The human ventilatory response to stress: rate or depth?

Abstract

Many stressors cause an increase in ventilation in humans. This is predominantly reported as an increase in minute ventilation (V̇E). But, the same V̇E can be achieved by a wide variety of changes in the depth (tidal volume, V_T ) and number of breaths (respiratory frequency, ƒ_R ). This review investigates the impact of stressors including: cold, heat, hypoxia, pain and panic on the contributions of ƒ_R and V_T to V̇E to see if they differ with different stressors. Where possible we also consider the potential mechanisms that underpin the responses identified, and propose mechanisms by which differences in ƒ_R and V_T are mediated. Our aim being to consider if there is an overall differential control of ƒ_R and V_T that applies in a wide range of conditions. We consider moderating factors, including exercise, sex, intensity and duration of stimuli. For the stressors reviewed, as the stress becomes extreme V̇E generally becomes increased more by ƒ_R than V_T . We also present some tentative evidence that the pattern of ƒ_R and V_T could provide some useful diagnostic information for a variety of clinical conditions. In The Physiological Society's year of 'Making Sense of Stress', this review has wide-ranging implications that are not limited to one discipline, but are integrative and relevant for physiology, psychophysiology, neuroscience and pathophysiology.

Keywords: cold; heat; neurophysiology; pain; panic; respiratory frequency; tidal volume; ventilation.

Figure 1. The route by which V _T and ƒ_R may be altered

Reproduced from Younes & Remmers, 1981 (with permission).

Figure 2. Increase in tidal volume and respiratory frequency in response to the cold shock response cold exposure for ≤120 s (A) and prolonged cooling (>120 s; B)

Data extracted from the following references: Barwood et al. (2013, 2014); Frank et al. (1997); Eglin & Tipton (2005); Hayashi et al. (2006); Mantoni et al. (2007, 2008); Button et al. (2015); Eglin et al. (2015); Wagner & Horvath, (1985); Tipton & Golden (1987); Tipton et al. (1991).

Figure 3. Increase in tidal volume and respiratory frequency in response to passive heating (A) and the combination of exercise and heat exposure (B)

Data extracted from the following references: Cabanac & White (1995); Curtis et al. (2007, 2008b); Fan et al. (2008); Fujii et al. (2008a,b, 2012); Hayashi et al. (2006, 2011); Nelson et al. (2011, 2012); Tsuji et al. (2012a,b).

Figure 4. Increase in tidal volume and respiratory frequency in response to hypoxic exposure

Filled triangle represents individuals who required supplementary oxygen and the filled square represents those who did not require supplementary oxygen at altitude (5200 m) (Bernardi et al. 2006). Data extracted from the following references: Berssenbrugge et al. (1983); Easton & Anthonisen (1988); Georgopoulos et al. (1989); Morelli et al. (2004); Bernardi et al. (2006); Curtis et al. (2007); Savourey et al. (2007); Faiss et al. (2013); Richard et al. (2014); Puthon et al. (2016).

Figure 5. Increase in tidal volume and respiratory frequency in response to ‘panic’ induced by CO₂ inhalation (hypercarbia)

Open diamonds represent anxiety associated with anticipatory electric shock (Masaoka & Homma, 2001) and open squares represent social anxiety associated with being touched by an individual (Wilhelm et al. 2001). Data extracted from the following references: Papp et al. (1997); Pine et al. (1998, 2000); Gorman et al. (2000); Masaoka & Homma (2001); Wilhelm et al. (2001); Bailey & Holt (2002); Hoit et al. (2007).

Figure 6. Increase in tidal volume and respiratory frequency in response to painful stimuli

The filled circles represent data from research in which pain was induced by a combination of ischaemia and cutaneous electrical stimulation (Sarton et al. 1997). The open triangles represent pain experienced before an intercostobrachial nerve block in hand injuries (Bourke, 1997) and the open squares represent post‐cholecystectomy operative pain (Joris et al. 1992). Data extracted from the following references: Duranti et al. (1991); Joris et al. (1992); Bourke (1997); Sarton et al. (1997).

Figure 7. The brainstem respiratory network.

The brainstem respiratory network is organized into compartments that extend from the pons to caudal areas of the medulla. These include in the pons the Kolliker‐Fuse nucleus (KF) and the lateral parabrachial region (LPBr). In the medulla exists the ventral respiratory column (VRC) consisting of (rostral to caudal) the Bötzinger complex (BötC), pre‐Bötzinger complex (Pre‐BötC), the rostral and caudal ventral respiratory groups (r/c VRG). The VRC is located ventral to the nucleus ambiguus (NA), caudal to the facial nucleus (VII) and extends to the lateral reticular nucleus (LRt). Much interconnectivity between the Bötzinger and pre‐Bötzinger complexes is reciprocally inhibitory whereas the projections from central chemoreceptive areas coexisting within the retrotrapezoid nucleus (RTN) and the parafacial respiratory group (pFRG) are excitatory to the VRC. The KF plays a dominant role in cranial–spinal motor co‐ordination and respiratory phase switching. Visceral afferents such as lung inflation and peripheral chemoreceptor inputs relay via the nucleus tractus solitarii in the dorsomedial medulla (not shown) and connect directly or indirectly (via the pons) to the VRC. The image on the left is a parasagittal section from a rat brainstem. Abbreviations: Pn, ventral pontine nucleus; LRt, lateral reticular nucleus; SO, superior olive; Scp, superior cerebellar peduncle; V, motor nucleus of the trigeminal nerve.