Spike-firing resonance in hypoglossal motoneurons

During an inspiration the output of hypoglossal (XII) motoneurons (HMs) in vitro is characterized by synchronous oscillatory firing in the 20- to 40-Hz range. To maintain synchronicity it is important that the cells fire with high reliability and precision. It is not known whether the intrinsic properties of HMs are tuned to maintain synchronicity when stimulated with time-varying inputs. We intracellularly recorded from HMs in an in vitro brain stem slice preparation from juvenile mice. Cells were held at or near spike threshold and were stimulated with steady or swept sine-wave current functions (10-s duration; 0- to 40-Hz range). Peristimulus time histograms were constructed from spike times based on threshold crossings. Synaptic transmission was suppressed by including blockers of GABAergic, glycinergic, and glutamatergic neurotransmission in the bath solution. Cells responded to sine-wave stimulation with bursts of action potentials at low (< 3- to 5-Hz) sine-wave frequency, whereas they phase-locked 1: 1 to the stimulus at intermediate frequencies (3-25 Hz). Beyond the 1: 1 frequency range cells were able to phase-lock to subharmonics (1: 2, 1: 3, or 1: 4) of the input frequency. The 1: 1 phase-locking range increased with increasing stimulus amplitude and membrane depolarization. Reliability and spike-timing precision were highest when the cells phase-locked 1: 1 to the stimulus. Our findings suggest that the coding of time-varying inspiratory synaptic inputs by individual HMs is most reliable and precise at frequencies that are generally lower than the frequency of the synchronous inspiratory oscillatory activity recorded from the XII nerve.