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

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Abstract
Synaptic boutons, the points of communication between nerve cells, are so tiny that it has been impossible to record their electrical activity without slicing the brain. In a technical tour de force, Rancz et al. provide the first intracellular recordings from presynaptic boutons in the intact mammalian brain. Their results contradict the prevailing views — derived from in vitro work — on how the cerebellum integrates sensory information to control movement, by revealing an unexpected sensitivity of single brain connections to stimuli from the environment. The first intracellular recordings from presynaptic boutons in the intact mammalian brain are presented. These results contradict the prevailing views (derived from in vitro work) on how the cerebellum integrates sensory information to control movement, by revealing a hitherto unexpected sensitivity of single brain connections to stimuli from the environment. 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 cortex1,2—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 cells3 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.