High Frequency Burst Firing of Granule Cells Ensures Transmission at the Parallel Fiber to Purkinje Cell Synapse at the Cost of Temporal Coding

By Boeke J. van Beugen, Zhenyu Gao, Henk-Jan Boele, Freek E. Hoebeek, C. D. De Zeeuw. 2013

78 citations recorded by the source corpus.

Cerebellar granule cells (GrCs) convey information from mossy fibers (MFs) to Purkinje cells (PCs) via their parallel fibers (PFs). MF to GrC signaling allows transmission of frequencies up to 1 kHz and GrCs themselves can also fire bursts of action potentials with instantaneous frequencies up to 1 kHz. So far, in the scientific literature no evidence has been shown that these high-frequency bursts also exist in awake, behaving animals. More so, it remains to be shown whether such high-frequency bursts can transmit temporally coded information from MFs to PCs and/or whether these patterns of activity contribute to the spatiotemporal filtering properties of the GrC layer. Here, we show that, upon sensory stimulation in both un-anesthetized rabbits and mice, GrCs can show bursts that consist of tens of spikes at instantaneous frequencies over 800 Hz. In vitro recordings from individual GrC-PC pairs following high-frequency stimulation revealed an overall low initial release probability of ~0.17. Nevertheless, high-frequency burst activity induced a short-lived facilitation to ensure signaling within the first few spikes, which was rapidly followed by a reduction in transmitter release. The facilitation rate among individual GrC-PC pairs was heterogeneously distributed and could be classified as either “reluctant” or “responsive” according to their release characteristics. Despite the variety of efficacy at individual connections, grouped activity in GrCs resulted in a linear relationship between PC response and PF burst duration at frequencies up to 300 Hz allowing rate coding to persist at the network level. Together, these findings support the hypothesis that the cerebellar granular layer acts as a spatiotemporal filter between MF input and PC output (D’Angelo and De Zeeuw, 2009).

Subfields: Cellular and Molecular Neuroscience, Neurology, Sensory Systems

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Citations in the corpus

Network Structure within the Cerebellar Input Layer Enables Lossless Sparse Encoding (2014, background): “This is approximately one billion, if we assume that events are integrated in 30 ms windows (Figure S4B; Schwartz et al., 2012; van Beugen et al., 2013) for a lifetime of 1 year.”
Synaptic representation of locomotion in single cerebellar granule cells (2015, background): “The high firing rates of granule cells during locomotion was organized in bursts, reminiscent of the high-frequency bursts observed in granule cells with some forms of sensory stimulation (van Beugen et al., 2013), which in turn can be transmitted reliably to the Purkinje cell (Valera et al., 2012).”