Limits...
In vivo conditions induce faithful encoding of stimuli by reducing nonlinear synchronization in vestibular sensory neurons.

Schneider AD, Cullen KE, Chacron MJ - PLoS Comput. Biol. (2011)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Physics, McGill University, Montreal, Quebec, Canada.

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.

Show MeSH
Effects of the bias current and noise intensity on resting discharge rate and variability, and resonance strength and frequency.The effects of the bias current  and noise intensity  on the resting discharge rate and variability as quantified by the coefficient of variation (CV) were explored. A) Resting discharge rate as a function of  and . B) CV as a function of  and . Parameter values were the same as those previously described. C) Oscillation index from zap stimuli as a function of  and noise intensity . D) Oscillation frequency as a function of  and noise intensity .
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC3140969&req=5

pcbi-1002120-g007: Effects of the bias current and noise intensity on resting discharge rate and variability, and resonance strength and frequency.The effects of the bias current and noise intensity on the resting discharge rate and variability as quantified by the coefficient of variation (CV) were explored. A) Resting discharge rate as a function of and . B) CV as a function of and . Parameter values were the same as those previously described. C) Oscillation index from zap stimuli as a function of and noise intensity . D) Oscillation frequency as a function of and noise intensity .

Mentions: Our simulation results are largely contrary to recordings from VN neurons performed in vivo. Indeed, many VN neurons accurately follow the time course of vestibular stimuli through changes in firing rate and do not display synchronization or phase locking for frequencies between 0 and 25 Hz [16]. As our modeling results described above were obtained for high values of and were robust to increases in the bias current , it is unlikely that the discrepancy between our model results and experimental recordings from VN neurons in vivo is due to a change in membrane conductance or the fact that VN neurons might be in a depolarized state in vivo. Thus, while our results show that increasing the bias current such that the firing rate increases to values seen in vivo did increase the range of frequencies for which our model could faithfully encode the time course of sinusoidal input, this alone was not sufficient to eliminate nonlinear synchronization for the full range of frequencies found in natural vestibular stimuli (Figures 6D,6E,7A).


In vivo conditions induce faithful encoding of stimuli by reducing nonlinear synchronization in vestibular sensory neurons.

Schneider AD, Cullen KE, Chacron MJ - PLoS Comput. Biol. (2011)

Effects of the bias current and noise intensity on resting discharge rate and variability, and resonance strength and frequency.The effects of the bias current  and noise intensity  on the resting discharge rate and variability as quantified by the coefficient of variation (CV) were explored. A) Resting discharge rate as a function of  and . B) CV as a function of  and . Parameter values were the same as those previously described. C) Oscillation index from zap stimuli as a function of  and noise intensity . D) Oscillation frequency as a function of  and noise intensity .
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3140969&req=5

pcbi-1002120-g007: Effects of the bias current and noise intensity on resting discharge rate and variability, and resonance strength and frequency.The effects of the bias current and noise intensity on the resting discharge rate and variability as quantified by the coefficient of variation (CV) were explored. A) Resting discharge rate as a function of and . B) CV as a function of and . Parameter values were the same as those previously described. C) Oscillation index from zap stimuli as a function of and noise intensity . D) Oscillation frequency as a function of and noise intensity .
Mentions: Our simulation results are largely contrary to recordings from VN neurons performed in vivo. Indeed, many VN neurons accurately follow the time course of vestibular stimuli through changes in firing rate and do not display synchronization or phase locking for frequencies between 0 and 25 Hz [16]. As our modeling results described above were obtained for high values of and were robust to increases in the bias current , it is unlikely that the discrepancy between our model results and experimental recordings from VN neurons in vivo is due to a change in membrane conductance or the fact that VN neurons might be in a depolarized state in vivo. Thus, while our results show that increasing the bias current such that the firing rate increases to values seen in vivo did increase the range of frequencies for which our model could faithfully encode the time course of sinusoidal input, this alone was not sufficient to eliminate nonlinear synchronization for the full range of frequencies found in natural vestibular stimuli (Figures 6D,6E,7A).

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Physics, McGill University, Montreal, Quebec, Canada.

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.

Show MeSH