Motoneuron firing patterns underlying fast oscillations in phrenic nerve discharge in the rat

Abstract

Fast oscillations are ubiquitous throughout the mammalian central nervous system and are especially prominent in respiratory motor outputs, including the phrenic nerves (PhNs). Some investigators have argued for an epiphenomenological basis for PhN high-frequency oscillations because phrenic motoneurons (PhMNs) firing at these same frequencies have never been recorded, although their existence has never been tested systematically. Experiments were performed on 18 paralyzed, unanesthetized, decerebrate adult rats in which whole PhN and individual PhMN activity were recorded. A novel method for evaluating unit-nerve time-frequency coherence was applied to PhMN and PhN recordings. PhMNs were classified according to their maximal firing rate as high, medium, and low frequency, corresponding to the analogous bands in PhN spectra. For the first time, we report the existence of PhMNs firing at rates corresponding to high-frequency oscillations during eupneic motor output. The majority of PhMNs fired only during inspiration, but a small subpopulation possessed tonic activity throughout all phases of respiration. Significant time-varying PhMN-PhN coherence was observed for all PhMN classes. High-frequency, early-recruited units had significantly more consistent onset times than low-frequency, early/middle-recruited and medium-frequency, middle/late-recruited PhMNs. High- and medium-frequency PhMNs had significantly more consistent offset times than low-frequency units. This suggests that startup and termination of PhMNs with higher firing rates are more precisely controlled, which may contribute to the greater PhMN-PhN coherence at the beginning and end of inspiration. Our findings provide evidence that near-synchronous discharge of PhMNs firing at high rates may underlie fast oscillations in PhN discharge.

Hypoxia triggers short term potentiation of phrenic motoneuron discharge after chronic cervical spinal cord injury

“…Similar to a few prior reports (Lee et al, 2013; Marchenko et al, 2012), we noted a small number of PhrMNs which burst throughout the respiratory cycle (i.e., tonic bursting). Rogers and colleagues have reported tonic PhrMN activity in spinal-intact rats (Marchenko et al, 2012), and we have observed the same using an intraspinal recording approach in spinal-intact rats (M.S.…”

“…Rogers and colleagues have reported tonic PhrMN activity in spinal-intact rats (Marchenko et al, 2012), and we have observed the same using an intraspinal recording approach in spinal-intact rats (M.S. Sandhu and D.D.…”

Patterns of Phrenic Nerve Discharge after Complete High Cervical Spinal Cord Injury in the Decerebrate Rat

“…In a previous study, we performed a systematic analysis of phrenic motoneuron discharge patterns in bulbospinal-intact decerebrate rats, which revealed distinct subpopulations of units segregating by maximal firing frequency and, within a frequency class, qualitatively exhibiting highly analogous time-frequency profiles. 75 While these firing dynamics may reflect the activity of bulbospinal inputs, they likely also represent a segregation of phrenic motoneurons by intrinsic biophysical membrane properties (i.e., action potential duration, time/space constants, and active conductances). [76][77][78][79][80][81] These motoneuronal classes, in conjunction with interneuronal elements may interact to generate phasic activity following the elimination of overriding excitatory supraspinal drive and/or descending tonic inhibition by spinal transection in conjunction with disinhibition of C 1 -C 2 prephrenic interneurons with GABAz/STR.…”

The role of spinal GABAergic circuits in the control of phrenic nerve motor output

“…2A; see also Ref. 54). Presumed interneurons (INs) were identified by the absence of uncorrelated waveform in the STA (Fig.…”