Drive to the human respiratory muscles

Abstract

The motor control of the respiratory muscles differs in some ways from that of the limb muscles. Effectively, the respiratory muscles are controlled by at least two descending pathways: from the medulla during normal quiet breathing and from the motor cortex during behavioural or voluntary breathing. Neurophysiological studies of single motor unit activity in human subjects during normal and voluntary breathing indicate that the neural drive is not uniform to all muscles. The distribution of neural drive depends on a principle of neuromechanical matching. Those motoneurones that innervate intercostal muscles with greater mechanical advantage are active earlier in the breath and to a greater extent. Inspiratory drive is also distributed differently across different inspiratory muscles, possibly also according to their mechanical effectiveness in developing airway negative pressure. Genioglossus, a muscle of the upper airway, receives various types of neural drive (inspiratory, expiratory and tonic) distributed differentially across the hypoglossal motoneurone pool. The integration of the different inputs results in the overall activity in the muscle to keep the upper airway patent throughout respiration. Integration of respiratory and non-respiratory postural drive can be demonstrated in respiratory muscles, and respiratory drive can even be observed in limb muscles under certain circumstances. Recordings of motor unit activity from the human diaphragm during voluntary respiratory tasks have shown that depending on the task there can be large changes in recruitment threshold and recruitment order of motor units. This suggests that descending drive across the phrenic motoneurone pool is not necessarily consistent. Understanding the integration and distribution of drive to respiratory muscles in automatic breathing and voluntary tasks may have implications for limb motor control.

Introduction

Although we may think of breathing as a mostly automatic function, we regularly make complex and precise voluntary changes in breathing, for example, to speak, eat and hold our breaths under water. The human inspiratory and expiratory muscles are skeletal muscles, but their neural control is quite different from that of most other skeletal muscles such as limb muscles. Some unique aspects of the neural control of human inspiratory muscles will be the focus of this review. How do the inspiratory muscle motor units behave? Is their neural control like other skeletal muscles? Does the size principle of recruitment apply to human inspiratory motoneurones?

From a motor control point of view, the neural circuitry for the respiratory muscles is unique because the motoneurones must be activated rhythmically and repeatedly to maintain ventilation. Their control is via two major descending pathways: the control can be automatic via bulbospinal pathways from the medulla to the motoneurones (e.g. during normal breathing) or voluntary via at least some direct corticospinal pathways (e.g. during a sniff). Additionally, the descending drive must be coordinated appropriately to activate all the inspiratory pump muscles that act on the chest wall, in concert with the upper airway muscles so as to breathe through a patent airway (Fig. 1). This coordination must occur all the time: when we are awake, sleeping, speaking, eating or exercising.

The ability to study motor unit activity in human inspiratory muscles makes it possible for us to examine the behaviour of single inspiratory motoneurones during involuntary breathing or in voluntary tasks without the effects of sedation or anaesthesia. This is not easily done in animal studies. Our laboratory has attempted to address the way that human inspiratory muscle motor control is organised and some results will be described in this review.