Physiological and Psychological Effects of Escape ... - IngentaConnect

RESEARCH ARTICLE

Physiological and Psychological Effects of Escape from a Sunken Submarine on Shore and at Sea Marion Trousselard, Corinne Cian, Pierre-Alain Barraud, Ouamar Ferhani, Alain Roux, Damien Claverie, Frederic Canini, and Patrice Baert TROUSSELARD M, CIAN C, BARRAUD P-A, FERHANI O, ROUX A, CLAVERIE D, CANINI F, BAERT P. Physiological and psychological effects of escape from a sunken submarine on shore and at sea. Aviat Space Environ Med 2009; 80:850–6. Introduction: The stress effects induced by diverse military scenarios are usually studied under tightly controlled conditions, while only limited research has addressed realistic scenarios. This study was designed to compare the effects of two levels of realism in stressful training for escape from a sunken submarine. Methods: Thirteen qualified submariners served as subjects. All had previously participated in underwater escape training using a simulated submarine in a land-based tank submerged at a depth of 6 m; for this study, they repeated the simulator escape, following which six of them executed escape from an actual submarine lying at a depth of 30 m on the sea floor. The men were studied before the exercises, immediately after surfacing, and 2 h later. Measured variables included sympathovagal balance, salivary cortisol, perceived mood, and sleep, as well as short-term and declarative memory. Results: Compared to the simulator exercise in the tank, the escape at sea showed the following significant differences: 1) higher salivary cortisol values (6.33 6 3.9 nmol z L21 on shore and 13.38 67.5 nmol z L21 at sea); 2) greater adverse changes in mood, including vigor, tension, and ability to fall asleep; and 3) impairment in declarative memory. Responses were found to differ further for the five submariners who had prior experience of accident or injury while at sea. Conclusion: The psychophysiological and cognitive effects of military exercises may be influenced by the realism of conditions and by prior exposure to life-threatening situations. Keywords: submarine, acute stress reaction, life-threatening event.

T

HE RESPONSE TO acute stress involves allostasis, the process of achieving homeostasis through physiological and behavioral changes caused by perceived demand (15). The main physiological response involves the autonomic nervous system (ANS), which controls the release of adrenalin from the sympathetic-adrenal-medullary system, and the hypothalamo-pituitary-adrenal (HPA) axis, which produces cortisol. Stress is thought of as adaptive, since it promotes emergency coping under physical threat (fight or flight response). However, some data highlight its negative influence on cognition (10,13). While it is unclear which aspects of cognition could be impaired by an acute stressor and to what extent, an enhanced stress reaction has been associated with impairments in declarative memory and preserved short-term memory (13). Exposures to acute stress are inevitable components of military life. Therefore, studies in the military context are of considerable interest to researchers investigating stress mechanisms. Over the years, stress responses and cognitive degradation during diverse military contexts 850

have largely been documented using scenarios designed to simulate stressful situations (10). These studies activated biological stress reactions sometimes at intense levels. However, their simulation conditions made them unable to mimic the stress reactions, and even the trauma, as observed in real life. Studies comparing stress reactions in cases of naturalistic and simulated stressor conditions may prove valuable for further understanding of stress reactions. Moreover, experience of life-threatening events in the course of a lifetime may strongly influence the perceived stress. This was mainly investigated in the case of posttraumatic stress disorder (8,17). Unfortunately, for nonclinical individuals, data on the relationship between prior life-threatening or traumatic experiences and psychobiological and cognitive stress-responses are also scarce. The present study was, therefore, initiated to compare: 1) military training under simulated threatening circumstances and under realistic conditions; and 2) subjects’ psychobiological reactions in both situations according to their history. The experiment was based on an exercise for escaping from a submarine simulator submerged in a tank (Sim) and an escape from a sunken submarine at sea (Sub). It was expected that the stress reactions induced by the Sim condition would be further increased in the Sub condition. Stress reactions from stressor exposure were evaluated using physiological (i.e., cortisol level, sympathetic activation) and behavioral (i.e., cognitive and emotional performances) markers at various times. The second aim was achieved using a self-report of subjects’ exposure to previous incidents or accidents in past submarine missions and to compare psychophysiological stress reactions according to the subjects’ stress histories. It was hypothesized that indi-

From the Centre de Recherches du Service de Santé des Armées, Département des Facteurs Humains, La Tronche Cedex, France. This manuscript was received for review in January 2009. It was accepted for publication in July 2009. Address reprint requests to: Christian Raphel, 88 impasse Olympe de Gouges, 38920 Crolles, France; Christian.raphel@wanadoo.fr. Reprint & Copyright © by the Aerospace Medical Association, Alexandria, VA. DOI: 10.3357/ASEM.2503.2009

Aviation, Space, and Environmental Medicine x Vol. 80, No. 10 x October 2009

SUNKEN SUBMARINE ESCAPE EFFECTS—TROUSSELARD ET AL. viduals with a submarine stress history would perceive an escape situation as more threatening and consequently exhibit higher stress responses and lower cognitive performances than stress-free individuals.

assessed at three times: immediately before the escape exercise (Baseline); 30 min after the escape exercise (Escape); and 2 h after the escape exercise (Recovery). Both conditions were supervised by the research team so that assessments were controlled at each step of the protocol.

METHODS Subjects

Physiological Assessment: Cardiac Vagal Tone

Thirteen healthy men (mean age 30.8 yr, SD 4.6) were recruited via opportunity sampling from submarine crews attending simulated submarine escape training at the French Training Institute to Submariner Safety in Brest. They had served 10.7 6 5.2 yr on active duty. Their educational background varied from 1 yr (i.e., submarine school) to 4 yr (i.e., more specialized technical courses). They had submarine simulator training experience (number of training sessions: 3 6 1.5), but had no experience of an escape from a sunken submarine at sea. Among these individuals, five reported accidents in the past: two submariners were involved in a collision during a mission and the three others reported open fractures or large cuts due to steering errors. The individuals with exposure to a stress event (History, H) did not differ from the others (No History, NH) in terms of age, educational background, and escape training experience. The H individuals had had no escape training practice since their accidents. All volunteer individuals gave written informed consent before participation. The study was approved by the ethics committee of the French Military Health Service.

Cardiac vagal tone was evaluated from electrocardiogram (ECG) recorded using a portable recorder (Vitaport CPS, Temec, Kerkrade, Netherlands) during each experimental step. It was digitized with a 1000-Hz sampling rate to accurately detect R-wave peaks. The ECG trace and the detection marks were displayed together to be checked. All the ECG data were free from arrhythmia and artifact, except five cases of singular premature heart beats. The time series of interbeat intervals was generated and the spectral analysis of heart rate variability (HRV) was then carried out using the Fast Fourier Transform algorithm (11). The HRV spectral analysis focused on low- (LF, , 0.1 HZ) and high-frequency (HF, . 0.15 Hz) bands. The LF rhythm contains both sympathetic and parasympathetic contributions, whereas the HF rhythm primarily reflects vagal efferent tonus. According to published recommendations (5), HRV was quantified by LF/HF ratio, assumed to reflect the cardiac sympathovagal balance. A shift of sympathovagal balance toward parasympathetic dominance produces a decreased LF/HF ratio, whereas a shift of sympathovagal balance toward sympathetic dominance produces an increase of LF/HF ratio.

Operational and Experimental Procedures In October 2007, the submarine headquarters based at Brest organized the escape training in the submarine simulator submerged in a tank at 6 m (Sim). The escape exercise was performed in November 2007 from the French attack nuclear submarine SNA Emeraude, which was submerged at a depth of 30 m in the Mediterranean Sea (Sub). Although the generic procedures for escaping were similar between the Sim and the Sub conditions, they differed in technical abilities and in risks of decompression accidents. In both conditions, the escape rate was one submariner every 20 min to be as close as possible to what would be done in case of real emergency in a sunken submarine. In the Sub condition, after escape the submariners were picked up by a lifeboat and transported within 20 min to the medical ship to be examined. Although all subjects escaped from the simulator, only six of them escaped from the submarine due to naval technical reasons. The training procedure consisted of one theoretical training session following by two escape conditions. The first one took place in the submarine airlock simulator (Sim) and the second one in the sunken submarine (Sub). Both escape sessions were carried out between 1530 and 1800 in order to control circadian variation. The experimental procedure was the same for the two escape sessions. A 12-h overnight urine sample was collected the night before the escape exercise and mood and sleep questionnaires were completed in the morning. Physiological, endocrine, and cognitive performances were then

Endocrine Assessments Salivary cortisol, a reliable marker used for HPA axis activity (13), was sampled at the Baseline, Escape, and Recovery steps leading to 39 samples from the 13 subjects involved in the Sim and 18 samples from the 6 subjects involved in the Sub escape. Each 5-ml saliva sample was collected in Salivettew tubes according to the specifications of the provider (Sarstedt, Inc., Newton, NC). Eating, drinking, and smoking were not permitted 2 h before each collection. Once filled, the tubes were centrifuged, sampled into 1.5-ml aliquots, and stored at 280°C until analysis. Two samples from Sub condition were discarded due to too little saliva. The nocturnal urinary free cortisol excretion was assessed as a marker of anticipatory anxiety. The subjects were instructed to collect urine from 1800 to 0600. Once retrieved, urine volume was measured and a 2-ml sample was taken, and then stored at 280°C until further analysis. Cortisol concentrations were measured using radioimmunoassay kits according to the protein concentration rates (Siemens Healthcare Diagnostics, Nuremberg, Germany). The urinary cortisol excretion rates were calculated according to the diuresis and the creatinine excretion rates. Mood and Sleep Questionnaires A computerized subjective sleep questionnaire (2) was used to evaluate the quality of the subjects’ sleep


851

SUNKEN SUBMARINE ESCAPE EFFECTS—TROUSSELARD ET AL. during the night before each session. It consisted of two items (i.e., restoration quality and ability to fall asleep) featured by visual analog scales from “2”on the left to “1” on the right. The subjects “hooked” a visual pointer on a sliding scale using the mouse and dragged the pointer to the appropriate location on the scale (12 cm long). Mood was evaluated at the beginning of both sessions using a computerized abbreviated version (5-min) of the Profile of Mood States (POMS) (16). It consisted of an adjective checklist of 37 items rated on a 5-point scale that ranged from 1, “not at all,” to 5, “extremely.” The subjects were asked to answer according to their present mood. Six factors were then calculated: anxiety-tension, depression-dejection, anger-hostility, fatigue-inertia, vigor-activity, and confusion-bewilderment. Cognitive Test Battery The cognitive test battery was designed to be completed in less than 15 min, the temporal window allowed by the exercises. It included the following, in order: 1) Declarative memory, which was tested using a set of 12 pictures shown during 10 s at the beginning of the test battery. The free recall with false recall (recall of pictures outside of the set) and recognition (recognition of pictures of the set among 24 pictures) was assessed 15 min later. A new set of pictures was presented at each time of assessment. 2) Short-term memory was studied using the 10-min Digit span test. A set of numerical digit strings, composed of 4 to 8 digits, was presented for learning to the subjects. Each string was presented during 1 s with a 0.5-s interval between two consecutive strings. The subjects’ task was to memorize the complete string of digits and to recall it by clicking using the mouse on the appropriate digits on a visual keypad displayed on the monitor. Recall was required either in the same or the reverse order of presentation. The number and the mean reaction time of correct retrievals were considered.

RESULTS Physiological Assessment For the Sim condition, as for the Sub condition, no significant difference was observed on LF/HF among the three steps (Fig. 1). No significant difference was observed between conditions for each time-point. Three Pearson correlations addressed the relationship between LF/HF values in the Sim and Sub conditions for Baseline (4.01 6 2.19 for Sim and 3.87 6 4.34 for Sub), Escape (4.42 6 2.74 for Sim and 7.91 6 9.93 for Sub), and Recovery (2.77 6 2.12 for Sim and 4.23 6 5.22 for Sub). Correlations were found to be statistically significant for Baseline (r5 5 0.84; P , 0.05) and Escape (r5 5 0.77; P , 0.05), but not for Recovery (r5 5 0.14; P . 0.05). This indicates that for Baseline and Escape, respectively, the LF/HF values in the Sim and Sub conditions are positively related and that for Recovery the LF/HF values in Sim and Sub are not related. Endocrine Assessments The nocturnal cortisol excretion rates did not differ between the Sim and Sub conditions. In the Sim condition, salivary cortisol concentrations decreased steadily [Time effect, F(2,12) 5 6.50, P , 0.05; Fig. 2] with higher Baseline values (7.87 6 4.19 nmol z L21) compared to Sub (6.33 6 3.91 nmol z L21; P , 0.05) and Recovery (3.22 6 1.57 nmol z L21; P , 0.05) and higher Escape values compared to Recovery (P , 0.01). Three separate Pearson correlations addressed the relationship between time points. A correlation between Escape and Recovery was found to be statistically significant (r12 5 0.81, P 5 0.05) while the correlations between Baseline and Escape and Baseline and Recovery were found statistically nonsignificant (r12 5 0.51, P 5 0.06, and r12 5 0.48, P 5 0.07, respectively). Whether or not subjects with higher cortisol concentrations after the escape were prone to higher

Data Analysis and Statistical Methods Statistical analysis was performed using the SPSS 11.0 software package (SPSS Inc., Chicago, IL). Physiological, endocrine, and cognitive data time courses (Baseline, Escape, and Recovery) were studied within each experimental condition using repeated-measure analyses of variance (ANOVA). If necessary, post hoc analyses were carried out using Newman-Keuls tests. Relationships among physiological, endocrine, and cognitive responses were studied using Pearson’s correlation test. Comparisons between conditions (Sim vs. Sub) were done on the subsample of six submariners who participated in the two escape sessions. Paired t-tests were used separately on each experimental step. Comparisons between subjects according to their history of submarine accidents (H vs. NH) were carried out using independent t-tests. Because there were too few subjects for the Sub condition, it was done only in the Sim condition. Statistical significance was set at P , 0.05. Results were expressed as mean and SD. 852

Fig. 1. Mean (SD) LF/HF according to the measurement times in military men during each of the escape conditions (Sim and Sub). LF and HF indicate low frequency and high frequency, respectively.


SUNKEN SUBMARINE ESCAPE EFFECTS—TROUSSELARD ET AL. ship between cortisol concentration during the Sim and Sub for Baseline, Escape, and Recovery. No correlation was found between conditions, whatever the considered experimental step (r5 5 20.30, P 5 0.55 for Baseline; r5 5 0.68; P 5 0.13 for Escape; r5 5 0.66, P , 0.15 for Recovery). Sleep and Mood Questionnaires The nights before the escape exercises, subjects showed an increase in ability to fall sleep [t(5) 5 2.23, P 5 0.05] before the Sim as compared to the Sub (10.34 6 0.87 cm and 8.1 6 3.72 cm, respectively). Compared to Sub, the Sim condition induced a higher activity-vigor factor [Sim: 15.14 6 3.71, Sub: 13.00 6 2.58; t(5) 5 2.04, P , 0.001] and a lower anxiety-tension factor [Sim: 0.57 6 1.51, Sub: 2.14 6 1.34; t(5) 5 22.66, P , 0.05]. Cognitive Test Battery Fig. 2. Mean (SD) salivary cortisol concentrations according to the measurement times in military men during each of the escape conditions (Sim and Sub). * P , 0.05 for mean difference in salivary cortisol at escape time.

cortisol concentrations at Recovery, cortisol concentration at Baseline was not related to cortisol concentration at Escape and Recovery. When regarding the relationship among physiological and endocrine responses for each time point separately, no correlation was observed between cortisol and LF/HF values in either step (r12 5 20.14, P 5 0.64 for Baseline; r12 5 20.14, P 5 0.63 for Escape; r12 5 0.11, P 5 0.73 for Recovery). In the Sub condition, salivary cortisol increased during Escape [time effect, F(2,5)515.32, P , 0.01] with higher Escape cortisol values (13.83 6 7.56 nmol z L21) compared to Baseline (6.19 6 3.10 nmol z L21, P , 0.01) and Recovery (4.25 6 2.59 nmol z L21, P , 0.01). The three separate Pearson correlations performed to address the relationship among endocrine responses between time points were found to be statistically significant (r5 5 0.84, P 5 0.03 between Baseline and Escape; r5 5 0.75, P 5 0.05 between Baseline and Recovery; r5 5 0.89, P 5 0.01 between Escape and Recovery). This indicates that subjects with higher cortisol concentration at Baseline exhibited higher cortisol concentration after the escape and at Recovery. Three separate Pearson correlations addressed the relationship between the physiological and endocrine responses for each time point. Correlations were found to be statistically significant for Escape (r5 5 0.98, P , 0.001) and Recovery (r5 5 0.89, P 5 0.01), but not for Baseline (r5 5 20.01, P 5 0.98). This indicates that subjects prone to higher cortisol concentration at Escape and Recovery are prone to higher LF/HF value while cortisol concentration and LF/HF are not related at Baseline. Comparisons between conditions only revealed that salivary cortisol level was higher in the Exercise condition for Escape [t(5)53.04, P , 0.05 with 13.38 6 7.51 nmol z L21 for Exercise and 6.33 6 3.93 nmol z L21 for Sim]. Three Pearson correlations addressed the relation-

Considering picture recall, no difference was observed among experimental steps, whatever the condition. When comparing conditions, subjects had significantly worse recall of pictures during Escape in the Sub vs. Sim conditions [Sim: 9.33 6 1.41, Sub: 7.50 6 2.44; t(5)53.37, P , 0.001]. No difference between conditions was found in any of the experimental steps in recognition and false recall performances. Considering the digit-span test, a significant timeeffect [F(2, 11) 5 5.01, P , 0.05] was observed during Sim for the number of correct retrievals in the case of reverse order of presentation: Escape (6.16 6 1.89) and Recovery (6.02 6 1.86) were higher than Baseline (5.03 61.76, P , 0.05 for the two steps). The same was observed for Exercise [F(2,5) 5 4.64, P , 0.05], with Escape (6.01 6 1.33) and Recovery (6.33 6 1.14) higher than Baseline (4.92 6 1.43, P , 0.05 for the two steps). In both conditions, no difference among experimental steps was observed for the direct order task. No difference between conditions was observed for any of the experimental steps. Effects of History of a Submarine Accident Because there were too few subjects for the Sub condition, this analysis was carried out only in the Sim condition (Fig. 3). Considering LF/HF, H subjects had higher values than NH subjects at Recovery [t(11)53.32, P , 0.001 with 7.02 6 2.31 for H and 4.73 6 2.63 for NH]. Within each history group, three Pearson correlations addressed the relationship between time points for LF/HF values. For the H group, correlations were found to be statistically significant (r4 5 0.98, P , 0.001 between Baseline and Escape; r4 5 0.92, P 5 0.02 between Baseline and Recovery; r5 5 0. 90, P 5 0.03 between Escape and Recovery). This indicates that subjects with higher LF/HF values at Baseline exhibited higher LF/HF values after the Escape and at Recovery. For the NH group, correlations were found to be non-significant (r7 5 0.36, P 5 0.36 between Baseline and Escape; r7 5 20.12, P 5 0.77 between Baseline and Recovery; r7 5 0.26, P 5 0.53 between Escape and Recovery), indicating that LF/HF value between time points were not related.


853

SUNKEN SUBMARINE ESCAPE EFFECTS—TROUSSELARD ET AL. nmol z L21 for H and 6.42 6 4.31 nmol z L21 for NH], and Recovery [t(11) 5 4.10, P , 0.001 with 4.81 6 6.90 nmol z L21 for H and 1.81 6 3.12 nmol z L21 for NH]. Within each history group, three Pearson correlations addressed the relationship between time points for cortisol levels. For the H group, correlations were found to be statistically significant (r4 5 0.69, P 5 0.05 between Baseline and Escape; r4 5 0.90, P , 0.01 between Baseline and Recovery; r5 5 0.62, P 5 0.05 between Escape and Recovery). This indicates that subjects with higher cortisol levels at Baseline exhibit higher cortisol levels after the Escape and higher cortisol levels at Recovery. For the NH group, correlations were found to be non-significant (r7 5 0.35, P 5 0.56 between Baseline and Escape; r7 5 0.26, P 5 0.66 between Baseline and Recovery; r7 5 0.39, P 5 0.51 between Escape and Recovery), indicating that cortisol level between time points are not related. Within both history groups, three separate Pearson correlations addressed the relationship between the physiological and endocrine responses for each time point. No correlation was found to be statistically significant, whatever the group (Baseline: r4 5 20.14, P 5 0.82 for H and r7 5 20.01, P 5 0.99 for NH; Escape: r4 5 20.26, P 5 0.66 for H and r7 5 0.29, P 5 0.48 for NH; Recovery: r4 5 0.44, P 5 0.45 for H and r7 5 20.17, P 5 0.67 for NH). Whatever the group, cortisol concentration and LF/HF are not related at each time point. The night before the simulation, the ability to fall sleep was lower in H subjects as compared to NH subjects [t(11) 5 2.68, P , 0.05 with 4.82 6 0.89 cm for H and 11.91 6 0.52 cm for NH]. Sleep restoration quality was also lower in H subjects as compared to NH subjects [t(11) 5 1.79, P 5 0.05 with 7.52 6 1.91 cm for H and 10.80 6 1.51 cm for NH]. No difference in nocturnal cortisol rates and POMS scoring was noticed between groups. Regarding the picture test performances, H subjects had higher false recall at Escape than NH subjects [t(11) 5 2.12, P 5 0.05 with 0.42 6 0.89 false recall for H and 0 for NH]. No difference in digit-span test was observed between history groups. DISCUSSION

Fig. 3. Effects of history of submarine accidents (H vs. NH) on different assessments according to the times of the escape training. * P , 0.05 for mean differences in responses between the two groups.

H subjects also had higher salivary cortisol levels than NH subjects at Baseline [t(11) 5 2.07, P , 0.05 with 9.91 6 6.41 nmol z L21 for H and 5.83 6 4.11 nmol z L21 for NH], Escape [t(11) 5 1.82, P , 0.05 with 11.30 6 7.22 854

The present study compared the physiological and behavioral responses induced by military escape training from a submarine simulator to a realistic at-sea condition. For the two escape conditions, mood and sleep perception were evaluated before the Escape and sympathovagal balance (LF/HF ratio), cortisol salivary levels, and short-term and declarative memories were assessed before (Baseline), 30 min after (Escape), and 2 h after (Recovery) the escape exercises. The sympathovagal response first did not differ between the two conditions, Sim and Sub. However, an individual pattern of ANS activation may exist as suggested by the positive correlations observed for the sympathovagal responses between conditions during Baseline and Escape steps. The ranking of subjects for ANS activation was not modified by the conditions, suggesting that during exposure to the escapes, similar


SUNKEN SUBMARINE ESCAPE EFFECTS—TROUSSELARD ET AL. processes lie beneath the sympathovagal responses for a subject. For the Recovery step, however, ANS activation recovery after the Sim escape training failed to predict ANS activation recovery after the Sub escape. Individual differences due to the context of escaping modified the time course of ANS activation. ANS recovery may be a critical issue because failing to shut down ANS activation after a stress event could have deleterious effects on health (12). ANS activation particularly depends on the vagal tone, which is considered an important individual adjustment parameter for recovery after exposure to acute stress (12). Healthy physiology and resilient adaptive style are expressed by high levels of vagal adaptive variability (12). Whether those subjects prone to faster vagal-induced recovery after Exercise were more resilient is a subject for further investigation. Although subjects exhibited similar HPA axis activation before the two escape exercises (there was no difference in the nocturnal cortisol excretion rates, or in the baseline salivary cortisol levels between the two escape exercises), the two escape conditions differed in the endocrine responses as shown by the salivary cortisol patterns. The steady decrease of salivary cortisol concentrations during Simulation is congruent with what is observed prior to public speaking or prior to a first jump for novice parachutists (7). This pattern is highly evocative for an anticipation of threat, which disappears with the beginning of action. Conversely, salivary cortisol values increased during exposure to the Escape under realistic (Sub) conditions and returned to baseline 2 h after escaping. This HPA activation time course is not surprising as cortisol levels increase 20-40 min after exposure to military stress (10,13). This further cortisol increase suggests that the submarine escape was a stressor. This is supported by the fact that subjects with higher cortisol values also exhibited an increased shift of the sympathovagal balance toward sympathetic dominance (higher LF/HF values). A similar relationship was observed between ANS and HPA activations 2 h after escaping. These results suggest that the Sub condition induced a higher allostatic load than the Sim condition and that it disappeared 2 h after escape. Accordingly, subjects also exhibited: 1) a decreased activity-vigor with an increased anxiety-tension in POMS; and 2) a disturbed ability to fall sleep before the Sub as compare to the Sim condition. Such a difference between conditions could be explained by a judgment of the task being uncontrollable for the submarine escape, as suggested by Dickerson and Kemeny (3). Another explanation based on a social-evaluative threat due to headquarters’ focus for the Sub condition could also be taken into account (3). The impact of the two stress conditions on cognitive functions differed according to the assessed performances. The pattern of performance for short-term memory for the direct order task did not differ between the two conditions. The same was observed for the reverse order task with a particular time pattern, with the lower performance being observed for Baseline as compared to Escape and Recovery. During the time preced-

ing escaping, submariners had to switch from “remember the procedures for the imminent escape” to “remember the short-term memory task.” According to the cognitive load theory (14), the process by which information is maintained or stored in the brain for briefs periods of time is limited by the amount of resources available when the information is being processed. At Baseline, the resources may not be available due to the reverse order task, known to induce a higher cognitive load compared to the more automated order task. Conversely, there was no additive operational task during Escape and Recovery, explaining the lesser amount of impairment in the “reverse order” task. Regarding declarative memory, recall ability was reduced after escaping in the Sub condition. This cognitive degradation was concomitant with the salivary cortisol increase. Furthermore, it disappeared 2 h afterward in parallel with the decrease in cortisol level. It could be suggested that the mechanisms underpinning such results involve stress through cortisol elevation. Indeed, glucocorticoids have been shown to influence multiple regions of the brain as implied in the memory processes (1,9,13), with the hippocampus being involved in declarative memory (recall ability) and the prefrontal cortex in short-term memory (reverse order task alteration). Lastly, our results highlighted that individuals with a history (H) of prior exposure to submarine accidents exhibited a higher stress response than individuals without any history (NH). Indeed, the former exhibited higher cortisol levels and a decreased ability to fall sleep compared with the latter. This is an important problem since the prevalence of having experienced a submarine threatening event was 38.4% in the study population, which is slightly out of the range of 40–90% found in previous studies (6). Interestingly, the escape training elicited a range of patterned endocrine and autonomic responses for subjects already exposed to a submarine accident. This supports the premise that there could be stressor-specific pathways to activation when re-exposure to a prior stressor occurs. From a mechanistic point of view, these results could be viewed as a function of a sensitization process, known to facilitate further evoked responses. It is caused by both an increased arousal in the central nervous system and the stress-induced cortisol increase (1,9,15). This hypothesis is supported by our results showing an enhanced stress reaction and the higher acute stress reaction levels also observed in a surviving naval crew compared to a normative male sample (4). Although the present study had important limitations, i.e., the small size and highly selected sample of subjects, it highlights the role of the history of a subject in the physiological and behavioral responses induced by a military stress exposure. ACKNOWLEDGMENTS This study is part of an ongoing project on military psychology supported by the French ‘Service de Santé des Armées’. We would like to acknowledge the submariners implied in this research, the Naval Force headquarters, and A. Job for their technical contributions to this study.


855

SUNKEN SUBMARINE ESCAPE EFFECTS—TROUSSELARD ET AL. Authors and afﬁliations: Marion Trousselard, Dr., Ph.D., Corinne Cian, Ph.D., Pierre-Alain Barraud, engineer, Ouamar Ferhani, Ph.D., Alain Roux, technician, Damien Claverie, Dr., and Frederic Canini, Dr., Ph.D., Centre de Recherches du Service de Santé des Armées, Département des Facteurs Humains, La Tronche Cedex, France; and Patrice Baert, Dr., ESNLE, SNLE le terrible, équipage bleu, Centre Roland Morillot, France.

REFERENCES 1. Aggleton JP, Brown MW. Episodic memory, amnesia and the hippocampal-anterior thalamic axis. Behav Brain Sci 1999; 22:425–44. 2. Bogui P, Keita M, Dah C, Fidier N, Buguet-Brown ML, Buguet A. [The sleep of Africans and Europeans in the Ivory Coast: questionnaire study.] [In French.] Sante 2002; 12:263–70. 3. Dickerson SS, Kemeny ME. Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychol Bull 2004; 130:355–91. 4. Eid J, Jonhsen BH, Thayer JF. Post-traumatic stress symptoms following shipwreck of a Norwegian Navy frigate – an early follow-up. Personality and Individual Differences 2001; 30: 1283–95. 5. Heart rate variability: standards of measurement, physiological interpretation, and clinical use. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Circulation 1996; 93:1043–65. 6. Hidalgo RB, Davidson JR. Posttraumatic stress disorder: epidemiology and health related consideration. J Clin Psychiatry 2000; 61(7)5–13.

856

7. Lupien SJ, McEwen BS. The acute effects of corticosteroids on cognition: integration of animal and human models studies. Brain Res Brain Res Rev 1997; 24:1–27. 8. Mageroy N, Riise T, Johnson BH, Moen BE. Coping with lifethreatening events was associated with better self-perceived health in a naval cross-sectional study. J Psychosom Res 2008; 65:611–8. 9. McEwen BS, de Kloet ER, Rostene W. Adrenal steroid receptors and actions in the nervous system. Physiol Rev 1986; 66:1121–88. 10. Morgan III CA, Wang S, Mason J, Southwick SM, Fox P, et al. Hormones profiles in humans experiencing military survival training. Biol Psychiatry 2000; 47:891–901. 11. Niskanen JP, Tarvainen MP, Ranta-Aho PO, Karjalainen PA. Software for advanced HRV analysis. Comput Methods Programs Biomed 2004; 76:73–81. 12. Porges SW. Cardiac vagal tone: a physiological index of stress. Neurosci Biobehav Rev 1995; 19:225–33. 13. Robinson SJ, Sünram-Lea SI, Leach J, Owen-Lynch PJ. The effects of exposure to an acute naturalistic stressor on working memory, state anxiety and salivary cortisol concentrations. Stress 2008; 11:115–24. 14. Sweller J. Cognitive load theory, learning difficulty and instructional design. Learning and Instruction 1994; 4:295–312. 15. Sterling P, Eyer J. Allostasis: a new paradigm to explain arousal pathology. In: Fisher S, Reason J, eds. Handbook of life stress, cognition, and health. New York: John Wiley & Sons; 1988:629– 49. 16. Shacham S. A shortened version of profile of mood states. J Pers Assess 1983; 47:305–6. 17. Van der Kolk BA. Trauma and memory. Encyclopedia of Stress. Amsterdam: Elsevier (Academic Press); 2007:765–7.
