Eye position signals in the flocculus of the monkey during smooth‐pursuit eye movements

1. Discharges of Purkinje cells and mossy fibres were recorded from the flocculus of monkeys trained to fixate a small visual target and to track the target when it moved slowly. 2. Discharges of Purkinje cells changed tonically with shifts of gaze. Firing rates were linearly related to eye positions for either the entire or more than half the eye‐position range in 12·6% of Purkinje cells tested (76/603 units). 3. The eye position‐related activity (position component) was observable in these cells also during smooth‐pursuit eye movements. It was typically seen during slow eye movements (velocities less than 10 deg/s) but became undetectable during high velocity movements (faster than 50 deg/s). 4. The position component became prominent when smooth pursuit was executed at the preferred loci of the individual cells. In the majority of the cells tested at their preferred loci, the position component was observable to a relatively high frequency, such as 0·5 Hz (± 10 deg; peak velocity 31 deg/s). 5. Forty‐five mossy fibre units showed saccade‐related bursts and position‐related intersaccadic tonic activity during steady eye position. In each unit, the position component was found only during fixations within a specific range of eye positions. During fixations outside these regions, all position‐related mossy fibres were completely silent. 6. During sinusoidal smooth‐pursuit eye movements, the mossy fibres also displayed cyclic modulations in activity. All fibres discharged with eye movements in one direction and were silent during eye movements in the other direction. 7. Saccade‐related bursts from mossy fibres led the onset of saccades, ranging from 0 to 19 ms with a mean lead‐time of 6·9 ms. This observation negates the possibility that the position‐related signals might represent proprioceptive impulses from the stretch receptors of the extraocular muscle.