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Modeling of sustained spontaneous network oscillations of a sexually dimorphic brainstem nucleus: the role of potassium equilibrium potential

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Abstract

Intrinsic oscillators in the central nervous system play a preeminent role in the neural control of rhythmic behaviors, yet little is known about how the ionic milieu regulates their output patterns. A powerful system to address this question is the pacemaker nucleus of the weakly electric fish Apteronotus leptorhynchus. A neural network comprised of an average of 87 pacemaker cells and 20 relay cells produces tonic oscillations, with higher frequencies in males compared to females. Previous empirical studies have suggested that this sexual dimorphism develops and is maintained through modulation of buffering of extracellular K+ by a massive meshwork of astrocytes enveloping the pacemaker and relay cells. Here, we constructed a model of this neural network that can generate sustained spontaneous oscillations. Sensitivity analysis revealed the potassium equilibrium potential, EK (as a proxy of extracellular K+ concentration), and corresponding somatic channel conductances as critical determinants of oscillation frequency and amplitude. In models of both the pacemaker nucleus network and isolated pacemaker and relay cells, the frequency increased almost linearly with EK, whereas the amplitude decreased nonlinearly with increasing EK. Our simulations predict that this frequency increase is largely caused by a shift in the minimum K+ conductance over one oscillation period. This minimum is close to zero at more negative EK, converging to the corresponding maximum at less negative EK. This brings the resting membrane potential closer to the threshold potential at which voltage-gated Na+ channels become active, increasing the excitability, and thus the frequency, of pacemaker and relay cells.

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Acknowledgements

We would like to thank Masashi Kawasaki (University of Virginia, Charlottesville) for fruitful discussion, as well as the two anonymous reviewers for their helpful comments on the manuscript. This research was supported by Grant 1946910 and Research Experiences for Undergraduates Supplement to Grant 1538505, both from the National Science Foundation (GKHZ); an Advanced Research/Creative Endeavor Award, a PEAK Experiences Trailblazer Award, and a Dr. Andrew I. Schafer Researcher Co-op Scholarship, all from Northeastern University (DH); and a Hungarian State Eötvös Scholarship from the Tempus Public Foundation (DL). We would also like to acknowledge the generous computational and technical support provided by the Northeastern University Discovery Cluster and ITS Research Computing Department.

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  1. Daniel Hartman and Dávid Lehotzky contributed equally to this work

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  1. Laboratory of Neurobiology, Department of Biology, Northeastern University, Boston, MA, 02115, USA

    Daniel Hartman, Dávid Lehotzky, Iulian Ilieş & Günther K. H. Zupanc

  2. Research Computing, Northeastern University, Boston, MA, 02115, USA

    Mariana Levi

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Hartman, D., Lehotzky, D., Ilieş, I. et al. Modeling of sustained spontaneous network oscillations of a sexually dimorphic brainstem nucleus: the role of potassium equilibrium potential. J Comput Neurosci 49, 419–439 (2021). https://doi.org/10.1007/s10827-021-00789-2

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