Effects of reversible shutdown of the monkey flocculus on the retention of adaptation of the horizontal vestibulo-ocular reflex

Abstract

There are two different proposals regarding the role of the cerebellar flocculus in the adaptation of the vestibulo-ocular reflex: that the flocculus is the site for both the induction and retention of the adaptation, or that the flocculus plays an important role in the induction, but the vestibular nuclei to which the flocculus issues its efferences are the site of retention. To locate the memory trace for the adaptation of the vestibulo-ocular reflex, we determined effects of acute pharmacological shutdown of the bilateral cerebellar flocculi in four Macaca fuscata. The gain of the horizontal vestibulo-ocular reflex was measured by sinusoidal oscillation of the turntable by 10° (peak-to-peak) at 0.33 Hz in the dark. Two hours of 0.33 Hz–10° sinusoidal oscillation of the turntable while viewing the stationary checked-pattern screen through a ×2.2 magnifying lens adaptively increased the horizontal vestibulo-ocular reflex gain by 0.2 on the average. The gain increase lasted for 1 h when the monkeys were left with their heads fixed in darkness, but it disappeared within 24 h after the monkeys were returned to their cages where they had free movements. The effects of injections of 5 or 10% lidocaine chloride into the bilateral floccular areas (8 μl for each side) immediately after adaptation occurred were determined in nine sessions. The gain of the horizontal vestibulo-ocular reflex immediately decreased to the level before the adaptation. These effects of lidocaine lasted for at least 1 h. On the contrary, injections of the same amount of Ringer’s solution, tested in eight sessions, hardly affected gain of the horizontal vestibulo-ocular reflex over 1-h period. These depressant effects of lidocaine injections were specific to the gains increased by adaptation. These results suggest that the memory trace for the short-term adaptation of the horizontal vestibulo-ocular reflex gain induced by 2 h of sustained visual-vestibular interactions resides within the flocculus.