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Precise temperature compensation of phase in a rhythmic motor pattern.

Lamont S Tang1, Marie L Goeritz, Jonathan S Caplan

  • 1Volen Center and Biology Department, Brandeis University, Waltham, Massachusetts, United States of America.

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|September 9, 2010
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Summary

Cold-blooded animals maintain neuronal circuit function across temperatures. This study reveals that while pyloric rhythm frequency increases with temperature, the timing (phase) of key neurons remains stable, suggesting evolutionary pressure for temperature compensation in neuronal circuits.

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Area of Science:

  • Neuroscience
  • Comparative Physiology
  • Computational Biology

Background:

  • Neuronal circuits in cold-blooded animals must function despite environmental temperature changes.
  • Central pattern generating circuits produce rhythmic motor patterns essential for survival.
  • The stomatogastric ganglion provides a model system for studying neuronal circuit dynamics.

Purpose of the Study:

  • To investigate the effects of temperature on the pyloric rhythm in the crab Cancer borealis.
  • To determine how temperature influences the frequency and phase relationships of key neurons in the pyloric circuit.
  • To explore the role of ionic currents and computational models in temperature compensation.

Main Methods:

  • Experimental analysis of the pyloric rhythm in Cancer borealis at different temperatures (7°C to 23°C).
  • Quantification of rhythm frequency and phase relationships of Pyloric Dilator (PD), Lateral Pyloric (LP), and Pyloric (PY) neurons.
  • Development and analysis of over 1,000 computational models of bursting neurons and the LP neuron with varying maximal conductances.

Main Results:

  • Pyloric rhythm frequency increased approximately 4-fold (Q(10) ≈ 2.3) with a temperature shift from 7°C to 23°C.
  • Phase relationships between PD, LP, and PY neurons exhibited near-perfect temperature compensation.
  • Ionic currents (input conductance, synaptic currents, I(A), I(h)) had Q(10) values ranging from 1.8 to 4, influencing LP neuron phase.
  • Computational models showed that temperature compensation of LP neuron phase was enhanced when currents had Q(10) values near 2.

Conclusions:

  • Neuronal circuits in cold-blooded animals possess mechanisms for temperature compensation.
  • Despite diverse maximal conductances across neurons, evolutionary pressures likely constrain the Q(10) values of critical currents to ensure functional stability.
  • Temperature compensation is crucial for maintaining rhythmic motor patterns in ectothermic species.