Sports Med 2004; 34 (2): 117-132

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 117 1. Respiratory Effort Sensation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 118 1.1 Length-Tension Inappropriateness (LTI): A Unifying Paradigm for Dyspnoea . . . . . . . . . . . . . . . . 118 1.2 The Neurophysiology of LTI and Effort Sensation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 118 1.2.1 Motor Command . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 118 1.2.2 Afferent Scaling of the Mechanical Response . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 119 1.2.3 The Influence of Prior Experience . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 119 2. The Role of Respiratory Muscle Tension in Effort Sensation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 120 2.1 Pattern of Tension Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 120 2.2 Functional Weakening of Inspiratory Muscles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 120 2.3 Respiratory Muscle Fatigue . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 121 3. Effect of Respiratory Muscle Training Upon Respiratory Effort Sensation . . . . . . . . . . . . . . . . . . . . . . . . 123 3.1 Healthy Human Volunteers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123 3.2 Patients with Chronic Obstructive Pulmonary Disease . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 124 3.3 Patients with Asthma . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 127 4. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 129 A consistent finding of recent research on respiratory muscle training (RMT) Abstract in healthy humans has been an attenuation of respiratory discomfort (dyspnoea) during exercise. We argue that the neurophysiology of dyspnoea can be explained in terms of Cambell’s paradigm of length-tension inappropriateness. In the context of this paradigm, changes in the contractile properties of the respiratory muscles modify the intensity of dyspnoea predominantly by changing the required level of motor outflow to these respiratory muscles. Thus, factors that impair the contractile properties of the respiratory muscles (e.g. the pattern of tension development, functional weakening and fatigue) have the potential to increase the intensity of dyspnoea, while factors that improve the contractile properties of these respiratory muscles (e.g. RMT) have the potential to reduce the intensity of dyspnoea. In patients with obstructive pulmonary disease, functional weakening of the inspiratory muscles in response to dynamic lung hyperinflation appears to be a central component of dyspnoea. A decrease in the intensity of respiratory effort sensation (during exercise and loaded breathing) has been observed in both 118 McConnell & Romer healthy individuals and patients with obstructive pulmonary disease after RMT. We conclude that RMT has the potential to reduce the severity of dyspnoea in healthy individuals and in patients with obstructive pulmonary disease, and that this probably occurs via a reduction in the level of motor outflow. Further work is required to clarify the role of RMT in the management of other disease conditions in which the function of the respiratory muscles is impaired, or the loads that they must overcome are elevated (e.g. cardiorespiratory and neuromuscular disorders). Recent studies of respiratory muscle training term ‘length-tension inappropriateness’ (LTI) to ex(RMT) in healthy humans have reported post-trainplain how the sensation of dyspnoea might be ‘transing decreases in the perceptions of respiratory effort duced’ to consciousness.[7] Campbell argued that during exercise.[1-5] These findings suggest that imhumans have a quantitative, conscious appreciation provements in the contractile properties of the of the degree of effort associated with breathing, and respiratory muscles modify respiratory effort at a that dissociation or a mismatch between the central fundamental level. Abatement of unpleasant or unrespiratory motor activity and the mechanical rescomfortable respiratory effort sensations (dyspnoea) ponse of the respiratory system may produce a senis of interest to the sports and pulmonary clinician, sation of respiratory discomfort (dyspnoea). More since this holds the promise of a management tool recently, the LTI paradigm has been generalised to for those limited by these sensations. Thus, the include not only afferent sensory inputs from purpose of this review is to consider the role of respiratory muscles, but information emanating respiratory muscle function in the genesis of from receptors throughout the respiratory system.[8] dyspnoea and to examine the evidence that specific When viewed in the context of the LTI paradigm, RMT ameliorates dyspnoea. The review will draw the role of respiratory muscle function in the percepupon evidence from healthy young adults, as well as tion of dyspnoea becomes intuitively predictable. patients with chronic obstructive pulmonary disease Thus, the intensity of dyspnoea is increased when (COPD) and asthma. changes in respiratory muscle length (i.e. volume) or tension (i.e. pressure) are inappropriate for the out1. Respiratory Effort Sensation going motor command. In the ensuing sections, we will explore the neurophysiological evidence that supports the validity of the LTI paradigm. Within 1.1 Length-Tension Inappropriateness (LTI): A the context of LTI, we will also consider the role of Unifying Paradigm for Dyspnoea respiratory muscle function in the genesis of Throughout this review we use the term ‘respiradyspnoea. tory effort sensation’ to describe the distillation of 1.2 The Neurophysiology of LTI and sensations associated with the urge to breathe and Effort Sensation the sensory experience that arises from the motor response to that urge. The terms ‘breathlessness’ 1.2.1 Motor Command and ‘dyspnoea’ have been used interchangeably to describe what Jonathan Meakins termed “the conIn the years that have followed Campbell’s first sciousness of the necessity for increased respiratory enunciation of LTI,[7] neurophysiology has provided effort”.[6] Meakins’ definition of dyspnoea was the further evidence to support the assertion that there is first to provide a unifying theory to explain the a conscious awareness of the outgoing respiratory presence of dyspnoea in both patients and healthy motor command to the respiratory muscles.[9-12] It volunteers, and was developed further by Moran has been suggested that a conscious awareness of Campbell’s group in the 1960s. Campbell coined the central motor command occurs via corollary dis 2004 Adis Data Information BV. All rights reserved. Sports Med 2004; 34 (2) Dyspnoea: Role of Respiratory Muscle Function and Training 119 charge from the brainstem respiratory neurones to respiratory drive. Non-spindle group II fibres and the sensory cortex during spontaneous breathing,[9] many of the slower-conducting, thinly myelinated or from cortical motor centres to the sensory cortex group III fibres are mechanically sensitive and resduring voluntary respiratory efforts (see figure 1, pond to muscle contraction, stretch or both. Other path 1).[12] The greater the magnitude of the corollagroup III afferents and group IV afferents respond to ry signals, the greater the intensity of dyspnoea. various metabolites produced during exercise or to Evidence supporting this notion stems from studies noxious levels of mechanical strain. In the context of that have altered the coupling between motor outafferent feedback, there may also be supplemental flow and muscle tension; for example, decreased information provided by arterial chemoreceptors muscle length,[12] fatigue,[11] and partial paralysis.[10] (central and peripheral), pulmonary receptors Each of these conditions increases the sense of (stretch, irritant and C fibres), and upper airway respiratory effort associated with a given level of receptors, but their precise role is unclear and bemuscle tension (see section 2). yond the scope of this review (for detailed discussion see Banzett and Lansing[14]). Although it has 1.2.2 Afferent Scaling of the Mechanical Response been argued that sensations accompanying muscular In the LTI paradigm, central motor outflow comcontraction come from the activated muscle directly mand is referenced to afferent feedback signals from (see figure 1, path 2), the current consensus of peripheral receptors in muscle, joints and tendons. opinion is that the sensory integration of feedforGroup Ia and some group II afferents innervate ward and feedback mechanisms provides a finemuscle spindles, which signal changes in muscle tuning adjustment of the exertional signal (figure 1, fibre length (i.e. lung volume). Golgi tendon organs path 3).[8] (group Ib afferents) signal changes in intramuscular tension and exert inhibitory influences on central 1.2.3 The Influence of Prior Experience In LTI theory, prior experience is used to make judgements regarding the appropriateness of the motor command relative to the mechanical response.[7] Research suggests that this prior experience can have a substantial and rapid influence upon respiratory effort sensation. For example, using a simple category scale (0, 1, 2) to designate no load, small load, and moderate load, respectively, McCloskey[15] found that healthy volunteers downgrade the magnitude of effort to added respiratory loads following as few as 20 breaths against an increased background load. Similarly, Revelette and Wiley[16] asked study participants to estimate the magnitude of a series of inspiratory resistive loads before and after a 2-minute period of breathing against a nonfatiguing inspiratory load equivalent to 80% of their maximum inspiratory mouth pressure (MIP). Load estimates were significantly higher under the control condition than following the 80% of MIP loading task. Similar results to those found for the respiratory muscles were also obtained for load magnitude estimation in the elbow flexors.[16] Revelette and Wiley[16] offered two explanations for the acute atMotor cortex Sensory cortex Skeletal muscle Motor