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

Abstract

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.

Altered Neuron Excitability and Synaptic Plasticity in the Cerebellar Granular Layer of Juvenile Prion Protein Knock-Out Mice with Impaired Motor Control

“…Slow EPSPs and action potentials are expected to reduce the velocity and temporal precision of mossy fiber-granule cell synaptic transmission (D'Angelo et al, 1995(D'Angelo et al, , 1997Cathala et al, 2003), the absence of repetitive firing to prevent coding of afferent information into spike bursts (Chadderton et al, 2004;Jörntell and Ekerot, 2006;Nieus et al, 2006;Rancz et al, 2007), and the absence of LTP to limit granular layer changes by specific input patterns (Mapelli and D'Angelo, 2007). This could bring about a diffused impairment of synaptic transmission and plasticity throughout the cerebellar network (Casado et al, 2002;Brunel et al, 2004).…”

Tonic Activation of GABAB Receptors Reduces Release Probability at Inhibitory Connections in the Cerebellar Glomerulus

“…The single quantum conductance (214 pS) is relatively large compared with the resting whole cell conductance (ϳ1,000 pS; Arenz et al 2008;Armano et al 2000;D'Angelo et al 1995;Rancz et al 2007), so that even a single quantum can determine a remarkable inhibitory effect contrasting the depolarization caused by excitatory synapses. The proposed synaptic arrangement and release statistics are similar to those of the neighboring mossy fiber-granule cell synapse (Saviane and Silver 2006a,b;Sola et al 2004), indicating that the glomerular system can provide an appropriate excitatory/inhibitory balance to the granule cells.…”

“…Golgi cells usually respond to punctuate stimulation with short high-frequency spike bursts (Rancz et al 2007;Solinas et al 2007a,b;Vos et al 1999). To imitate native Golgi cell patterns, we tested the effect of five-impulse 100-Hz stimulus trains (Fig.…”

Intermediate conductance calcium-activated potassium channels modulate summation of parallel fiber input in cerebellar Purkinje cells

“…Bias current was applied to sustain a tonic firing frequency of ∼50 Hz (49.7 ± 1.8 Hz, n = 9) before and after drug application. Parallel fiber inputs were stimulated at 100 Hz (five pulses) to mimic frequencies of input relevant to sensory stimulation (1,35). After application of TRAM-34, there was an increase in both peak baseline voltage (59 ± 25.6%, n = 5, Recordings and plots of baseline voltage during 25 Hz parallel fiber stimulus trains in a coronal slice in the absence of picrotoxin to preserve feed-forward inhibition.…”