Precise Temperature Compensation of Phase in a Rhythmic Motor Pattern

Lamont S Tang,Jonathan S Caplan,Mehmet Fisek,Eve Marder,Marie L Goeritz,Adam L Taylor,William A Harris

doi:10.1371/journal.pbio.1000469

Abstract

Author SummaryThe neural circuits that produce behaviors such as walking, chewing, and swimming must be both robust and flexible to changing internal and environmental demands. How then do cold-blooded animals cope with temperature fluctuations when the underlying processes that give rise to circuit performance are themselves temperature-dependent? We exploit the crab stomatogastric ganglion to understand the extent to which circuit features are robust to temperature perturbations. We subjected these circuits to temperature ranges they normally encounter in the wild. Interestingly, while the frequency of activity in the network increased 4-fold over these temperature ranges, the relative timing between neurons in the network—termed phase relationships—remained constant. To understand how temperature compensation of phase might occur, we characterized the temperature dependence (Q10's) of synapses and membrane currents. We used computational models to show that the experimentally measured Q10's can promote phase maintenance. We also showed that many model bursting neurons fail to burst over the entire temperature range and that phase maintenance is promoted by closely restricting the model neurons' Q10's. These results imply that although ion channel numbers can vary between individuals, there may be strong evolutionary pressure that restricts the temperature dependence of the processes that contribute to temperature compensation of neuronal circuits.

Highlights

The nervous systems of cold-blooded animals must function across significant ranges of temperature despite the fact that the signal transduction pathways and synaptic and intrinsic membrane currents are all temperature-dependent
We show that temperature drastically alters the frequency of the pyloric rhythm, its phase relationships are remarkably temperature invariant
The top trace shows a burst of the Pyloric Dilator (PD) neurons, the second trace shows the activity of the Lateral Pyloric (LP) neuron, and the bottom trace shows the activity of the PY neurons

Summary

Introduction

The nervous systems of cold-blooded animals must function across significant ranges of temperature despite the fact that the signal transduction pathways and synaptic and intrinsic membrane currents are all temperature-dependent. This is intriguing because one would not expect all cellular processes to have the same temperature dependence, and it is hard to imagine that functional circuit integrity would necessarily be maintained when temperature is altered. All biological processes have characteristic Q10’s that describe the changes in their rates as a function of temperature. How different can the various Q10’s that govern the intrinsic and synaptic conductances within a circuit be and still allow appropriate function to be maintained despite environmental temperature change? How different can the various Q10’s that govern the intrinsic and synaptic conductances within a circuit be and still allow appropriate function to be maintained despite environmental temperature change? Which attributes of circuit performance are temperature dependent and which, if any, are temperature compensated?

Methods

Results

Conclusion