Inferior olive oscillations gate transmission of motor cortical activity to the cerebellum

Inferior olivary (IO) neurons display spontaneous oscillatory activity, yet the importance of these oscillations for shaping the responses of this system to its afferents is uncertain. We used multiple electrode recording of crus 2a Purkinje cell complex spikes (CSs) in ketamine-xylazine-anesthetized rats to investigate olivocerebellar responses to activation of motor cortico-olivary pathways. Trains of electrical stimuli were applied to the motor cortex at frequencies between 4 and 30 Hz. Various frequency-response curves were observed, with the most common types being unimodal with a maximum at 9.5 +/- 2.3 Hz and bimodal with peaks at 8.9 +/- 1.0 and 15.1 +/- 1.3 Hz. To determine whether IO oscillatory properties underlie the resonance peaks in the frequency-response curves, apamin and charybdotoxin were injected into the IO. These toxins, which weaken and enhance spontaneous IO oscillations, respectively, had corresponding effects on the sharpness of resonance peaks. Next, the variation of CS entrainment patterns with frequency was investigated to characterize the nature of the IO oscillator. Low-frequency (4 Hz) stimulation was relatively ineffective in entraining CS activity. Between 4 and 30 Hz, two predominant entrainment patterns emerged. For low-frequency (4-6 Hz) and high-frequency (17-30 Hz) ranges, a 1:2 entrainment dominated, whereas in the intermediate range (6-17 Hz), 1:1 entrainment was most prevalent. These results indicate that IO neurons respond as nonlinear oscillators to afferent signals.