Recovery from unilateral labyrinthectomy in rhesus monkey

M. Fetter, D. S. Zee

Research output: Contribution to journalArticlepeer-review


1. We recorded eye movements in six rhesus monkeys before and after unilateral labyrinthectomy and quantified the compensation for both the static and the dynamic disturbances of the vestibuloocular reflex (VOR). 2. When first recorded after labyrinthectomy (18-20 h postlesion), all animals had a spontaneous nystagmus with mean slow-phase velocities ranging from 24 to 54°/s measured in darkness and 0-4°/s measured in the light. The level of nystagmus diminished quickly, and by postoperative day 25 mean values ranged from 4 to 22°/s, measured in darkness. The waveform of individual slow phases was variable, but in the first postoperative week its trajectory usually showed an increasing, or an increasing then decreasing, velocity. This finding indicates that peripheral vestibular lesions can alter the function of the ocular motor eye-position integrator. 3. The VOR gain (eye velocity/head velocity, corrected for spontaneous nystagmus) during rotations (30-300°/s) in the dark was diminished from nearly 1.0 preoperatively to ~0.5 when first measured after labyrinthectomy, except for rotations toward the lesioned side at high speeds for which the gain was even lower. Within the first few postoperative days, for rotations toward the intact side, the VOR gain increased rapidly, to ~0.8. For rotations toward the lesioned side similar behavior was noted for stimuli of 30-60°/s, but at higher velocities compensation proceeded more slowly. By 3 mo postoperatively gains had reached values ranging from 0.77 to 1.03 for rotations toward the intact side and from 0.61 to 0.98 for rotations toward the lesioned side. Values were higher for lower-velocity stimuli. 4. Caloric testing with ice water in the unoperated ear elicited nystagmus with a mean value of maximum slow-phase velocity of 129°/s preoperatively and 195°/s 3 mo postoperatively. There was no caloric response on the lesioned side. From the increase in caloric responses from the intact ear we infer considerable restoration of spontaneous activity of vestibular neurons on the deafferented side. 5. The time constant of the VOR was a function of stimulus speed preoperatively with a maximum mean value of 35 s for a 60°/s stimulus. After labyrinthectomy the VOR time constant was low (6.0-9.1 s) at all speeds. Subsequently, in three animals only, there was a small increase (2-3 s) in VOR time constant during the 3-mo period following labyrinthectomy. These results indicate that labyrinthectomy profoundly and persistently impairs the action of the vestibular velocity-storage mechanism. 6. The velocity-storage component of the optokinetic system, as reflected in optokinetic afternystagmus (OKAN), was also markedly impaired by labyrinthectomy. OKAN was nearly absent (initial velocity of OKAN was 4-13% of preop values) for drum rotations directed toward the intact side and markedly diminished for drug rotations toward the lesioned side (30-43% of preop values). The time constant of the discharge of OKAN was decreased to 4-6 s (preop >45 s) for both directions. By 3 mo postlesion the initial velocity of OKAN had increased for both directions but only to ~50-60% of preop values, and the time constant of OKAN had slightly increased, to 7-9 s. These enduring changes in OKAN following labyrinthectomy probably reflect alterations in the tonic levels of activity in central vestibular/optokinetic velocity-storage mechanism. 7. To interpret the changes in vestibular responses after labyrinthectomy we used a hypothetical model of bilateral central vestibular connections, including an inhibitory vestibular commissure. We could easily simulate the reduction of spontaneous nystagmus and the changes in VOR gain that occurred following labyrinthectomy without resorting to changes in the gains of vestibular commissure pathways. We assumed an extralabyrinthine source of vestibular tone, to eliminate spontaneous nystagmus, and an increase in the sensitivity of central vestibular neurons to afferent inputs, to restore VOR gain. We could also simulate the changes in gain of the VOR by altering commissural gains, but restoration of static VOR balance still required readjustment of extralabyrinthine sources of tone. We suggest that changes in commissural gains either play no role at all, or at most only help to make fine ajdustments, in the restoration of static vestibular balance.

Original languageEnglish (US)
Pages (from-to)370-393
Number of pages24
JournalJournal of neurophysiology
Issue number2
StatePublished - 1988

ASJC Scopus subject areas

  • Neuroscience(all)
  • Physiology


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