The Contribution of Single Synapses to Sensory Representation in Vivo

Abstract

The extent to which synaptic activity can signal a sensory stimulus limits the information available to a neuron. We determined the contribution of individual synapses to sensory representation by recording excitatory postsynaptic currents (EPSCs) in cerebellar granule cells during a time-varying, quantifiable vestibular stimulus. Vestibular-sensitive synapses faithfully reported direction and velocity, rather than position or acceleration of whole-body motion, via bidirectional modulation of EPSC frequency. The lack of short-term synaptic dynamics ensured a highly linear relationship between velocity and charge transfer, and as few as 100 synapses provided resolution approaching psychophysical limits. This indicates that highly accurate stimulus representation can be achieved by small networks and even within single neurons.

Sensory transmission in cerebellar granule cells relies on similarly coded mossy fiber inputs

“…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). It is conceivable that the mossy fiber convergence patterns differ between different functional areas of the cerebellum; for example, the whisker system may function differently from other somatosensory systems, in that they may have the sole function of event detection, not proprioception.…”

“…Granule cells have been found to be relatively simple spike encoders; that is, they feature a relatively linear and uncomplicated conversion of depolarization level to spike rate (7,15). Thus, it is a logical consequence that the spike output of the granule cells also can be expected to ref lect this coding principle, at least during low-intensity, rate-coded mossy fiber activation, which appears to be the prevailing form of activation under this behavior (16,17). But during high-intensity mossy fiber bursts, the translation of mossy fiber input to a depolarization level in the granule cell possibly may not be entirely linear; for example, both cuneate and LRN mossy fibers can fire at up to 1,000 Hz during skin stimulation (2,18), a frequency at which the depression of the synaptic transmission to granule cells is profound (7).…”

“…In contrast, in the system studied here, it was shown previously that a single mossy fiber will not activate the granule cell spike, not even when activated at 1000 Hz, but spike activation depends on the synchronous activation of 3 or 4 mossy fibers (7). Arenz et al (17) reported that granule cells with rotation-activated EPSC-inputs had very small EPSCs that were not modulated during rotation, even though all of the medium-to-large EPSCs were clearly modulated. They concluded that the nonmodulated EPSCs may represent nonvestibular information (17).…”

Variable timing of synaptic transmission in cerebellar unipolar brush cells

“…Moreover, during regular trains of presynaptic stimulation, EPSC peaks displayed significant depression within the first five stimuli that already became almost complete at a stimulation frequency of 20 Hz. This result stands in stark contrast to mossy fiber-granule cell EPSCs, for which short-term depression is virtually absent at comparable rates (15,21). Furthermore, the relatively large capacitance of the UBC membrane reduces the capacity for fast EPSC components to depolarize UBCs, as currents are effectively low-pass filtered while charging the cell.…”

“…Vestibular mossy fibers in vivo typically display background discharge rates of 5-10 Hz in anesthetized mice in the flocculus (15) or as averaged during a vestibular tilt stimulus in the uvula-nodulus (16). We therefore investigated the development of EPSC amplitudes during trains of presynaptic stimulation.…”