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The Journal of Neuroscience, September 3, 2008, 28(36):8955-8967; doi:10.1523/JNEUROSCI.5469-07.2008

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Cellular/Molecular
Synaptic and Cellular Properties of the Feedforward Inhibitory Circuit within the Input Layer of the Cerebellar Cortex

Roby T. Kanichay and R. Angus Silver

Department of Neuroscience, Physiology, and Pharmacology, University College London, London WC1E 6BT, United Kingdom

Correspondence should be addressed to Prof. R. Angus Silver, Department of Neuroscience, Physiology, and Pharmacology, University College London, Gower Street, London WC1E 6BT, UK. Email: a.silver{at}ucl.ac.uk

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°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 µs). 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 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.

Key words: cerebellum; synaptic integration; Golgi cell; mossy fiber; inhibition; interneuron

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Received Dec. 11, 2007; revised July 18, 2008; accepted July 21, 2008.

Correspondence should be addressed to Prof. R. Angus Silver, Department of Neuroscience, Physiology, and Pharmacology, University College London, Gower Street, London WC1E 6BT, UK. Email: a.silver{at}ucl.ac.uk

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