1. Intracellular recordings were obtained from cerebellar nuclear neurones in the isolated brain stem-cerebellar preparation of guinea-pigs in vitro. The electrical properties of the cells were quite similar to those reported in in vitro slice studies. They had an average resting potential of -56.7 +/- 1.8 mV, an input resistance of 23.8 +/- 4.9 M omega, and a time constant of 12.5 +/- 2.7 ms. The action potentials had an average amplitude of 57.3 +/- 5.28 mV (n = 20). 2. In addition to the ionic mechanisms required for the generation of the fast action potential, cerebellar nuclear neurones displayed a low-threshold Ca2+-dependent spike which produced a powerful rebound excitation following anodal break. This type of electroresponsiveness was absent in the slice preparation. 3. The anodal break response was further enhanced by the presence of a non-inactivating Na+ conductance similar to that described in Purkinje cells. 4. Following electrical stimulation of the cerebellar cortex or the underlying white matter, excitatory and inhibitory synaptic potentials (EPSP-IPSP sequences) could be recorded in cerebellar nuclear neurones. The EPSPs were elicited by direct activation of collaterals of mossy or climbing fibre afferents. The IPSPs followed direct or orthodromic Purkinje cell activation. 5. The integrity of the olivo-cerebellar system was tested by the administration of harmaline which produced powerful EPSP-IPSP sequences or pure IPSPs in cerebellar nuclear neurones. These IPSPs were often followed by a rebound firing of the cells. 6. These results indicate that the olivo-cerebellar pathway, in addition to its activation of the cerebellar cortex, exerts a powerful and complex set of synaptic events on cerebellar nuclear cells. As such it is a true afferent system, having a distinct role in cerebellar physiology.