Spatiotemporal network coding of physiological mossy fiber inputs by the cerebellar granular layer

PLoS Comput Biol. 2017 Sep 21;13(9):e1005754. doi: 10.1371/journal.pcbi.1005754. eCollection 2017 Sep.

Abstract

The granular layer, which mainly consists of granule and Golgi cells, is the first stage of the cerebellar cortex and processes spatiotemporal information transmitted by mossy fiber inputs with a wide variety of firing patterns. To study its dynamics at multiple time scales in response to inputs approximating real spatiotemporal patterns, we constructed a large-scale 3D network model of the granular layer. Patterned mossy fiber activity induces rhythmic Golgi cell activity that is synchronized by shared parallel fiber input and by gap junctions. This leads to long distance synchrony of Golgi cells along the transverse axis, powerfully regulating granule cell firing by imposing inhibition during a specific time window. The essential network mechanisms, including tunable Golgi cell oscillations, on-beam inhibition and NMDA receptors causing first winner keeps winning of granule cells, illustrate how fundamental properties of the granule layer operate in tandem to produce (1) well timed and spatially bound output, (2) a wide dynamic range of granule cell firing and (3) transient and coherent gating oscillations. These results substantially enrich our understanding of granule cell layer processing, which seems to promote spatial group selection of granule cell activity as a function of timing of mossy fiber input.

MeSH terms

  • Action Potentials / physiology
  • Biological Clocks / physiology*
  • Cerebellar Cortex / physiology*
  • Computer Simulation
  • Humans
  • Models, Neurological*
  • Nerve Fibers / physiology*
  • Nerve Net / physiology*
  • Spatio-Temporal Analysis*
  • Synaptic Transmission / physiology

Grant support

This work was supported by funding from the Okinawa Institute of Science and Technology Graduate University. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. SH was supported by Japan Society for the Promotion of Science, KAKENHI Grant Number 15K06715 (https://www.jsps.go.jp/english/e-grants/).