Discharge properties of human diaphragm motor units with ageing

Abstract

Key points Ageing is associated with changes in the respiratory system including in the lungs, rib cage and muscles. Neural drive to the diaphragm, the principal inspiratory muscle, has been reported to increase during quiet breathing with ageing. We demonstrated that low‐threshold motor units of the human diaphragm recruited during quiet breathing have similar discharge frequencies across age groups and shorter discharge times in older age. With ageing, motor unit action potential area increased. We propose that there are minimal functionally significant changes in the discharge properties of diaphragm motor units with ageing despite remodelling of the motor unit in the periphery. Abstract There are changes in the skeletal, pulmonary and respiratory neuromuscular systems with healthy ageing. During eupnoea, one study has shown relatively higher crural diaphragm electromyographic activity (EMG) in healthy older adults (>51 years) than in younger adults, but these measures may be affected by the normalisation process used. A more direct method to assess neural drive involves the measurement of discharge properties of motor units. Here, to assess age‐related changes in neural drive to the diaphragm during eupnoea, EMG was recorded from the costal diaphragm using a monopolar needle electrode in participants from three age groups (n ≥ 7 each): older (65–80 years); middle‐aged (43–55 years) and young (23–26 years). In each group, 154, 174 and 110 single motor units were discriminated, respectively. A mixed‐effects linear model showed no significant differences between age groups for onset (group mean range 9.5–10.2 Hz), peak (14.1–15.0 Hz) or offset (7.8–8.5 Hz) discharge frequencies during eupnoea. The motor unit recruitment was delayed in the older group (by ∼15% of inspiratory time; p = 0.02 cf. middle‐aged group) and had an earlier offset time (by ∼15% of inspiratory time; p = 0.04 cf. young group). However, the onset of multiunit activity was similar across groups, consistent with no global increase in neural drive to the diaphragm with ageing. The area of diaphragm motor unit potentials was ∼40% larger in the middle‐aged and older groups (P < 0.02), which indicates axonal sprouting and re‐innervation of muscle fibres associated with ageing, even in middle‐aged participants.

Motor unit behaviour of the ageing human diaphragm: mid‐life crisis for the inspiratory pump?

“…Of note, in the study by Nguyen et al . (), maximum inspiratory pressures were higher in middle‐aged participants compared with young participants, and were generally well protected even in older participants. Evidence of such compensation reminds us of the remarkable capacity within physiological systems to achieve homeostasis often against the odds.…”

“…Diaphragm motor unit potentials were generally of greater area, which most likely is reflective of re-innervation of denervated muscle fibres by spared phrenic motor axons, a process that commonly gives rise to grouped muscle fibres, as described in aged mouse diaphragm (Greising et al 2015). Because all assessments in the study by Nguyen et al (2019) were performed during quiet breathing, the motor potentials classified were slow fatigue-resistant units contributing to low-force production by the diaphragm, which is wholly adequate for resting breathing and indeed a broad range of ventilatory behaviours. Thus a limitation of the study acknowledged by the authors is that high-force demand motor units were not characterized, such as those recruited in support of non-ventilatory behaviours such as loaded breaths, efforts against an occluded airway, or cough.…”

“…Indeed, there is a growing interest in the design and implementation of rehabilitative strategies that strive to harness and protect compensatory neural mechanisms that limit respiratory insufficiency in affected states. In this issue of The Journal of Physiology, Nguyen et al (2019) characterize motor unit behaviour of the costal diaphragm during quiet breathing, seeking to directly address if respiratory neural drive to the primary muscle of breathing is increased with advancing age, as suggested by the observation made by other investigators of elevated normalized crural diaphragm electromyogram activity in healthy older individuals (Jolley et al 2009).…”

“…In this issue of The Journal of Physiology , Nguyen et al . () characterize motor unit behaviour of the costal diaphragm during quiet breathing, seeking to directly address if respiratory neural drive to the primary muscle of breathing is increased with advancing age, as suggested by the observation made by other investigators of elevated normalized crural diaphragm electromyogram activity in healthy older individuals (Jolley et al . ).…”

“…Because all assessments in the study by Nguyen et al . () were performed during quiet breathing, the motor potentials classified were slow fatigue‐resistant units contributing to low‐force production by the diaphragm, which is wholly adequate for resting breathing and indeed a broad range of ventilatory behaviours. Thus a limitation of the study acknowledged by the authors is that high‐force demand motor units were not characterized, such as those recruited in support of non‐ventilatory behaviours such as loaded breaths, efforts against an occluded airway, or cough.…”