Abstract
A recent controversy has emerged concerning the existence of long pauses, presumably reflecting bistability of membrane potential, in the cerebellar Purkinje cells (PC) of awake animals. It is generally agreed that in the anesthetized animals and in vitro, these cells switch between two stable membrane potential states: a depolarized state (the ‘up-state’) characterized by continuous firing of simple spikes (SS) and a hyperpolarized state (the ‘down-state’) characterized by long pauses in the SS activity. To address the existence of long pauses in the neural activity of cerebellar PCs in the awake and behaving animal we used extracellular recordings in cats and find that approximately half of the recorded PCs exhibit such long pauses in the SS activity and transition between activity – periods with uninterrupted SS lasting an average of 1300 ms – and pauses up to several seconds. We called these cells pausing Purkinje cells (PPC) and they can easily be distinguished from continuous firing Purkinje cells. In most PPCs, state transitions in both directions were often associated (25% of state transitions) with complex spikes (CSs). This is consistent with intracellular findings of CS-driven state transitions. In sum, we present proof for the existence of long pauses in the PC SS activity that probably reflect underlying bistability, provide the first in-depth analysis of these pauses and show for the first time that transitions in and out of these pauses are related to CS firing in the awake and behaving animal.
Highlights
Cerebellar Purkinje cells (PC) are one of the most physically striking and enigmatic neurons in the central nervous system
Long pauses in SS activity were evident in half of the cells we recorded in non-anesthetized cats
The two PC categories were well separated on coefficient of variation, bi-exponential fit to the ISI histogram, and bimodality of the instantaneous firing rate (IFR) suggesting that the categories are not artifacts of any particular data analysis
Summary
Cerebellar Purkinje cells (PC) are one of the most physically striking and enigmatic neurons in the central nervous system. The field is in need of convincing proof of the existence of such pauses and a thorough analysis of their characteristics in the awake animal is required in order to settle the controversy and provide the basis for serious modeling Another prominent issue in the current controversy revolves around the relationship of long pauses in SS activity to that of the second PC neural signature, the CS. In intracellular and extracellular recordings from anesthetized animals and in in vitro experiments, the CS can trigger a transition either from the pausing state of the PCs to its active state or vice versa (Loewenstein et al, 2005; Schonewille et al, 2006) This striking link between the two spiking signatures of the cerebellar PCs has never been observed to occur in the awake and behaving animals and is both surprising and difficult to explain with current cerebellar models
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