Flocculectomy and unit activity in the vestibular nuclei during visual-vestibular interactions

Activity of neurons in the vestibular nuclei of alert monkeys was recorded extracellularly after total unilateral and bilateral flocculectomy and partial paraflocculectomy. Type 1 horizontal cells that were encountered after flocculectomy responded to visual and vestibular stimuli and to conflict stimulation, i.e., to rotation in a subject-stationary visual surround, as do vestibular neurons in the normal animal. The major difference between neurons in the normal and lesioned animals was that more time was needed to reach steady state firing levels during optokinetic stimulation at a constant velocity after operation. As shown previously (Waespe et al. 1983) the longer time course is related to increased initial retinal slip velocities that occur after flocculectomy as a result of an inability to change eye velocity rapidly in response to visual stimulation. It does not signify a change in the dynamics of neurons in the vestibular nuclei that mediate the vestibulo-ocular reflex (VOR). The similarity in modulation of horizontal Type 1 vestibular neurons in normal and flocculectomized monkeys makes it unlikely that floccular Purkinje cells suppress the horizontal VOR in the monkey during conflicting visual and vestibular stimuli by inhibiting or disfacilitating secondary or tertiary vestibular neurons. This is consistent with earlier findings that indicate that visual-oculomotor pathways responsible for ocular pursuit or for rapid changes in OKN do not go through the vestibular nuclei. Rather the point of interaction of the flocculus output with the VOR appears to be external to the vestibular nuclei. There was a close correspondence between the slow phase velocity of nystagmus and unit activity in the vestibular nuclei under a wide variety of test conditions after flocculectomy. This is consistent with the postulate that frequencies of vestibular nuclei neurons represent a summation of activity in direct vestibulo-oculomotor pathways and indirect pathways that include the velocity storage mechanism. These are the major remaining sources of activity that generate slow phases of nystagmus after the direct visual-oculomotor pathways have been partially interrupted by flocculectomy (Waespe et al. 1983). Horizontal Type 1 neurons which responded to vestibular and optokinetic stimulation with increases in frequency above 1 spike/s/degree/s were rarely encountered after flocculectomy. These cells were present on the normal side in a monkey after unilateral flocculectomy. We infer that vestibular nuclei neurons that project mossy fibers to the flocculus are inactivated or disappear as a result of surgical ablation of their axons. This could also contribute to the reduced gain of vestibular nystagmus, OKAN and off-vertical nystagmus that was observed in some of the animals after lesion.