Increased responsiveness of Purkinje cells associated with climbing fiber inputs to neighboring neurons

Abstract

Experiments were performed in unanesthetized decerebrate cats to determine if the responsiveness of Purkinje cells in the cerebellar cortex is related to the occurrence of a climbing fiber input to neighboring neurons. The responses to a mechanical tap applied to the dorsum of the ipsilateral forepaw were recorded simultaneously from up to three Purkinje cells in the surface folia of lobule V. In the initial paradigm, the response of a Purkinje cell to the forepaw stimulus was conditioned by spontaneous climbing fiber inputs to neighboring neurons. As a control, a poststimulus time histogram (PSTH) was constructed from each Purkinje cell''s simple spike response to the forepaw stimulus applied randomly relative to the occurrence of complex spikes in the neighboring cell. A second histogram was constructed from responses to stimuli applied at fixed intervals after the occurrence of spontaneous climbing fiber inputs to a neighboring cell. By determining the ratio of the cell''s responses in the control and conditioned histograms it was demonstrated that the simple spike response was accentuated when the peripheral stimulus was applied at short intervals (20-50 ms) following the complex spikes in the other neurons of the set. Using a different paradigm, the relationship was determined between a Purkinje cell''s responsiveness to forepaw stimuli and the climbing fiber inputs evoked by the same stimuli in a neighboring neuron. The simple spike responses were separated into two groups based on the presence or absence of an evoked climbing fiber input to the neighboring neuron. Separate histograms were constructed from these two groups of trials, and the ratios of the simple spike response amplitudes in these 2 histograms were quantitatively determined. It was found that climbing fiber inputs evoked in a Purkinje cell by a forepaw stimulus can be associated with an increased simple spike responsiveness in neighboring neurons. The modification in a Purkinje cell''s responsiveness associated with either spontaneous or evoked climbing fiber inputs to neighboring cells could be characterized as an accentuation of the existing components of the simple spike response. Usually the same response component in a cell was enhanced when associated with climbing fiber inputs of different neurons. In addition, the climbing fiber input to one neuron could be associated with an enhanced excitatory response in one cell and an enhanced inhibitory response in another. The generalized cross correlation between climbing fiber inputs to the Purkinje cells of a set was calculated. Positive correlation in the evoked climbing fiber activity was related to the increased simple spike responsiveness. An increased gain in a Purkinje cell''s response to a peripheral stimulus can be associated with either evoked or spontaneous climbing fiber inputs to a neighboring neuron. Since the increased responsiveness occurred when the climbing fiber inputs to the Purkinje cells in the set were highly correlated, the synchronous activation of climbing fiber inputs appears to be an important aspect of the observed change in responsiveness. Evidently peripheral stimuli synchronously activate climbing fiber inputs to a group of Purkinje cells, resulting in an increase in their gain to the associated mossy fiber input.