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The Journal of Neuroscience, August 8, 2007, 27(32):8709-8718; doi:10.1523/JNEUROSCI.1274-07.2007

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Cellular/Molecular
Neuromodulators, Not Activity, Control Coordinated Expression of Ionic Currents

Olga Khorkova¹ and Jorge Golowasch^1,2

¹Federated Department of Biological Sciences and ²Department of Mathematical Sciences, New Jersey Institute of Technology, Newark, New Jersey 07102

Correspondence should be addressed to Jorge Golowasch, Department of Mathematical Sciences, New Jersey Institute of Technology, University Heights, Newark, NJ 07102. Email: jorge.p.golowasch{at}njit.edu

Electrical activity in identical neurons across individuals is often remarkably similar and stable over long periods. However, the ionic currents that determine the electrical activity of these neurons show wide animal-to-animal amplitude variability. This seemingly random variability of individual current amplitudes may obscure mechanisms that globally reduce variability and that contribute to the generation of similar neuronal output. One such mechanism could be the coordinated regulation of ionic current expression. Studying identified neurons of the Cancer borealis pyloric network, we discovered that the removal of neuromodulatory input to this network (decentralization) was accompanied by the loss of the coordinated regulation of ionic current levels. Additionally, decentralization induced large changes in the levels of several ionic currents. The loss of coregulation and the changes in current levels were prevented by continuous exogenous application of proctolin, an endogenous neuromodulatory peptide, to the pyloric network. This peptide does not exert fast regulatory actions on any of the currents affected by decentralization. We conclude that neuromodulatory inputs to the pyloric network have a novel role in the regulation of ionic current expression. They can control, over the long term, the coordinated expression of multiple voltage-gated ionic currents that they do not acutely modulate. Our results suggest that current coregulation places constraints on neuronal intrinsic plasticity and the ability of a network to respond to perturbations. The loss of conductance coregulation may be a mechanism to facilitate the recovery of function.

Key words: neuromodulation; ionic currents; coregulation; activity; crustacean; stomatogastric; decentralization

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Received March 21, 2007; revised June 26, 2007; accepted June 27, 2007.

Correspondence should be addressed to Jorge Golowasch, Department of Mathematical Sciences, New Jersey Institute of Technology, University Heights, Newark, NJ 07102. Email: jorge.p.golowasch{at}njit.edu

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