Precise Temperature Compensation of Phase in a Rhythmic Motor Pattern e1000469

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 temper...

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Published inPLoS biology Vol. 8; no. 8
Main Authors Tang, Lamont S, Goeritz, Marie L, Caplan, Jonathan S, Taylor, Adam L, Fisek, Mehmet, Marder, Eve
Format Journal Article
LanguageEnglish
Published San Francisco Public Library of Science 01.08.2010
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Abstract 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 (Q10~2.3) 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 Q10's of the input conductance, synaptic currents, transient outward current (IA), and the hyperpolarization-activated inward current (Ih), 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 Q10'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 Q10's of the processes that contribute to temperature compensation of neuronal circuits.
AbstractList 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 (Q10~2.3) 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 Q10's of the input conductance, synaptic currents, transient outward current (IA), and the hyperpolarization-activated inward current (Ih), 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 Q10'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 Q10's of the processes that contribute to temperature compensation of neuronal circuits.
Author Taylor, Adam L
Caplan, Jonathan S
Fisek, Mehmet
Marder, Eve
Tang, Lamont S
Goeritz, Marie L
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Copyright 2010 Tang et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Tang LS, Goeritz ML, Caplan JS, Taylor AL, Fisek M, et al. (2010) Precise Temperature Compensation of Phase in a Rhythmic Motor Pattern. PLoS Biol 8(8): e1000469. doi:10.1371/journal.pbio.1000469
Copyright_xml – notice: 2010 Tang et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Tang LS, Goeritz ML, Caplan JS, Taylor AL, Fisek M, et al. (2010) Precise Temperature Compensation of Phase in a Rhythmic Motor Pattern. PLoS Biol 8(8): e1000469. doi:10.1371/journal.pbio.1000469
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