Abstract
Previous studies have shown that neurons within the vestibular nuclei (VN) can faithfully encode the time course of sensory input through changes in firing rate in vivo. However, studies performed in vitro have shown that these same VN neurons often display nonlinear synchronization (i.e. phase locking) in their spiking activity to the local maxima of sensory input, thereby severely limiting their capacity for faithful encoding of said input through changes in firing rate. We investigated this apparent discrepancy by studying the effects of in vivo conditions on VN neuron activity in vitro using a simple, physiologically based, model of cellular dynamics. We found that membrane potential oscillations were evoked both in response to step and zap current injection for a wide range of channel conductance values. These oscillations gave rise to a resonance in the spiking activity that causes synchronization to sinusoidal current injection at frequencies below 25 Hz. We hypothesized that the apparent discrepancy between VN response dynamics measured in in vitro conditions (i.e., consistent with our modeling results) and the dynamics measured in vivo conditions could be explained by an increase in trial-to-trial variability under in vivo vs. in vitro conditions. Accordingly, we mimicked more physiologically realistic conditions in our model by introducing a noise current to match the levels of resting discharge variability seen in vivo as quantified by the coefficient of variation (CV). While low noise intensities corresponding to CV values in the range 0.04–0.24 only eliminated synchronization for low (<8 Hz) frequency stimulation but not high (>12 Hz) frequency stimulation, higher noise intensities corresponding to CV values in the range 0.5–0.7 almost completely eliminated synchronization for all frequencies. Our results thus predict that, under natural (i.e. in vivo) conditions, the vestibular system uses increased variability to promote fidelity of encoding by single neurons. This prediction can be tested experimentally in vitro.
Highlights
The vestibular system provides information about head motion relative to space that is necessary for maintaining posture, computing spatial orientation, and perceiving self-motion
The activities of single vestibular neurons recorded in the brains of awake behaving animals show that they can accurately transmit information about the time course of head motion, which is necessary for several behaviors such as the vestibulo-ocular reflex required for gaze stabilization
We investigated the cause for this discrepancy by studying how a mathematical model of vestibular neuron activity responds to mimics of sensory stimulation under different conditions
Summary
The vestibular system provides information about head motion relative to space that is necessary for maintaining posture, computing spatial orientation, and perceiving self-motion. Peripheral vestibular afferents encode the detailed time course of either horizontal rotations, vertical rotations, or linear acceleration through changes in their firing rates and spike timing [1,2,3,4]. Type B neurons display a resonance at frequencies within the behaviorally relevant range that increases the tendency of small amplitude, high-frequency synaptic inputs to trigger non-linear firing behavior in the form of synchronization to the peaks of the input [12,13] This synchronization severely limits the range of input frequencies and amplitudes for which the activity of type B neurons accurately follows the input [13,14,15]. Type A neurons, despite displaying a resonance, tend to follow the time course of current injection accurately for a much wider range of stimulus amplitudes [12,13]
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