Abstract
Computational modeling and experimentation in a model system for network dynamics reveal how network phase relationships are temperature-compensated in terms of their underlying synaptic and intrinsic membrane currents.
Most animal species are cold-blooded, and their neuronal circuits must maintain function despite environmental temperature fluctuations. The central pattern generating circuits that produce rhythmic motor patterns depend on the orderly activation of circuit neurons. We describe the effects of temperature on the pyloric rhythm of the stomatogastric ganglion of the crab,
Cancer borealis
. The pyloric rhythm is a triphasic motor pattern in which the Pyloric Dilator (PD), Lateral Pyloric (LP), and Pyloric (PY) neurons fire in a repeating sequence. While the frequency of the pyloric rhythm increased about 4-fold (Q
10
∼2.3) as the temperature was shifted from 7°C to 23°C, the phase relationships of the PD, LP, and PY neurons showed almost perfect temperature compensation. The Q
10
's of the input conductance, synaptic currents, transient outward current (I
A
), and the hyperpolarization-activated inward current (I
h
), all of which help determine the phase of LP neuron activity, ranged from 1.8 to 4. We studied the effects of temperature in >1,000 computational models (with different sets of maximal conductances) of a bursting neuron and the LP neuron. Many bursting models failed to monotonically increase in frequency as temperature increased. Temperature compensation of LP neuron phase was facilitated when model neurons' currents had Q
10
's close to 2. Together, these data indicate that although diverse sets of maximal conductances may be found in identified neurons across animals, there may be strong evolutionary pressure to restrict the Q
10
's of the processes that contribute to temperature compensation of neuronal circuits.
The 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 (Q
10
's) of synapses and membrane currents. We used computational models to show that the experimentally measured Q
10
'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' Q
10
'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.