Ontogenesis of olivocerebellar relationships. II. Spontaneous activity of inferior olivary neurons and climbing fibermediated activity of cerebellar Purkinje cells in developing rats.

During development of vertebrate cerebellum, a multiple innervation of each Purkinje cell (PC) by several climbing fibers (CFs) (Crépel, F., J. Mariani, and N. Delhaye-Bouchaud (1976) J. Neurobiol. 7: 567-578; Mariani, J., and J. -P. Changeux (1981) J. Neurosci. 1: 696-702) precedes the one-to-one relationship characteristic of the adult stage. In the present study, the spontaneous activity of inferior olivary neurons (whose axons constitute the CFs) and the spontaneous activity elicited in PCs by the CF system were investigated in developing rats. Extracellular unitary recordings were obtained in medial and dorsal accessory olives from 249 neurons from 1-day-old to adult animals. The mean discharge rate varied from 0.19 spike . sec-1 on day 1 to 1.69 spikes . sec-1 on postnatal day 21 and 1.78 spikes . sec-1 in adult animals. Although the spontaneous discharge was low, interspike interval histograms were constructed for a sample of cells. Their modal value varied from a mean value of 660 msec on day 1 to 250 msec in the adult with, however, marked variations at each age in the young animals. Intracellular recordings from PCs were performed in rats ranging in age from 5 to 15 postnatal days. The spontaneous (i.e., asynchronous) discharge of excitatory postsynaptic potentials mediated neurons at the same age. The main results are the following: (1) In PCs innervated by one CF, the mean frequency of CF-EPSPs was similar to the discharge of inferior olivary neurons; (2) in PCs innervated by several CFs, the mean discharge of CF-EPSPs was much higher than the discharge of inferior olivary neurons; (3) as a whole, the CF-mediated activity of PCs decreased from day 5 to day 11, while the multiple innervation disappeared; from then on, the activity increased with the maturation of inferior olivary neurons until adult values. The ratio of the frequencies of CF-EPSPs and olivary neurons discharges gives an approximate mean number of CF collaterals per PC at each age; it varied from 3.6 on day 5 to values close to 1 on day 11 and the following days.