CEREBELLAR INFLUENCE ON OLIVARY EXCITABILITY IN THE CAT

This study examines the influence of the cerebellum on the excitabilit y of inferior olivary neurons in the cat. Two major pathways from the cerebellar nuclei to the inferior olive have been investigated by elec trophysiological and anatomical techniques, The first, excitatory path way connects the cerebellar nuclei through nuclei at the mesodiencepha lic junction with the inferior olive. The second is the direct, GABAer gic, nucleo-olivary pathway. Intra- as well as extracellular recording s obtained in the rostral part of the medial accessory and principal o lives revealed that electrical stimulation with a short burst of three pulses delivered at the mesodiencephalic junction results in short-la tency activation (4-8 ms) of most olivary neurons. More than half of t he units showed, in addition to the short-latency activation, a consis tent response with a much longer latency (similar to 180 ms). Many uni ts (66%) that responded to mesodiencephalic stimulation could also be activated by superior cerebellar peduncle stimulation with a similar s timulation paradigm (latency 9-15 ms). However, in such cases consiste nt long-latency responses were only rarely recorded (7%). To distingui sh between the effect of the two pathways, both of which are activated by superior cerebellar peduncle stimulation, an electrolytic lesion o f the nucleo-olivary fibres was made in the brainstem in six experimen ts. The effect of this lesion was verified in three cases by retrograd e horseradish peroxidase tracing from the rostral inferior olive at th e end of the experiment. This time only extracellular recordings were made. Stimulation of the mesodiencephalic junction still resulted in e asily activated olivary units which showed an increased probability of firing a long-latency action potential. Stimulation of the superior c erebellar peduncle now resulted in a 50% decrease in probability of ac tivating olivary units in the short-latency range. However, a five-fol d increase in the chance of triggering action potentials in the long-l atency interval was noted, implying that many units reacted only with a long-latency action potential. The results obtained with our experim ental paradigm appear enigmatic since it is well established that the nucleo-olivary pathway is GABAergic and thus, by convention, should be inhibitory to the olivary neurons. However, it is possible to explain these results in terms of dynamic coupling of olivary neurons. This c oncept ascribes an important role to the nucleo-olivary pathway in reg ulating the degree of electrotonic coupling between olivary neurons (p robably by a shunting mechanism) and as such may be an important instr ument in the regulation of synchronous and rhythmic olivary discharges . Thus, lesion of this pathway would be expected to result in coupling of large aggregates of olivary cells. It seems likely that these stro ngly coupled cell ensembles are more difficult to activate by incoming afferent volleys. However, once activated, the coupled olivary neuron s develop an oscillation of the membrane potential which may be convey ed, electrotonically, to neighbouring neurons and subsequently, during the depolarizing phase of the oscillation, result in a more easily tr iggered rebound or long-latency response. It is concluded that cerebel lar output may not merely inhibit olivary neurons, but also, in conjun ction with an excitatory nucleo-mesodiencephalo-olivary circuit, modul ate olivary excitability in a rather complex manner.