High-fidelity transmission of sensory information by single cerebellar mossy fibre boutons

By E. Rancz, T. Ishikawa, Ian Duguid, Paul Chadderton, Séverine Mahon, Michael Häusser. 2007

297 citations recorded by the source corpus.

Understanding the transmission of sensory information at individual synaptic connections requires knowledge of the properties of presynaptic terminals and their patterns of firing evoked by sensory stimuli. Such information has been difficult to obtain because of the small size and inaccessibility of nerve terminals in the central nervous system. Here we show, by making direct patch-clamp recordings in vivo from cerebellar mossy fibre boutons—the primary source of synaptic input to the cerebellar cortex—that sensory stimulation can produce bursts of spikes in single boutons at very high instantaneous firing frequencies (more than 700 Hz). We show that the mossy fibre–granule cell synapse exhibits high-fidelity transmission at these frequencies, indicating that the rapid burst of excitatory postsynaptic currents underlying the sensory-evoked response of granule cells can be driven by such a presynaptic spike burst. We also demonstrate that a single mossy fibre can trigger action potential bursts in granule cells in vitro when driven with in vivo firing patterns. These findings suggest that the relay from mossy fibre to granule cell can act in a ‘detonator’ fashion, such that a single presynaptic afferent may be sufficient to transmit the sensory message. This endows the cerebellar mossy fibre system with remarkable sensitivity and high fidelity in the transmission of sensory information.

Subfields: Cognitive Neuroscience, Neurology, Sensory Systems

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Citations in the corpus

Re-evaluating circuit mechanisms underlying pattern separation (2019, neutral): “…present in cerebellar granule cells (Brickley et al., 1996) ensures a high spike threshold (Hamann et al., 2002) that typically requires activation of three of the four mossy fibre inputs (D’Angelo et al., 1995; Jörntell and Ekerot, 2006; Rothman et al., 2009; but see Rancz et al., 2007).”
Synaptic Integration in Cerebellar Granule Cells (2008, background): “Recently, a paper was published claiming that a granule cell can be activated by a single afferent mossy fiber [7].”
Multimodal integration in granule cells as a basis for associative plasticity and sensory prediction in a cerebellum-like circuit. (2010, background): “This observation is consistent with findings in the rat cerebellum that high-frequency activation of a single MF input is sufficient to evoke GC firing (Rancz et al., 2007).”
Synaptic and cellular properties of the feed-forward inhibitory circuit within the input layer of the cerebellar cortex (2008, background): “In contrast, experiments in decerebrate and anesthetized animals show that tactile stimulation of whiskers and forelimbs evokes a barrage of EPSCs at hundreds of hertz in GrCs arising from one or multiple MFs, which exhibit low firing rates at rest (Jörntell and Ekerot, 2006; Rancz et al., 2007).”
Control of cerebellar granule cell output by sensory-evoked Golgi cell inhibition (2015, methodology): “In vivo patch-clamp recordings were made from granule cells in Crus II of the cerebellar cortex of 18- to 24-d-old Sprague–Dawley rats anesthetized with a ketamine/xylazine mixture as described (23, 25).”
elife.elifesciences.org RESEARCH ARTICLE Convergence of pontine and (2013, unknown): “Granule cells can generate action potentials in response to a single mossy fiber input (Rancz et al., 2007).”
Are mushroom bodies cerebellum-like structures? (2011, background): “…cerebellum, the glomerular synapse is thought to promote spillover of neurotransmitter throughout the glomerulus, thereby enhancing transmission efficacy (DiGregorio et al., 2002; Rancz et al., 2007); the basically identical structure of the insect microglomerulus suggests a similar role.”
Sensory transmission in cerebellar granule cells relies on similarly coded mossy fiber inputs (2009, background): “Our findings regarding granule cell function differ from the conclusions drawn from granule cell recordings in whiskerrelated areas of the rat (9) and in a vestibular-related system of the mouse (17).”
NMDA receptors with incomplete Mg2+ block enable low-frequency transmission through the cerebellar cortex (2012, background): “The high-frequency bursting phase is not essential for GC layer throughput Sensory stimuli encoded by brief high-frequency MF bursts have been shown to be efficiently transmitted by GCs (Chadderton et al., 2004; Rancz et al., 2007; Barmack and Yakhnitsa, 2008; Rothman et al., 2009; Sawtell, 2010) du”
Synaptic representation of locomotion in single cerebellar granule cells (2015, methodology): “In vivo whole-cell voltage-clamp and current-clamp recordings were obtained from cerebellar granule cells and mossy fiber boutons as previously described (Chadderton et al., 2004; Rancz et al., 2007; Duguid et al., 2012).”
Multimodal sensory integration in single cerebellar granule cells in vivo (2015, background): “Electrophysiological recordings have shown that somatosensory inputs to crus I and II (Chadderton et al., 2004; Rancz et al., 2007) and vestibular signals to the flocculus (Arenz et al.”