- Top of page
In two studies, the cold shock and diving responses were investigated after human face immersion without prior hyperventilation to explore the mechanism(s) accounting for reductions in maximal apnoeic times (ATmax) at low water temperatures. In study 1, ATmax, heart rate (HR) and cutaneous blood cell velocity were measured in 13 non-apnoea-trained males during apnoeic face immersion in 0, 10, 20 and 33°C water and room air (AIR). In study 2, six males were measured during non-apnoeic face immersion in 0, 10 and 33°C water for ventilation (), respiratory exchange ratio (RER), HR and oxygen consumption (), as well for end-tidal partial pressures of oxygen () and carbon dioxide (). Results indicated that the ATmax of 30.7 s (s.d. 7.1 s) at 0°C (P < 0.001) and 48.2 s (s.d. 16.0 s) at 10°C (P < 0.05) were significantly shorter than that of ∼58 s in AIR or 33°C. During apnoea at 0, 10, 20 and 33°C, both the deceleration of HR (P < 0.05) and peripheral vasoconstriction (P < 0.05), as well as the peak HR at 0°C (P= 0.002) were significantly greater than in AIR. At 0°C in comparison with 33°C, non-apnoeic face immersions gave peaks in (P= 0.039), RER (P= 0.025), (P= 0.032) and HR (P= 0.011), as well as lower minimum values for (P= 0.033) and HR (P= 0.002). With as the covariate, ANCOVA showed that remained significantly greater (P= 0.003) at lower water temperatures. In conclusion, during face immersion at 10°C and below, there is a non-metabolic, neurally mediated cold shock-like response that shortens apnoea, stimulates ventilation and predominates over the oxygen conserving effects of the dive response.
Several studies indicate a significant reduction in maximum apnoeic time during face-only immersion in water of 10°C and below (Whayne & Killip, 1967; White et al. 2002; Jay & White, 2006). The mechanism responsible for this reduced apnoea has yet to be determined, but it thought to be related to either the cold shock response (CSR; Tipton, 1989) and/or a cold-induced increase in metabolic rate (Lin et al. 1974; Hayward et al. 1984; Sterba & Lundgren, 1985). The CSR is elicited by sudden whole-body immersion in cold water and is characterized by an immediate tachycardia and peripheral vasoconstriction, as well as by a large inspiratory gasp followed by an uncontrolled hyperventilation (Tipton, 1989). The CSR magnitude may be related to differences in the regional densities of cutaneous cold receptors on the torso relative to those on the limbs (Tipton & Golden, 1987; Burke & Mekjavic, 1991). In contrast, the diving response (DR) that follows apnoeic face-only immersion is characterized by a bradycardia, peripheral vasoconstriction and an elevated blood pressure (Gooden, 1994). The DR has been demonstrated to have an oxygen conserving effect in trained apnoeic divers in water of ∼10°C (Andersson et al. 2002, 2004). This effect appears to be sufficient both to prolong voluntary apnoea (Schagatay & Andersson, 1998) and to suppress ventilation (Mukhtar & Patrick, 1986). However, evidence suggests that a DR is not always evident. Face-only immersion in water of 17°C stimulated ventilation (Stewart et al. 1998), and this hyperventilation may be coupled to an increased metabolic rate (Hayward et al. 1984; Sterba & Lundgren, 1985).
The CSR has been suggested to be the predominant initial physiological response in ∼5 to ∼20°C water during both whole-body submersion (Sterba & Lundgren, 1979, 1985; Hayward et al. 1984) and whole-body, head-out immersion (Tipton, 1989). This is thought to be a consequence of a large afferent drive from cutaneous cold receptors directly stimulating the respiratory control centre in the medulla oblongata (Tipton, 1989). However, it has yet to be ascertained whether the CSR occurs with face-only immersion in water below ∼10°C, when maximal reductions in apnoeic times are evident (Whayne & Killip, 1967; White et al. 2002; Jay & White, 2006).
The aim of the present investigation was to explore the mechanism(s) accounting for reductions in maximal apnoeic times after sudden face-only immersion at varying water temperatures. To this end, components of the CSR and DR were followed in two studies. In the first study, maximum apnoeic times, the concurrent heart rate, cutaneous blood cell velocity and haemoglobin oxygen saturation responses were measured during face-only immersion in both room air and in water between 0 and 33°C. In the second study, non-apnoeic study, ventilation, heart rate and oxygen consumption responses were measured during face-only immersion in 0, 10 and 33°C water. It was hypothesized that during face-only immersion in water of 10°C and below, there would be significantly shorter maximal apnoeic times and significantly heightened ventilation in non-apnoeic conditions. Similar to whole-body, head-out immersion, it was reasoned that apnoeic durations would be a consequence of a heightened cutaneous cold temperature-sensitive neuronal drive to inspire rather than being a consequence of oxygen conserving influences of the DR or cold-induced increase in metabolic rate.
- Top of page
The primary findings of the present investigation are that face-only immersion in colder water (≤ 10°C) reduces maximal apnoeic time (ATmax) and stimulates ventilation. The HR results (Table 1) demonstrate a novel finding that, with sudden face immersion and apnoea, a significantly greater tachycardia occurs at 0°C relative to AIR. This HR response is indicative of a cold shock-like response (CSLR) similar to the CSR with whole-body immersion in cold water (Tipton & Golden, 1987). This CSLR appears to be the underlying reason for shorter ATmax during face-only immersion at 0°C. This became evident in study 2, for non-apnoeic face immersion at 0°C and to a lesser extent at 10°C, when a hyperventilation was apparent during 60 s of face immersion relative to that in 33°C water. This was evidenced (Table 2) by significantly lower and greater peaks of , end-tidal oxygen partial pressure and the RER. Furthermore, after removing the influence on mean ventilation resulting from changes in oxygen consumption, became significantly greater with decreasing water temperature (Fig. 5), and this supported the idea that the changes in ventilation were temperature induced. Together, these results provide new evidence that a CSR, with a tachycardia and hyperventilation, is evident with non-apnoeic face immersion in cold water. There were also two striking similarities between the apnoea and non-apnoea studies. First, a tachycardia was always observed within the first seconds of face immersion at 0°C and second, this tachycardia was followed by a bradycardia (Table 1 and Fig. 4C). Thus, the time course of these two responses indicates that in the initial seconds after face immersion a CSR or a CSLR is evident. Subsequent to this, with or without apnoea, a bradycardia developed that is indicative of a DR.
The HR components of the DR during apnoeic immersion (Table 1) appeared to develop more quickly at lower water temperatures, with the mean slowing or deceleration in HR (dHR/dt) of −89.5 beats min−2 (s.d. 28.0 beats min−2) during face immersion in 0°C water being 80% greater than the mean dHR/dt value of −49.8 beats min−2 (s.d. 22.4 beats min−2) at 33°C. Many authors have previously described this inversely proportional relationship between the bradycardic response and water temperature during face immersion and apnoea (Kawakami et al. 1967; Hong, 1987; Gooden, 1994). Furthermore, the observations of a mild bradycardia and vasoconstriction with apnoea in AIR (Table 1) are also consistent with a minor DR that is evident without facial immersion and cooling (Foster & Sheel, 2005). Others have demonstrated that a DR in humans can serve as an oxygen conserving mechanism, resulting in a lower arterial oxygen desaturation (Andersson & Schagatay, 1998; Andersson et al. 2002) and a slower depletion of the lung oxygen stores during apnoea and face immersion at 10°C (Andersson et al. 2004).
Also evident during face immersion with apnoea was a greater decline in cutaneous blood cell velocity of the foot (ΔCBVfoot) and calf (ΔCBVcalf) in comparison with AIR. As such, the results are consistent with the literature that indicates the DR to be simultaneous with a cutaneous vasoconstriction (Gooden, 1994) that is also known to progressively increase over the duration of face immersion in cold water (Heistad & Abboud, 1974; Andersson et al. 2000).
It is suggested that the functional significance of the DR in humans is to facilitate a prolonged voluntary apnoea (Gooden, 1994). However, the DR may not be sufficiently strong enough in untrained breath-hold divers to prolong apnoea (Sterba & Lundgren, 1988; Schagatay et al. 1999). The maximal apnoeic times observed in study 1 showed a reduced rather than prolonged apnoea with face immersion in 0°C when there was the most pronounced bradycardic response. This suggests that the predominant mechanism accounting for reduced apnoea duration with intense skin cooling of the facial area is that of a cold temperature-sensitive neuronal drive to inspire. This heightened respiratory effort appeared to negate any potential benefits upon ATmax from the subsequent development of the DR. The maximal duration apnoea times (ATmax) observed in study 1 (Fig. 2) are in agreement with earlier observations of a significantly reduced apnoea ability at water temperatures of 10°C and below with face-only immersion (Whayne & Killip, 1967; White et al. 2002; Jay & White, 2006).
The initial tachycardia observed during the first 10–15 s of apnoeic face immersion was the primary indication of a CSLR during the face-only immersion in cold water. The magnitude of this tachycardia appeared to be temperature dependent, with the size of the peak HR reached after face immersion (ΔHRpeak) being significantly greater in 0°C water in comparison with AIR or 33°C water. Previously, a sustained mild tachycardia after a 30 s apnoea was evident at positive intra-oesophageal pressures above 10 cmH2O (Song et al. 1969). The tachycardia at these pressures has been described to be a consequence of this mechanical impairment of the venous return to the heart (Craig, 1963, 1965). However, intra-oesophageal pressure becomes more negative with a greater depth of inspiration (Agostoni & Rahn, 1960), and tachycardia during apnoea is only assured in the expiratory position (Song et al. 1969). In the present study, the depth of inspiration was 50% of IC and therefore intra-esophageal would be below 10 cm H2O and probably negative. A negative intra-oesophageal pressure would not be impairing venous return, and at 50% IC this should not result in a tachycardia (Song et al. 1969). The tachycardia reported by Song et al. (1969) was also found to be abolished with apnoea and face immersion in 5 and 20°C water across a full range of intra-oesophageal pressures. This suggests that in 5°C water, the diving bradycardia induced by face immersion would override any mechanical effects of high positive intra-oesophageal pressures that can give rise to a tachycardia. Furthermore, in study 2 for non-apnoeic face immersion, there was a significantly greater tachycardia with initial face immersion in 0°C in comparison with 33°C water when intra-oesophegeal pressures would not have been elevated. Together, these results suggest evidence of a CSLR with apnoeic face-only immersion, and this tachycardia is a consequence of skin cooling rather than resulting from a mechanical impairment of venous return.
It could be suggested that the greater tachycardia observed during the initial stages of face immersion with and without apnoea at 0°C may result from psychological factors, such as the anxiety associated with immersing the face in stirred ice water (0°C). While this is a possibility, it seems unlikely, since there was no significant main effect of immersion condition upon HRrest at the point of immersion in either the apnoea or the non-apnoea study.
In comparison with whole-body, head-out immersions, the magnitude of the stimulation of ventilation appears proportionally smaller. In 10°C water without apnoea, increases in ventilation from rest of 600% (Cooper et al. 1976) and as high as 1000% (Tipton & Golden, 1987) were evident during the first minute of whole-body, head-out immersion. In the present study, non-apnoeic face immersion gave a mean peak ventilation that was 97% greater than that at 33°C. Likewise, HR increases upon whole-body, head-out immersion ranged from 20 beats · min−1 in 27°C water (Cooper et al. 1976) to between 87 and 129 beats · min−1 in 0°C water (Hayward & Eckerson, 1984). Presently in the non-apnoeic face immersion at 0°C, the HR increased by only 19 beats · min−1 (s.d. 5 beats · min−1) for the non-apnoeic face immersion. These smaller ventilation and HR responses for the present non-apnoeic face immersion study in comparison with whole-body, head-out immersion CSR (Cooper et al. 1976; Tipton & Golden, 1987) are most likely to be a consequence of the smaller facial area immersed. However, this CSR could also be influenced by variations in the surface density of cold receptors per unit area. Burke & Mekjavic (1991) employed mouth occlusion pressures and a surface-area-corrected cold sensitivity index that gave a greater gasp response for the torso in comparison with the arms or legs. This suggested a greater density of cold receptors per unit area on the torso relative to the limbs of their cold-immersed volunteers. However, is it noteworthy that Tipton & Golden (1987) showed just the opposite, in that limbs gave a greater gasp response than the torso on cold immersion. These two studies (Tipton & Golden, 1987; Burke & Mekjavic, 1991) highlight that the regional surface density of cold receptors is another contribution that needs to be considered when comparing magnitudes of cold shock responses for the whole-body, head-out and face-only immersions.
The CSR found during non-apnoeic face immersion appears to be similar in several respects to the CSR found with whole-body, head-out immersion. The response occurred within 10 s of face immersion, suggesting a cutaneous-induced neural stimulation of ventilation. This time frame was not sufficient for changes in core temperature and a subsequent thermoregulatory metabolic response. Both the HR elevations with apnoeic face immersion as well as changes in ventilation for non-apnoeic face immersion appear to be dependent on water temperature and therefore upon the rate of facial skin cooling. It is proposed, similar to that for whole-body immersion, that face immersion with or without apnoea gives an increased inspiratory effort that is initiated by afferent sensory information arising from the cutaneous cold-sensitive neurones of the face. These cutaneous cold-sensitive neurones are located in the superficial epidermal layer (Hensel et al. 1951) and they increase ventilation by directly stimulating the respiratory centre (Keatinge & Evans, 1961; Duffin et al. 1975). Such a neural reflex pathway for the stimulation of ventilation with face cooling has previously been ascribed to long descending axons that arise from the ophthalmic division of the trigeminal nerve. This division of the trigeminal nerve primarily conveys senses of temperature, possibly making monosynaptic contacts with the respiratory rhythm generator in the pons and medulla oblongata (Stewart et al. 1998).
Some previous literature has suggested that shorter apnoeic times in lower water temperatures result from elevated metabolic rates (Lin et al. 1974; Hayward et al. 1984; Sterba & Lundgren, 1985). With variance resulting from oxygen consumption removed, mean still showed a temperature dependence (Fig. 5), suggesting a non-metabolic cutaneous cold temperature-sensitive neuronal stimulation of ventilation with face-only immersion in cold water. As mentioned above, this statement is made with the provision that end-tidal gases were representative of alveolar gases and that responses reflected metabolic changes.
To further describe the mechanisms of the CSR or CSLR during face-only immersion, future studies appear warranted. The ventilation components of the CSR apparent during non-apnoeic face immersion need to be measured across a larger range of water temperatures and over a longer immersion period. It is apparent that the 60 s duration for the non-apnoeic immersions in study 2 may have restricted the observed amplitude of the CSR and DR response, since a physiologically steady condition was probably not achieved. Our next studies will be to establish the extent of the temperature dependence, the magnitude and the time course of this response.
In conclusion, in males not trained for apnoea, face-only immersion at 10°C and below results in significantly shorter apnoeic durations. It is proposed that this is a consequence of a cutaneous cold temperature-sensitive neuronal drive to inspire that is indicative of a cold shock-like response. This drive predominates over the potential oxygen conserving and apnoea prolonging effects of a diving response and the potential apnoea shortening increases in metabolic rate at lower water temperatures. During the initial seconds of face-only immersion in these lower water temperatures, this was supported by significant heart rate elevations, with and without apnoea, and by significantly heightened ventilation without apnoea.