Abstract

Synaptic currents display a large degree of heterogeneity of their temporal characteristics, but the functional role of such heterogeneities remains unknown. We investigated in rat cerebellar slices synaptic currents in Unipolar Brush Cells (UBCs), which generate intrinsic mossy fibers relaying vestibular inputs to the cerebellar cortex. We show that UBCs respond to sinusoidal modulations of their sensory input with heterogeneous amplitudes and phase shifts. Experiments and modeling indicate that this variability results both from the kinetics of synaptic glutamate transients and from the diversity of postsynaptic receptors. While phase inversion is produced by an mGluR2-activated outward conductance in OFF-UBCs, the phase delay of ON UBCs is caused by a late rebound current resulting from AMPAR recovery from desensitization. Granular layer network modeling indicates that phase dispersion of UBC responses generates diverse phase coding in the granule cell population, allowing climbing-fiber-driven Purkinje cell learning at arbitrary phases of the vestibular input.

Highlights

  • Sensory stimuli are encoded by populations of neurons with a diversity of spatio-temporal selectivity properties, which allow sensory systems to obtain accurate representations of such stimuli over the whole range of ecological spatial and temporal time scales

  • We investigated the functional consequences of this Granule Cells (GCs) phase shift variability on downstream Purkinje cells (PCs)

  • We have shown that Unipolar Brush Cells (UBCs) encode these inputs with a surprising degree of heterogeneity, their responses spanning all the possible range of phase shifts, at all the frequencies tested here

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Summary

Introduction

Sensory stimuli are encoded by populations of neurons with a diversity of spatio-temporal selectivity properties, which allow sensory systems to obtain accurate representations of such stimuli over the whole range of ecological spatial and temporal time scales. Primary vestibular neurons primarily encode the rotational velocity (semicircular canals) and linear acceleration (gravitational or inertial, in the otholitic organs) of the head (Arenz et al, 2008; Fernandez and Goldberg, 1971; Goldberg, 2000; Goldberg and Fernandez, 1971a, 1971b; Green and Angelaki, 2010; Sadeghi et al, 2007). These vestibular inputs are in turn used to adapt body posture, generate compensatory and orienting eye movements, and modify vasomotor autonomic functions. A similar idea was proposed for suppression of the self-

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