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The Journal of Neuroscience, September 3, 2003, 23(22):8152-8158

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Oscillations in Endogenous Inputs to Neurons Affect Excitability and Signal Processing

Marjorie A. Parkis,² Jack L. Feldman,³ Dean M. Robinson,¹ and Gregory D. Funk^1,4

¹Department of Physiology, Faculty of Medical and Health Sciences, University of Auckland, Auckland, New Zealand, ²Department of Organismal Biology and Anatomy, University of Chicago, Chicago, Illinois 60637, ³Systems Neurobiology Laboratory, Department of Neurobiology, University of California, Los Angeles, Los Angeles, California 90095-1763, and ⁴Department of Physiology, Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Alberta, T6G 2H7, Canada

Synchrony and oscillations in neuronal firing play important roles in information processing in the mammalian brain. Here, we evaluate their role in controlling neuronal output in a well defined motor behavior, breathing, using an in vitro preparation from neonatal rat that generates respiratory-related motor output. In this preparation, phrenic motoneurons (PMNs) receive endogenous rhythmic inspiratory currents with prominent oscillations in the 20-50 Hz range. We recorded these inspiratory currents in individual PMNs and used them as test inputs for the same motoneuron (MN) during the normally silent expiratory periods. The impact of the oscillations on MN output was evaluated by filtering the currents before injection. Responses to unfiltered inspiratory currents were indistinguishable from voltage changes during spontaneous inspiratory periods. More than 90% of action potentials occurred within milliseconds [-2 to +4] of the oscillation peaks. The timing of action potentials was highly reproducible in response to unfiltered currents. Attenuation of the oscillations by low-pass filtering (<50 Hz) decreased the precision in action potential timing and significantly reduced the number of action potentials by 35%. The adrenergic agonist phenylephrine increased instantaneous firing frequency in responses evoked by square-wave or low-pass filtered inspiratory currents but had no effect on firing frequency evoked by unfiltered currents. We conclude that oscillations control the precise timing of action potentials, help to maximize synaptic drive efficiency, and constrain MN firing frequencies to those optimal for muscle contraction.

Key words: oscillation; phrenic motoneuron; phenylephrine; respiration; excitability; rat; whole-cell recording

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Received Feb 12, 2003; revised May 22, 2003; accepted June 30, 2003.

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