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Decoding Purkinje cell simple spike trains: Patterns and pauses

Erik De Schutter

Theoretical Neurobiology, University of Antwerp, Belgium

The cerebellum is crucial for the precise temporal control of motor related tasks and conditioned behaviors. Yet, it is not clear how the cerebellum may signal precise timing at the cellular level. Prior studies of spike time coding in the cerebellum have focused on the discharge of Purkinje cells, but only considered mean firing rates of simple or complex spikes. Little attention has been paid to the temporal structure of the spike trains, even though spike timing may encode additional information in other systems. I will report on our experimental studies of the temporal structure of simple spike trains in Purkinje cells and present some ideas on how this may affect the target neurons in deep cerebellar nuclei (DCN).

Cerebellar Purkinje cells in vivo are commonly reported to spike in irregular fashion, documented by high coefficients of variation of interspike-intervals (ISI). In strong contrast, they fire very regularly in the in vitro slice preparation. We studied the nature of this difference in firing properties. We discovered the presence of highly precise regular spike patterns, lasting up to hundreds of milliseconds, in PC simple spike trains recorded in both anesthetized and awake rodents. Regular spike patterns, defined by low variability of successive ISIs, comprised over half the spikes, showed a wide range of mean ISIs, and were affected by behavioural state and tactile stimulation.

Onset of regular patterns was often synchronized in nearby Purkinje cells, but individual spikes in the patterns were not. Conversely, spikes surrounding pauses in the simple spike firing were often tightly synchronized. Such synchronized pauses may be important in evoking post-inhibitory rebound spikes, a powerful timing signal, in DCN neurons.

In model simulations we found that the regular patterns caused epochs of relatively constant synaptic conductance in DCN neurons. We propose that the function of regular patterns is to control the magnitude of ensuing post-inhibitory rebound spikes.