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Multiple Rhythmic States in a Model of the Respiratory Central Pattern Generator

¹Department of Mathematics, University of Pittsburgh, Pittsburgh; ²Department of Neurobiology and Anatomy, Drexel University College of Medicine, Philadelphia, Pennsylvania; ³Cellular and Systems Neurobiology Section, Porter Neuroscience Research Center, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland; and ⁴A. B. Kogan Research Institute for Neurocybernetics, South Federal University, Rostov-on-Don, Russia

Submitted 22 June 2008; accepted in final form 27 January 2009

The three-phase respiratory pattern observed during normal breathing changes with alterations in metabolic or physiological conditions. A recent study using in situ perfused rat brain preparations demonstrated a reorganization of the respiratory pattern with sequential reduction of the brain stem respiratory network. Specifically, with removal of the pons, the normal three-phase pattern transformed to a two-phase inspiratory–expiratory pattern and, with more caudal transections, to one-phase, intrinsically generated inspiratory oscillations. A minimal neural network proposed to reproduce these transformations includes 1) a ringlike mutually inhibitory network composed of the postinspiratory, augmenting expiratory, and early-inspiratory neurons and 2) an excitatory preinspiratory neuron, with persistent sodium current (I_NaP)-dependent intrinsic bursting properties, that dynamically participates in the expiratory–inspiratory phase transition and inspiratory phase generation. We used activity-based single-neuron models and applied numerical simulations, bifurcation methods, and fast–slow decomposition to describe the behavior of this network in the functional states corresponding to the three-, two-, and one-phase oscillatory regimes, as well as to analyze the transitions between states and between respiratory phases within each state. We demonstrate that, although I_NaP is not necessary for the generation of three- and two-phase oscillations, it contributes to control of the oscillation period in each state. We also show that the transitions between states can be produced by progressive changes of drives to particular neurons and proceed through intermediate regimes, featuring high-amplitude late-expiratory and biphasic-expiratory activities or ectopic burst generation. Our results provide important insights for understanding the state-dependent mechanisms for respiratory rhythm generation and control.

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