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Cell-intrinsic mechanisms of temperature compensation in a grasshopper sensory receptor neuron.

Roemschied FA, Eberhard MJ, Schleimer JH, Ronacher B, Schreiber S - Elife (2014)

Bottom Line: The nervous systems of poikilothermic animals must have evolved mechanisms enabling them to retain their functionality under varying temperatures.Auditory receptor neurons of grasshoppers respond to sound in a surprisingly temperature-compensated manner: firing rates depend moderately on temperature, with average Q10 values around 1.5.Remarkably, this type of temperature compensation need not come at an additional metabolic cost of spike generation.

View Article: PubMed Central - PubMed

Affiliation: Institute of Theoretical Biology, Department of Biology, Humboldt-Universität zu Berlin, Berlin, Germany Bernstein Center for Computational Neuroscience Berlin, Berlin, Germany.

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Alternative measures of metabolic cost and energy efficiency of spiking.(A) Schematic illustration of the measures used (sodium-current-based and potassium-current-based cost, as well as energy efficiency estimated by the separability of sodium and potassium currents either in relation to the sodium current or the potassium current). (B) Impact of the model parameters'  values for all four measures. In all cases, temperature dependence of sodium inactivation,  had the largest impact on metabolic cost or energy efficiency. In contrast, the temperature dependence of delayed-rectifier potassium activation,  (which proved most influential for the temperature dependence of firing rate) exerted a smaller impact on both potassium- and sodium-based energy consumption. (C) The distribution of energy measures across all spike generation models as well as models with particularly high and low RMSD (subgroup of models within the bottom and top 25 percentile of RMSDs).DOI:http://dx.doi.org/10.7554/eLife.02078.010
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fig3s1: Alternative measures of metabolic cost and energy efficiency of spiking.(A) Schematic illustration of the measures used (sodium-current-based and potassium-current-based cost, as well as energy efficiency estimated by the separability of sodium and potassium currents either in relation to the sodium current or the potassium current). (B) Impact of the model parameters' values for all four measures. In all cases, temperature dependence of sodium inactivation, had the largest impact on metabolic cost or energy efficiency. In contrast, the temperature dependence of delayed-rectifier potassium activation, (which proved most influential for the temperature dependence of firing rate) exerted a smaller impact on both potassium- and sodium-based energy consumption. (C) The distribution of energy measures across all spike generation models as well as models with particularly high and low RMSD (subgroup of models within the bottom and top 25 percentile of RMSDs).DOI:http://dx.doi.org/10.7554/eLife.02078.010

Mentions: The impacts of conductance parameters on f-I curve temperature dependence and energy consumption were not significantly correlated in this case (ρ = −0.23, p=0.56). In particular, the key parameters of largest influence on these features belonged to different channel groups: potassium channels in case of temperature compensation and sodium channels in case of energy efficiency of spike generation. We verified that the large influence of sodium channels was not biased by our sodium-current-based definition of metabolic cost. Three alternative measures—two quantifying energy efficiency based on the separability of sodium and potassium currents (Alle et al., 2009), the other defined by the total potassium current—all confirmed the temperature dependence of sodium channel inactivation as the most influential parameter for spiking cost (Figure 3—figure supplement 1).


Cell-intrinsic mechanisms of temperature compensation in a grasshopper sensory receptor neuron.

Roemschied FA, Eberhard MJ, Schleimer JH, Ronacher B, Schreiber S - Elife (2014)

Alternative measures of metabolic cost and energy efficiency of spiking.(A) Schematic illustration of the measures used (sodium-current-based and potassium-current-based cost, as well as energy efficiency estimated by the separability of sodium and potassium currents either in relation to the sodium current or the potassium current). (B) Impact of the model parameters'  values for all four measures. In all cases, temperature dependence of sodium inactivation,  had the largest impact on metabolic cost or energy efficiency. In contrast, the temperature dependence of delayed-rectifier potassium activation,  (which proved most influential for the temperature dependence of firing rate) exerted a smaller impact on both potassium- and sodium-based energy consumption. (C) The distribution of energy measures across all spike generation models as well as models with particularly high and low RMSD (subgroup of models within the bottom and top 25 percentile of RMSDs).DOI:http://dx.doi.org/10.7554/eLife.02078.010
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4012639&req=5

fig3s1: Alternative measures of metabolic cost and energy efficiency of spiking.(A) Schematic illustration of the measures used (sodium-current-based and potassium-current-based cost, as well as energy efficiency estimated by the separability of sodium and potassium currents either in relation to the sodium current or the potassium current). (B) Impact of the model parameters' values for all four measures. In all cases, temperature dependence of sodium inactivation, had the largest impact on metabolic cost or energy efficiency. In contrast, the temperature dependence of delayed-rectifier potassium activation, (which proved most influential for the temperature dependence of firing rate) exerted a smaller impact on both potassium- and sodium-based energy consumption. (C) The distribution of energy measures across all spike generation models as well as models with particularly high and low RMSD (subgroup of models within the bottom and top 25 percentile of RMSDs).DOI:http://dx.doi.org/10.7554/eLife.02078.010
Mentions: The impacts of conductance parameters on f-I curve temperature dependence and energy consumption were not significantly correlated in this case (ρ = −0.23, p=0.56). In particular, the key parameters of largest influence on these features belonged to different channel groups: potassium channels in case of temperature compensation and sodium channels in case of energy efficiency of spike generation. We verified that the large influence of sodium channels was not biased by our sodium-current-based definition of metabolic cost. Three alternative measures—two quantifying energy efficiency based on the separability of sodium and potassium currents (Alle et al., 2009), the other defined by the total potassium current—all confirmed the temperature dependence of sodium channel inactivation as the most influential parameter for spiking cost (Figure 3—figure supplement 1).

Bottom Line: The nervous systems of poikilothermic animals must have evolved mechanisms enabling them to retain their functionality under varying temperatures.Auditory receptor neurons of grasshoppers respond to sound in a surprisingly temperature-compensated manner: firing rates depend moderately on temperature, with average Q10 values around 1.5.Remarkably, this type of temperature compensation need not come at an additional metabolic cost of spike generation.

View Article: PubMed Central - PubMed

Affiliation: Institute of Theoretical Biology, Department of Biology, Humboldt-Universität zu Berlin, Berlin, Germany Bernstein Center for Computational Neuroscience Berlin, Berlin, Germany.

Show MeSH
Related in: MedlinePlus