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Synaptic and cellular properties of the feedforward inhibitory circuit within the input layer of the cerebellar cortex.

ABSTRACT: Precise representation of the timing of sensory stimuli is essential for rapid motor coordination, a core function of the cerebellum. Feedforward inhibition has been implicated in precise temporal signaling in several regions of the brain, but little is known about this type of inhibitory circuit within the input layer of the cerebellar cortex. We investigated the synaptic properties of feedforward inhibition at near physiological temperatures (35 degrees C) in rat cerebellar slices. We establish that the previously uncharacterized mossy fiber-Golgi cell-granule cell pathway can act as a functional feedforward inhibitory circuit. The synchronous activation of four mossy fibers, releasing a total of six quanta onto a Golgi cell, can reset spontaneous Golgi cell firing with high temporal precision (200 mus). However, only modest increases in Golgi cell firing rate were observed during trains of high-frequency mossy fiber stimulation. This decoupling of Golgi cell activity from mossy fiber firing rate was attributable to a strong afterhyperpolarization after each action potential, preventing mossy fiber-Golgi cell signaling for approximately 50 ms. Feedforward excitation of Golgi cells induced a temporally precise inhibitory conductance in granule cells that curtailed the excitatory action of the mossy fiber EPSC. The synaptic and cellular properties of this feedforward circuit appear tuned to trigger a fast inhibitory conductance in granule cells at the onset of stimuli that produce intense bursts of activity in multiple mossy fibers, thereby conserving the temporal precision of the initial granule cell response.

SUBMITTER: Kanichay RT

PROVIDER: S-EPMC2923072 | biostudies-literature | 2008 Sep

REPOSITORIES: biostudies-literature

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Synaptic and cellular properties of the feedforward inhibitory circuit within the input layer of the cerebellar cortex.

Kanichay Roby T RT Silver R Angus RA

The Journal of neuroscience : the official journal of the Society for Neuroscience 20080901 36

Precise representation of the timing of sensory stimuli is essential for rapid motor coordination, a core function of the cerebellum. Feedforward inhibition has been implicated in precise temporal signaling in several regions of the brain, but little is known about this type of inhibitory circuit within the input layer of the cerebellar cortex. We investigated the synaptic properties of feedforward inhibition at near physiological temperatures (35 degrees C) in rat cerebellar slices. We establis ...[more]

PMID: 18768689

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Project description:Layer 1 of the neocortex is sparsely populated with neurons and heavily innervated by fibers from lower layers and proximal and distal brain regions. Understanding the potential functions of this layer requires a comprehensive understanding of its cellular and synaptic organization. We therefore performed a quantitative study of the microcircuitry of neocortical layer 1 (L1) in the somatosensory cortex in juvenile rats (P13-P16) using multi-neuron patch-clamp and 3D morphology reconstructions. Expert-based subjective classification of the morphologies of the recorded L1 neurons suggest 6 morphological classes: (1) the Neurogliaform cells with dense axonal arborizations (NGC-DA) and with sparse arborizations (NGC-SA), (2) the Horizontal Axon Cell (HAC), (3) those with descending axonal collaterals (DAC), (4) the large axon cell (LAC), and (5) the small axon cell (SAC). Objective, supervised and unsupervised cluster analyses confirmed DAC, HAC, LAC and NGC as distinct morphological classes. The neurons were also classified into 5 electrophysiological types based on the Petilla convention; classical non-adapting (cNAC), burst non-adapting (bNAC), classical adapting (cAC), classical stuttering (cSTUT), and classical irregular spiking (cIR). The most common electrophysiological type of neuron was the cNAC type (40%) and the most common morpho-electrical type was the NGC-DA-cNAC. Paired patch-clamp recordings revealed that the neurons were connected via GABAergic inhibitory synaptic connections with a 7.9% connection probability and via gap junctions with a 5.2% connection probability. Most synaptic connections were mediated by both GABAA and GABAB receptors (62.6%). A smaller fraction of synaptic connections were mediated exclusively by GABAA (15.4%) or GABAB (21.8%) receptors. Morphological 3D reconstruction of synaptic connected pairs of L1 neurons revealed multi-synapse connections with an average of 9 putative synapses per connection. These putative synapses were widely distributed with 39% on somata and 61% on dendrites. We also discuss the functional implications of this L1 cellular and synaptic organization in neocortical information processing.

Dataset Information

Synaptic and cellular properties of the feedforward inhibitory circuit within the input layer of the cerebellar cortex.

Publications

Synaptic and cellular properties of the feedforward inhibitory circuit within the input layer of the cerebellar cortex.

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