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Positive feedback loops sustain repeating bursts in neuronal circuits

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Abstract

Voluntary movements in animals are often episodic, with abrupt onset and termination. Elevated neuronal excitation is required to drive the neuronal circuits underlying such movements; however, the mechanisms that sustain this increased excitation are largely unknown. In the medicinal leech, an identified cascade of excitation has been traced from mechanosensory neurons to the swim oscillator circuit. Although this cascade explains the initiation of excitatory drive (and hence swim initiation), it cannot account for the prolonged excitation (10–100 s) that underlies swim episodes. We present results of physiological and theoretical investigations into the mechanisms that maintain swimming activity in the leech. Although intrasegmental mechanisms can prolong stimulus-evoked excitation for more than one second, maintained excitation and sustained swimming activity requires chains of several ganglia. Experimental and modeling studies suggest that mutually excitatory intersegmental interactions can drive bouts of swimming activity in leeches. Our model neuronal circuits, which incorporated mutually excitatory neurons whose activity was limited by impulse adaptation, also replicated the following major experimental findings: (1) swimming can be initiated and terminated by a single neuron, (2) swim duration decreases with experimental reduction in nerve cord length, and (3) swim duration decreases as the interval between swim episodes is reduced.

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Abbreviations

ADO:

Adenosine

BPE:

Bursts per episode

DP:

Dorsal posterior (nerve)

CNS:

Central nervous system

CPG:

Central pattern generator

IN:

Interneuron

MN:

Motoneurons

RCI:

Recurrent cyclic inhibition

RE:

Reciprocally excitatory

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Acknowledgement

Funding was provided by NSF grant IOB-0615631.

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Authors and Affiliations

  1. Department of Biology, University of Virginia, P.O. Box 400328, Charlottesville, VA, 22904-4328, USA

    Wolfgang Otto Friesen, Olivia J. Mullins & Ran Xiao

  2. Neuroscience Graduate Program, University of Virginia, Charlottesville, VA, 22904-4328, USA

    Wolfgang Otto Friesen, Olivia J. Mullins & John T. Hackett

  3. Department of Molecular Physiology and Biological Physics, University of Virginia, Charlottesville, VA, 22904-4328, USA

    John T. Hackett

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  1. Wolfgang Otto Friesen
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Correspondence to Wolfgang Otto Friesen.

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Friesen, W.O., Mullins, O.J., Xiao, R. et al. Positive feedback loops sustain repeating bursts in neuronal circuits. J Biol Phys 37, 317–345 (2011). https://doi.org/10.1007/s10867-010-9210-8

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