The activity of Purkinje cells (P-cells) in the flocculus of 8 lightly anesthetized cats and one alert cat was recorded for periods of up to several hours each. The resting simple spike (SS) rate in the anesthetized cats was 37 +/- 21 Hz (mean +/- standard deviation), similar to that observed in the alert cat. Complex spikes (CSs) were evoked by an electrode placed in the climbing fiber (CF) decussation or inferior olive (IO). For each P-cell, SS activity was suppressed completely at or above a cut-off frequency of evoked CSs; median cut-off rate was 5 Hz (range 1-10 Hz, 15 cells). Reversible lesions of the CF pathway were made by microinjection of 1-10 microliter of saturated lidocaine into the IO or CF decussation. This abolished spontaneous CS activity and produced two reversible effects on SS discharge: (1) an increase in mean SS rate of 98%, from 23 +/- 13 to 40 +/- 18 Hz (11 cells); and (2) a decrease of 50% in the variability of SS firing rate. Similar effects were observed in two P-cells whose CF axons were lesioned mechanically. These results show that electrical stimulation and reversible lesions in areas previously shown to alter the gain of the vestibulo-ocular reflex (VOR) also alter CF input to the flocculus, suggesting that the gain changes were caused by changes in CS rate. This study confirms and extends the observation that a reciprocal relationship exists between CS rate and SS background rate, and therefore further suggests that the changes in the gain of the VOR might be due to changes in SS background rate.