth pursuit signals and that lesions of the nph can fractionate the VOR and nystagmic responses to adequate stimuli.