Role of the flocculus and paraflocculus in optokinetic nystagmus and visual-vestibular interactions: Effects of lesions

Summary

• 1. Optokinetic nystagmus (OKN), optokinetic after-nystagmus (OKAN), vestibular nystagmus and visual-vestibular interactions were studied in monkeys after surgical ablation of the flocculus and paraflocculus. After bilateral flocculectomy the initial rapid rise in slow phase eye velocity of horizontal and vertical OKN was severely attenuated, and maximum velocities fell to the preoperative saturation level of OKAN. There is generally little or no upward OKAN in the normal monkey, and upward OKN was lost after bilateral lesions. Unilateral flocculectomy affected the rapid rise in horizontal velocity to both sides.

• 2. Consistent with the absence of a rapid response to steps of surround velocity, animals were unable to follow acceleration of the visual field with eye accelerations faster than about 3–57 °/s².

• 3. The slow rise in OKN slow phase velocity to a steady state level was prolonged after operation. However, rates of rise were approximately equal for the same initial retinal slips before and after operation. The similarity in the time course of OKN when adjusted for initial retinal slip, and in the gain, saturation level and time course of OKAN before and after flocculectomy indicates that the lesions had not significantly altered the coupling of the visual system to the velocity storage integrator or its associated time constant.

• 4. When animals were rotated in a subjectstationary visual surround after flocculectomy, they could not suppress the initial jump in eye velocity at the onset of the step. Despite this, they could readily suppress the subsequent nystagmus. The time constant of decline in the conflict situations was almost as short as in the normal monkey and was in the range of the peripheral vestibular time constant. This suggests that although the animals were unable to suppress rapid changes in eye velocity due to activation of direct vestibulo-oculomotor pathways, they had retained their ability to discharge activity from the velocity storage mechanism. Consistent with this, animals had no difficulty in suppressing OKAN after flocculectomy.

• 5. Visual-vestibular interactions utilizing the velocity storage mechanism were normal after flocculectomy, as was nystagmus induced by rotation about a vertical axis or about axes tilted from the vertical. Also unaffected were the discharge of nystagmus caused by tilting the head out of the plane of the response and visual suppression of nystagmus induced by off-vertical axis rotation. The flocculus does not appear to play an important role in mediating these responses.

• 6. The data before and after flocculectomy were simulated by a model which is homeomorphic to that presented previously. The model has direct pathways from the vestibular and visual systems. The visual and vestibular systems couple to a common velocity storage integrator. There is also a dump mechanism which shortens the time constant of the integrator when eye velocity exceeds surround velocity. An important element in the model is a nonlinearity that couples the visual system to the integrator. Approximate closed form relationships were established between the parameters of the nonlinearity and the dynamics of OKN and OKAN. The nonlinear element is assumed to receive a central representation of retinal slip as its input. Its output drives the velocity storage integrator. The model predicts the normal responses, and by removal of the direct pathway it simulates the data after flocculectomy. The nonlinearity explains why the storage integrator charges more slowly for larger initial retinal slips both in the normal animal and after flocculectomy. The model also predicts that surround velocity would be followed better during deceleration than acceleration. This is a result of activation of the dump mechanism which shortens the time constant of the velocity storage integrator, effectively discharging it. Activation of the dump mechanism is independent of the flocculus.

• 7. Although the flocculus is closely linked to the vestibular system, its function in the monkey appears closely related to production of rapid changes in eye velocity from the visual system, either during slow phases of nystagmus or during ocular pursuit (Zee et al. 1981). It does not appear to cancel the horizontal VOR at the level of the vestibular nuclei, nor does it directly affect the dynamics of vestibular nystagmus, OKAN or the velocity storage mechanism.