Precise temperature compensation of phase in a rhythmic motor pattern.

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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Main Authors: Lamont S Tang, Marie L Goeritz, Jonathan S Caplan, Adam L Taylor, Mehmet Fisek, Eve Marder
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2010-08-01
Series:PLoS Biology
Online Access:http://europepmc.org/articles/PMC2930868?pdf=render
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spelling doaj-3f60e233aa4f486299deb202a77ace932021-07-02T06:09:57ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852010-08-018810.1371/journal.pbio.1000469Precise temperature compensation of phase in a rhythmic motor pattern.Lamont S TangMarie L GoeritzJonathan S CaplanAdam L TaylorMehmet FisekEve MarderMost 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) approximately 2.3) as the temperature was shifted from 7 degrees C to 23 degrees 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.http://europepmc.org/articles/PMC2930868?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Lamont S Tang
Marie L Goeritz
Jonathan S Caplan
Adam L Taylor
Mehmet Fisek
Eve Marder
spellingShingle Lamont S Tang
Marie L Goeritz
Jonathan S Caplan
Adam L Taylor
Mehmet Fisek
Eve Marder
Precise temperature compensation of phase in a rhythmic motor pattern.
PLoS Biology
author_facet Lamont S Tang
Marie L Goeritz
Jonathan S Caplan
Adam L Taylor
Mehmet Fisek
Eve Marder
author_sort Lamont S Tang
title Precise temperature compensation of phase in a rhythmic motor pattern.
title_short Precise temperature compensation of phase in a rhythmic motor pattern.
title_full Precise temperature compensation of phase in a rhythmic motor pattern.
title_fullStr Precise temperature compensation of phase in a rhythmic motor pattern.
title_full_unstemmed Precise temperature compensation of phase in a rhythmic motor pattern.
title_sort precise temperature compensation of phase in a rhythmic motor pattern.
publisher Public Library of Science (PLoS)
series PLoS Biology
issn 1544-9173
1545-7885
publishDate 2010-08-01
description 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) approximately 2.3) as the temperature was shifted from 7 degrees C to 23 degrees 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.
url http://europepmc.org/articles/PMC2930868?pdf=render
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