Corresponding author M. D. White: Laboratory for Exercise and Environmental Physiology, 8888 University Drive, School of Kinesiology, Simon Fraser University, Burnaby, British Columbia, Canada, V5A 1S6. Email: email@example.com
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.
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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.
After approval was obtained for the experimental protocol from the Simon Fraser University Office of Research Ethics, sample sizes were determined using power calculations with β levels of 0.9 and α levels of 0.05. The effect size and standard deviations estimated for these calculations were 15 and 7% of the mean for apnoea in cold water (Hayward et al. 1984; Arnold, 1985) and 30 and 15% of the mean for ventilation in cold water (Hayward & Eckerson, 1984; Mekjavic & Bligh, 1989), respectively. To express the results at a 95% level of confidence, a minimum sample size of 12 was needed for the apnoea protocol (study 1) and a minimum sample size of five was needed for the non-apnoea protocol (study 2). In order to account for potential withdrawals, 13 male participants [aged 26 years (s.d. 6 years); height, 1.75 m (s.d. 0.1 m); weight, 74.1 kg (s.d. 10.3 kg)] volunteered for study 1; and six male participants [aged 27 years (s.d. 5 years); height, 1.83 m (s.d. 0.08 m); weight, 85.3 kg (s.d. 12.0 kg)] volunteered for study 2. Each participant was healthy, was a non-smoker, was not trained in apnoea, did not suffer from vascular diseases, was not hypertensive and had not received treatment for high blood pressure. After receiving an orientation session, a 24 h reflection period and being verbally informed of the procedures, the participant was asked to complete a health screening questionnaire and sign a written informed consent form conforming to the standards set by the Declaration of Helsinki. Each participant was asked not to drink tea or coffee during the 4 h period prior to an experiment, nor to consume alcohol in the evening preceding an experiment. A 45 min pretest session was conducted for each participant in order to provide complete familiarization with the experimental protocol, including repeatable rates of immersion, using several face immersions in 20°C water with (study 1) or without apnoea (study 2).
Inspiratory capacity (IC) of each participant in study 1 was measured in the prone position using a 13.5 l spirometer (Collins Inc., Baintree, MA, USA). Mean IC was 3.27 l (s.d. 0.62 l) All values for IC were corrected to body temperature and pressure saturated (BTPS).
In both studies, the participant lay prone on a cushioned table and suddenly immersed (i.e. no prior hyperventilation) his face into a stirred Styrofoam-insulated face-bath (0.50 m × 0.35 m × 0.23 m). Water flowed to and from the face-bath in insulated polyethylene tubing from a chiller/heater unit (model no. 1196, VWR International, Mississauga, ON, Canada) with an adjustable set-point (range 0–40°C).
For study 1, prior to each apnoea the participant inspired 50% of their predetermined IC from a 5 l rebreathing bag (Anaesthesia Assoc., Inc., San Marcos, CA, USA). The rebreathing bag was inflated with room air using a 13.5 l Collins spirometer. The rebreathing bag, a mouthpiece and a 45 cm length of 2 cm diameter corrugated respiratory tubing were connected to a three-way sliding valve (model no. 8270, Hans Rudolph Inc. Kansas City, MO, USA). The opposite end of the tubing was open to room air and was suspended by a clamp beside the face-bath. This procedure has been described previously (Jay & White, 2006).
For study 2, a mouthpiece connected a 20 cm length of rigid snorkel-shaped PVC conduit with a 2 cm inner diameter enabled the participant to breathe room air during face immersion. The opposite end of the snorkel conduit housed a mass flow sensor. Ventilation and composition of inspired and expired gases were measured using a breath-by-breath metabolic cart (model Vmax229c, Sensormedics, Yorba Linda, CA, USA). Gas samples were drawn from the participant's expired air to the metabolic cart at a rate of 0.65 l min−1. Carbon dioxide partial pressure was measured using non-dispersive infrared spectroscopy, and oxygen concentration was measured using a paramagnetic sensor. Prior to each session, gas mixtures of 4% CO2, 16% O2, balance N2; 26% O2, balance N2; and air were used to calibrate the gas analysers. A 3 l syringe was used to calibrate the mass flow sensor.
Throughout all face immersions for both studies, skin temperature was monitored at three points on the participant's face using 0.3 mm diameter T-type (copper–constantan) thermocouples (time constant < 0.5 s). Thermocouples were attached to the centre of the forehead (Tfore), the centre of the right zygomatic arch (Tcheek) and on the tip of the nose (Tnose), using surgical tape (Blenderm, 3M, St Paul, MN, USA).
Heart rate (HR) was continuously monitored using a pulse oximeter finger-clip (Masimo SET, Irvine, CA, USA) in study 1 and 2, and haemoglobin oxygen saturation ( ) was also measured and reported in study 1.
Cutaneous blood cell velocity (CBV) was used to estimate skin blood flow in study 1. The laser-Doppler probes employed had a fibre separation of 0.5 mm (moorLAB, MP12-V2 and MP7a, Moor Instruments Ltd, Axminster, UK) and were calibrated prior to testing using a flux standard of polystyrene microspheres. One probe was placed on the anterior surface of the right foot over the head of the fourth metatarsal (CBVfoot), and the second probe was positioned on the centre of the posterior surface of the right calf muscle (CBVcalf). The skin temperature of the measurement site for CBVcalf was regulated to 36.0°C (s.d. 0.1°C) using an integral skin heater (SH02, Moor Protocol Equipment, Axminster, UK). All probes were secured in place with adhesive tape.
All temperature, CBV, HR and data were monitored using a National Instruments (SCXI-1000, Austin, TX, USA) data acquisition system controlled by a personal computer using LabVIEW Software (version 7.1, National Instruments, Austin TX, USA). Samples were recorded at a frequency of 1 Hz in study 1 or on a breath-by-breath basis and subsequently averaged over 10 s intervals in study 2. Air temperatures in both studies were 22 ± 1°C.
Maximum duration apnoeas in study 1 were conducted with the participant's face immersed in water at 0, 10, 20 and 33°C or in the fifth control condition (AIR) into an empty water-bath [i.e. room air; Ta= 22°C (s.d. 1°C)]. Ventilation and HR responses in study 2 were measured with the participant's face immersed in 0, 10 and 33°C water. Presentation of the face immersion conditions in each study was balanced using a Latin square design. All face immersion conditions were repeated three times during each session at each water-bath temperature, and results are expressed as the three trial means for each participant. Common to study 1 and 2 protocols, which are each detailed below, was that all facial skin temperatures and HR had to return to pre-immersion resting values prior to the next trial. In the 33°C or AIR conditions, where no skin cooling occurred, there was a 10 min resting period before the next face immersion. Clothing insulation was standardized at ∼0.4–0.5 clo (i.e. cotton underwear, jeans, T-shirt, socks and shoes) for both studies.
Study 1 Prior to the beginning of an apnoea, the participant wore a nose-clip, lay in the prone position, breathed room air for 60 s and then, at the end of a regular breath, inhaled all of the air contained in the 5 l bag. Next, the face was immediately immersed to a depth 2 cm anterior of the tragus, and the breath was held until the breaking point. No hyperventilation was allowed prior to the apnoeas. A given apnoea was repeated if involuntary breathing movements indicative of the struggle phase were not observed before prior to the breaking point (Schagatay & Andersson, 1998).
Study 2 After instrumentation, the participant, wearing a nose-clip, lay resting in the prone position breathing room air through the snorkel conduit for 60 s with his face out of the water-bath. Next, the participant immersed his face in the water-bath to 2 cm anterior of the tragus and continued to breathe for 60 s.
Study 1 The data were analysed using a repeated-measures analyses of variance (ANOVA). The repeated factor of immersion condition (levels: 0, 10, 20 and 33°C and AIR) was employed with the dependent variables of maximal apnoea time (ATmax) and components of the HR response to face immersion as given in Fig. 1 for a sample participant. These components included HR at the point of face immersion (HRrest), magnitude of HR peak elevation after face immersion (ΔHRpeak), time to peak HR elevation (tHRpeak), minimum HR reached during face immersion (HRmin) and the deceleration of HR from HRpeak to HRmin (dHR/dt). Dependent variables also included changes in both CBVfoot and CBVcalf from the point of immersion to the minimum value reached during face immersion (ΔCBVfoot and ΔCBVcalf) and the rate of haemoglobin oxygen desaturation during apnoea (d /dt).
Study 2 The data were analysed using a one-way ANOVA with a repeated factor of immersion condition (levels: 0, 10 and 33°C) for the following dependent variables: the greatest elevations during face immersion of ventilation ( ); respiratory exchange ratio (RERmax); end-tidal oxygen partial pressure ( ) heart rate (HRpeak); and the greatest decrease during face immersion of end-tidal carbon dioxide partial pressure ( ) and heart rate (HRmin). Further analysis took place using simple linear correlations of the mean ventilation and the mean heart rate throughout immersion at 10 s intervals at 0, 10 and 33°C. An analysis of covariance (ANCOVA) was subsequently performed upon the 60 s mean of ventilation ( ) with the 60 s mean of oxygen consumption ( ) as the covariate. This was conducted by employing a simple regression model to determine what proportion of the variance in response was explained by . The model used is described below:
where: b1 is the intercept and Ω1 is the regression coefficient representing the independent contribution of to the explanation of the variance in . The residuals from this model ( ) were then assessed by a one-way ANOVA with the repeated factor of immersion condition (levels: 0, 10 and 33°C).
All analyses were performed using the statistical software package SPSS 11.5 for Windows (SPSS Inc., Chicago, IL, USA). When a significant main effect was apparent, post hoc analyses were performed on dependent variables with Student's paired t tests at each repeated level of immersion condition. The level of significance was set at 0.05.
Study 1: apnoeic face immersion
Maximal apnoeic times There was a significant main effect of immersion condition (F= 16.6, P < 0.001) upon ATmax. Significantly shorter values of ATmax were observed under the 0°C (P < 0.001) and 10°C (P= 0.045) face immersion conditions in comparison with AIR or the 33°C condition (Fig. 2).
Heart rate responses Mean values for all HR variables under each face immersion condition with apnoea are given in Table 1. For the group, there was no significant main effect of immersion condition (F= 0.6, P= 0.67) upon HRrest, and the mean HR was 73 beats · min−1 (s.d. 9 beats · min−1) at the point of immersion. There was a significant main effect of immersion condition (F= 4.9, P= 0.002) upon ΔHRpeak, with a significantly greater elevation in HR after face immersion observed under the 0°C immersion condition (P= 0.002) in comparison with AIR. There was no significant main effect of immersion condition (F= 0.5, P= 0.73) upon tHRpeak, with the mean peak HR elevation reached after 10.8 s (s.d. 4.4 s) of face immersion. There was a significant main effect of immersion condition (F= 17.8, P < 0.001) upon dHR/dt and this was explained by a significantly greater deceleration in HR from its peak elevation to the minimum values reached during apnoea in comparison with AIR under the 0°C (P < 0.001), 10 (P= 0.001), 20 (P= 0.001) and 33°C (P= 0.024) immersion conditions. There was a significant main effect of immersion condition (F= 4.7, P= 0.003) upon HRmin. This main effect was explained by significantly lower values in comparison with AIR in the 10°C (P= 0.002), 20°C (P= 0.004) and 33°C (P= 0.045) face immersions, with trend also observed for the 0°C condition (P= 0.050).
Table 1. Mean heart rate responses during apnoea and face immersion in 0°C, 10°C, 20°C and 33°C water and in the AIR control condition (study 1)
HRrest (beats · min−1)
ΔHRpeak (beats · min−1)
dHR/dt (beats min−2)
HRmin (beats · min−1)
Means are given for columns where no differences between conditions were observed. Reported data (n= 13, means ±s.d.) are for: heart rate at point of face immersion (HRrest); magnitude of heart rate elevation after immersion (ΔHRpeak); time to peak heart rate elevation (tHRpeak); rate of subsequent heart rate decline to HRmin (dHR/dt); and minimum heart rate reached during apnoea (HRmin). In comparison with the AIR control condition, *P≤ 0.05, **P≤ 0.01 and †P≤ 0.001; n.a., not applicable, in that if significant differences were evident it was not appropriate to calculate a mean across conditions.
72 ± 9
11 ± 7**
11.3 ± 2.8
−90 ± 28†
55 ± 6*
74 ± 8
7 ± 5
10.2 ± 4.0
−58 ± 24†
54 ± 9**
73 ± 8
7 ± 6
10.8 ± 3.5
−54 ± 25†
55 ± 9**
73 ± 10
8 ± 6
11.4 ± 4.4
−50 ± 22*
58 ± 11*
71 ± 8
5 ± 6
9.8 ± 6.8
−31 ± 15
61 ± 11
73 ± 9
10.8 ± 4.4
Cutaneous blood cell velocity During apnoea with face immersion, there was a significant main effect of immersion condition upon ΔCBVfoot (F= 3.2, P= 0.02) and ΔCBVcalf (F= 2.8, P= 0.04). The main effect for ΔCBVfoot was explained by significantly greater decreases in CBV under the 0°C (P= 0.003), 10°C (P= 0.001), 20°C (P= 0.012) and 33°C (P= 0.010) immersion conditions in comparison with AIR (Fig. 3, top panel). Likewise, for ΔCBVcalf significantly greater decreases were observed under the 0°C (P= 0.001), 10°C (P= 0.006), 20°C (P= 0.030) and 33°C (P= 0.004) immersion conditions in comparison with AIR (Fig. 3, bottom panel).
Haemoglobin oxygen saturation No significant main effect of immersion condition during apnoea was observed for (F= 0.4, P= 0.83). The mean rate of haemoglobin oxygen desaturation due to apnoea was 5.0% min−1 (s.d. 3.6% min−1) across all immersion conditions.
Study 2: non-apnoeic face immersion
Ventilation and oxygen consumption Mean values for all ventilation variables under each immersion condition for non-apnoeic face immersion are given in Table 2. There was a significant main effect of immersion condition upon (F= 6.8, P= 0.013) that was accounted for by a significantly greater peak in ventilation during face immersion at 0°C (P= 0.039) in comparison with 33°C (Fig. 4A). There was a significant main effect of immersion condition upon RERmax (F= 8.4, P= 0.007) that was explained by significantly greater peak respiratory exchange ratios during face immersion at 0°C (P= 0.025) and 10°C (P= 0.046) in comparison with 33°C. There was a significant main effect of immersion condition upon (F= 7.7, P= 0.009) that was explained by a significantly greater end-tidal oxygen partial pressure during face immersion at 0°C in comparison with 33°C (P= 0.032). There was a significant main effect of immersion condition (F= 8.4, P= 0.007) upon (Fig. 4B) that was explained by significantly lower values relative to 33°C during face immersion at 0°C (P= 0.033) with a trend evident at 10°C (P= 0.058). Simple linear correlations of the group means of ventilation and heart rate throughout immersion at 10 s intervals showed significant positive associations at 0 (r2= 0.95, P < 0.001), 10 (r2= 0.92, P= 0.001) and 33°C (r2= 0.94, P < 0.001). With the effect of removed, the ANCOVA showed a significant effect of immersion condition upon (F= 8.8, P= 0.003). Relative to 33°C, was significantly greater at both 0 (P= 0.002) and 10°C (P= 0.042; Fig. 5).
Table 2. Mean ventilation responses during breathing and face immersion in 0°C, 10°C and 33°C water over a 60 s period in the non-apnoea study 2
Reported data (n= 6, means ±s.d.) are for: peak values during 60 s face immersion of ventilation ( ), respiratory exchange ratio (RERmax) and end-tidal oxygen partial pressure ( ); and minimum values of end-tidal carbon dioxide partial pressure ( ). In comparison with 33°C, *P≤ 0.05.
31.6 ± 9.0*
1.40 ± 0.38*
15.81 ± 1.04*
4.06 ± 0.85*
23.7 ± 5.3
1.11 ± 0.14*
14.76 ± 1.02
4.65 ± 0.56
19.5 ± 4.8
0.94 ± 0.08
13.68 ± 0.56
5.38 ± 0.44
Non-apnoeic heart rate responses There was a significant main effect of immersion condition upon HRpeak (F= 11.2, P= 0.003) that was due to a significantly greater HR elevation after 10 s in 0°C (P= 0.011) in comparison with 33°C water (Fig. 4C). There was also a significant main effect of immersion condition upon HRmin (F= 26.9, P < 0.001) with a greater HR depression after 60 s during face immersion at 0 (P= 0.002) and 10°C (P= 0.021) in comparison with that in 33°C water (Fig. 4C).
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.
After accounting for the variation in resulting from changes in , a significantly greater was still observed during non-apnoeic face immersion (study 2). It could be argued that the use of as a covariate for during the non-steady-state initial response to face immersion may be confounded by a non-equilibrium between the gases in the alveolar space and the mouth, where gases were sampled. However, the high and significant positive correlations found between and HR throughout immersion in all three conditions suggested that the response reflected metabolic changes and that it could be employed as a covariate in the ANCOVA to separate the metabolic and temperature influences on .
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.
This research was sponsored by the Canadian Institutes of Health Research (SafetyNet Project 3a – Surface Exposure to Cold) and Natural Sciences and Engineering Research Council of Canada. The infrastructure for this study was provided by a Canadian Foundation for Innovation New Opportunities Grant.