Organization of olivocerebellar activity in the absence of excitatory glutamatergic input

The olivocerebellar system has been proposed to function as a timing device for motor coordination in which inferior olivary neurons act as coupled oscillators that spontaneously generate rhythmic and synchronous activity. However, the inferior olive receives excitatory afferents, which can also drive the activity of these neurons. The extent to which the olivocerebellar system can intrinsically generate synchronous activity and olivary neurons act as neuronal oscillators has not been determined. To investigate this issue, multiple electrode recordings of complex spike (CS) activity were obtained from 236 crus 2a Purkinje cells in anesthetized rats. Intraolivary injections of the glutamate antagonists 6-cyano-7-nitroquinoxaline-2,3-dione or 1,2,3,4-tetrahydro-6-nitro-2,3-dioxo-benzo[f]quinoxaline-7-sulfonamide disodium were made, and the resulting changes in CS activity were determined. Loss of evoked CS responses to motor cortex stimulation or perioral tactile stimulation was used to measure the efficacy of the block. Block of glutamatergic input decreased the average CS firing rate by approximately 50% but did not abolish spontaneous CS activity. The remaining CS activity was significantly more rhythmic than that in control. The patterns of synchrony were similar to those found in control conditions (i.e., synchronous CSs primarily occurred among Purkinje cells located within the same approximately 250-microm-wide rostrocaudally oriented cortical strip); however, this normal banding pattern was enhanced. These changes in CS activity were not observed with vehicle injections. The results suggest that excitatory afferent activity disrupts olivary oscillations and support the hypotheses that olivary neurons are capable of acting as neuronal oscillators and that synchronous CS activity results from electrotonic coupling of olivary neurons.