Duration of Purkinje cell complex spikes increases with their firing frequency

Abstract

Climbing fiber (CF) triggered complex spikes (CS) are massive depolarization bursts in the cerebellar Purkinje cell (PC), showing several high frequency spikelet components (±600 Hz). Since its early observations, the CS is known to vary in shape. In this study we describe CS waveforms, extracellularly recorded in awake primates (Macaca mulatta) performing saccades. Every PC analyzed showed a range of CS shapes with profoundly different duration and number of spikelets. The initial part of the CS was rather constant but the later part differed greatly, with a pronounced jitter of the last spikelets causing a large variation in total CS duration. Waveforms did not effect the following pause duration in the simple spike (SS) train, nor were SS firing rates predictive of the waveform shapes or vice versa. The waveforms did not differ between experimental conditions nor was there a preferred sequential order of CS shapes throughout the recordings. Instead, part of their variability, the timing jitter of the CS’s last spikelets, strongly correlated with interval length to the preceding CS: shorter CS intervals resulted in later appearance of the last spikelets in the CS burst, and vice versa. A similar phenomenon was observed in rat PCs recorded in vitro upon repeated extracellular stimulation of CFs at different frequencies in slice experiments. All together these results strongly suggest that the variability in the timing of the last spikelet is due to CS frequency dependent changes in PC excitability.

The dynamic relationship between cerebellar Purkinje cell simple spikes and the spikelet number of complex spikes

“…Our findings are in agreement with Gilbert (1976) who found a positive correlation between spikelet number and background simple spike rates in a small population of Purkinje cells located in the anterior lobe of awake monkeys. By contrast, Mano (1970) found no correlation between simple spike rate and spikelet number in Purkinje cells recorded from the oculomotor vermis in awake primates (see also Warnaar et al 2015). This difference is probably not related to species or the effects of anaesthesia because similar findings were found in our small sample of cells from the awake cat.…”

“…By contrast, Mano () found no correlation between simple spike rate and spikelet number in Purkinje cells recorded from the oculomotor vermis in awake primates (see also Warnaar et al . ). This difference is probably not related to species or the effects of anaesthesia because similar findings were found in our small sample of cells from the awake cat.…”

“…() found no such relationship, whereas other studies have found that complex spikes preceded by a complex spike occurring closer in time have both greater spikelet numbers (Campbell & Hesslow, ) and duration (Warnaar et al . ). However, the opposite relationship has also been reported (Hashimoto & Kano, ; Maruta et al .…”

“…One possible reason for the discrepancy with the findings of Mano () and Warnaar et al . () may be differences in the recording site location, particularly given the emerging evidence that Purkinje cells in zebrin‐positive and zebrin‐negative bands show different firing properties (Paukert et al . ; Lang et al .…”

“…Whether or not a relationship exists between the number of spikelets in a complex spike and the simple spike activity of the same Purkinje cell is unclear (Mano, 1970;Gilbert, 1976). Gilbert (1976) reported a positive relationship between background simple spike firing rate and spikelet number, whereas Mano (1970) and Warnaar et al (2015) found no relationship between complex spike waveform and the preceding simple spike firing rates. With regard to behaviour, a recent study in monkeys has shown that learning-related reductions in simple spike activity correlate with the duration of complex spikes during motor learning (Yang & Lisberger, 2014).…”