Activation of the human diaphragm during a repetitive postural task

Abstract

The co-ordination between respiratory and postural functions of the diaphragm was investigated during repetitive upper limb movement. It was hypothesised that diaphragm activity would occur either tonically or phasically in association with the forces from each movement and that this activity would combine with phasic respiratory activity. Movements of the upper limb and ribcage were measured while standing subjects performed repetitive upper limb movements 'as fast as possible'. Electromyographic (EMG) recordings of the costal diaphragm were made using intramuscular electrodes in four subjects. Surface electrodes were placed over the deltoid and erector spinae muscles. In contrast to standing at rest, diaphragm activity was present throughout expiration at 78 +/- 17% (mean +/- s.d.) of its peak inspiratory magnitude during repeated upper limb movement. Bursts of deltoid and erector spinae EMG activity occurred at the limb movement frequency (approximately 2.9 Hz). Although the majority of diaphragm EMG power was at the respiratory frequency (approximately 0.4 Hz), a peak was also present at the movement frequency. This finding was corroborated by averaged EMG activity triggered from upper limb movement. In addition, diaphragm EMG activity was coherent with ribcage motion at the respiratory frequency and with upper limb movement at the movement frequency. The diaphragm response was similar when movement was performed while sitting. In addition, when subjects moved with increasing frequency the peak upper limb acceleration correlated with diaphragm EMG amplitude. These findings support the argument that diaphragm contraction is related to trunk control. The results indicate that activity of human phrenic motoneurones is organised such that it contributes to both posture and respiration during a task which repetitively challenges trunk posture.

Figures

Figure 1. Raw EMG and movement data from a typical subject before, during and after rapid upper limb movements

Subjects maintained quiet respiration prior to movement. In the post-movement period subjects were instructed to breath normally followed by a deep inspiration with deliberate expiration through pursed lips. EMG activity recorded from the diaphragm intramuscular electrodes during inspiration but not forced expiration (final panel) indicates that the electrode remained in the diaphragm. In the first and third panels the diaphragm EMG during inspiration is presented at three times the amplification. Note that the diaphragm EMG activity during repetitive movement of the upper limb as fast as possible is modulated with respiration and persists during expiration. Insp, inspiration. EMG calibration, 500 μV. Upper limb movement range, −15 to 15 deg.

Figure 3. Power spectral densities and averaged data

The power spectrum and averaged data are presented for a representative subject for breathing with upper limb movement (A) and breathing without movement (B). The power spectra in A and B were calculated for 20 s periods of movement with breathing and breathing without movement, respectively, for a different subject to that presented in Figs 1 and 2. The vertical dashed lines indicate the frequencies of respiration (left) and upper limb movement (right) in A and the frequency of respiration in B. In A note the peak in the upper limb movement signal at approximately 3 Hz and the corresponding peaks in all EMG signals at this frequency and the smaller peaks at twice the movement frequency. In addition note the peak in the ribcage and diaphragm signals at the respiratory frequency of approximately 0.4 Hz. In B peaks of the diaphragm and ribcage movement signals are present at the respiratory frequency. Averaged data were aligned to the onset of upper limb flexion in A and to the onset of inspiration in B, as denoted by the arrows. The background levels of diaphragm and erector spinae EMG activity are shown by dark grey region presented in the average data for the expiratory trials. Vertical calibrations for power spectra: anterior deltoid EMG, 2 μV2; posterior deltoid EMG, 4 μV2; erector spinae EMG, 2.5 μV2; diaphragm EMG, 12.5 μV2; upper limb movement, 12 deg2; ribcage signal, 2 V2. Vertical calibrations for the averaged EMG data: anterior deltoid, 10 μV; posterior deltoid, 20 μV; erector spinae, 5 μV; diaphragm, 20 μV. Upper limb movement range: −15 to 15 deg.

Figure 2. Diaphragm EMG activity during movement with and without breathing

Raw diaphragm EMG from a typical subject during upper limb movement with apnoea and breathing is presented in A and C, respectively. Diaphragm r.m.s. EMG amplitudes for all subjects expressed as a percentage of the inspiratory r.m.s. EMG during upper limb movement with apnoea and breathing are presented in B and D, respectively. The 1 s segments selected for calculation of the r.m.s. EMG amplitude are indicated by the shaded vertical bars. Note the presence of diaphragm EMG activity during expiration with upper limb movement and when movement was performed without breathing. EMG calibration, 1 mV. Symbols indicate different subjects (S1–4).

Figure 4. Coherence analysis

Coherence between signals are presented for a typical subject along with the group mean recorded at the movement frequency (vertical dashed line at ≈3.5 Hz) along with the group mean for the diaphragm- ribcage coherence at the respiratory frequency (vertical dashed line at ≈0.4 Hz). Coherence approached 1 for all muscles with movement and between muscles at the movement frequency. At the respiratory frequency diaphragm EMG is the only signal coherent with the ribcage motion at the respiratory frequency. Abbreviations: AntD, anterior deltoid; Dia, diaphragm; ES, erector spinae; PostD, posterior deltoid.

Figure 5. Relationship between trunk muscle EMG and acceleration of the upper limb

A, root mean squared EMG amplitude calculated for 100 ms epochs of diaphragm and erector spinae are presented for a trial in which the frequency of upper limb movement increased from approximately 1 Hz to movement performed as fast as possible. Root mean squared EMG activity during inspiration and expiration preceding movement is shown to the left. EMG amplitude increased as the frequency of voluntary movement increased. I, inspiration; E, expiration. Vertical calibrations: diaphragm EMG, 25 μV; erector spinae EMG, 1 mV; shoulder displacement range, 15 to −15 deg; shoulder peak acceleration, 0.006 deg s−2. B, correlation between peak upper limb acceleration and r.m.s. EMG of diaphragm and erector spinae. Mean inspiratory and expiratory r.m.s. EMG levels are shown for comparison. There is a linear relationship between peak upper limb acceleration and EMG amplitudes (P < 0.001).

Figure 6. Diaphragm activity during rapid repetitive upper limb movement while sitting

Representative raw EMG and movement signals for upper limb movement during sitting (A) and corresponding power spectral densities (B). Note that similar to the data presented in Fig. 3 there are peaks in the diaphragm EMG power spectrum at the frequencies of respiration and upper limb movement. EMG calibration, 500 μV. Upper limb movement range is −15 to 15 deg. Vertical calibrations for power spectra: anterior deltoid EMG, 1 μV2; posterior deltoid EMG, 1 μV2; upper limb movement, 6 deg2; diaphragm EMG, 15 μV2; ribcage signal, 1 V2.

Figure 7. Integration of respiratory and ‘postural’ inputs to phrenic motoneurones

A, diaphragmatic representation of the four types of diaphragm EMG that have been identified (shown as rectified and low-pass filtered EMG). The upper trace shows a single burst of diaphragm EMG that occurs with single repetitions of upper limb flexion. In the second trace there is tonic activity in addition to superimposed phasic bursts of diaphragm EMG with repetitive upper limb movement. The third trace shows summation of inspiratory diaphragm EMG with the combined tonic and phasic modulation with repetitive upper limb movement. The lowest trace and the dashed line in the third trace show inspiratory diaphragm EMG. B, multiple inputs to the phrenic motoneurones arising from respiratory centres, (non-respiratory) higher centres and a variety of peripheral sources. Although the inspiratory drive arises predominantly from the ponto-medullary respiratory centres, ‘postural’ inputs may arise from higher centres, but during predictable repetitive movements some inputs may be reflex in origin and act at either spinal or supraspinal levels. Dashed lines indicate hypothesised inputs that have not been confirmed in the literature. (See Discussion for detail and references.)