Effect of repeated exposures to cold on cognitive performance in humans

Transcription

1 Physiology & Behavior 87 (2006) Effect of repeated exposures to cold on cognitive performance in humans Tiina M. Mäkinen a, *, Lawrence A. Palinkas b, Dennis L. Reeves c, Tiina Pääkkönen d, Hannu Rintamäki d,e, Juhani Leppäluoto d, Juhani Hassi a a Centre for Arctic Medicine, Thule Institute, University of Oulu, P.O. Box 5000, FIN-90014, Finland b School of Social Work, University of Southern California, Los Angeles, CA, USA c Clinvest Inc., USA d Department of Physiology, University of Oulu, Finland e Oulu Regional Institute of Occupational Health, Finland Received 22 June 2005; received in revised form 30 August 2005; accepted 27 September 2005 Abstract The effects of repeated exposure to cold temperature on cognitive performance were examined in 10 male subjects who were exposed to control (25 -C) and cold (10 -C) conditions on 10 successive days. A cognitive test battery (ANAM-ICE) was administered each day to assess complex and simple cognitive functioning accuracy, efficiency and response time. Rectal (T rect ) and skin temperatures, thermal sensations, metabolic rate (M) and cardiovascular reactivity were also recorded. With the used cold exposure, inducing cold sensations and discomfort, superficial skin cooling (6 7 -C) and a slightly lowered T rect (0.4 -C) we observed three distinct patterns of cognitive performance: 1) negative, reflected in increased response times and decreased accuracy and efficiency; 2) positive, reflected in decreased response time and increased efficiency; and 3) mixed, reflected in a pattern of increases in both accuracy and response time and decreases in efficiency, and a pattern of decreases in both accuracy and response time. T rect, thermal sensations, diastolic blood pressure (DBP) and heart rate (HR) were independent predictors of decreased accuracy, but also decreased response time. Cognitive performance efficiency was significantly improved and response times shorter over the 10-d period both under control and cold exposures suggesting a learning effect. However, the changes in cognitive performance over the 10-d period did not differ markedly between control and cold, indicating that the changes in the thermal responses did not improve performance. The results suggest that cold affects cognitive performance negatively through the mechanisms of distraction and both positively and negatively through the mechanism of arousal. D 2005 Elsevier Inc. All rights reserved. Keywords: Cognition; Cold; Acclimation; Habituation; Thermoregulation; Human 1. Introduction Mental performance plays a crucial role in areas of orientation, safety, decision making, work productivity, and reactions in challenging situations. Exposure to cold environmental temperatures may significantly affect cognitive performance [1,2]. It is well known that a severe enough cold exposure, causing marked whole body cooling, results in impaired cognitive performance (amnesia, central nervous system (CNS) decrements, unconsciousness) [3]. However, even exposure to less severe cold, which does not lower core * Corresponding author. Tel.: ; fax: address: tiina.makinen@oulu.fi (T.M. Mäkinen). temperature markedly, may produce cognitive decrements with adverse performance and health-related consequences [1]. This type of cold stress is more likely to occur in everyday occupational or leisure time activities. Most of the effects documented to be related to cold temperatures have demonstrated an increased number of errors and changes in response times in the performance of cognitive performance tests assessing vigilance, reasoning and memory. A recent meta-analysis demonstrated that under cold conditions (at or below 10 -C) especially reasoning, learning and memory tasks were impaired [2]. Impairment of short-term memory has been reported in individuals, even with brief, apparently nonhypothermic, cold exposures [3 8]. For example, exposure to acute cold stress impairs performance on the matching to sample task that reflects the functioning of short-term or /$ - see front matter D 2005 Elsevier Inc. All rights reserved. doi: /j.physbeh

2 T.M. Mäkinen et al. / Physiology & Behavior 87 (2006) working memory [9 11]. Some studies have reported a significant decrement in memory recall but not in recognition [4], while others have reported a significant decrement in recognition but not in recall [12]. Similarly, inconsistent results of the effects of cold on reasoning skills (e.g., symbol processing, mental arithmetic) have been obtained. Some studies have reported significantly impaired reasoning [5,6], while others found no significant decrements, despite a decline in core body temperature [4]. The effect of non-hypothermic cold exposure on response times is also inconsistent. Several studies have demonstrated that response times during cognitive tasks are slowed when subjects are exposed to cold air or water [3,6,12 15]. In other studies an increased arousal, reflected as shortened evoked potential latencies and response times in cold, was observed [9,11,16,17]. However, although subjects produced faster responses to some stimuli in the cold, they were usually less accurate in these conditions. Other studies found little or no effect on reaction time under cold conditions [14]. In most of these investigations, the hypothesis has been that cold is associated with a decline in cognitive performance. However, evidence of improved performance under moderate cold conditions in certain cognitive tasks has also been demonstrated [18]. The few studies that have examined the effects of repeated exposures to cold temperatures found either no effect of cold exposure or that performance is attenuated in complex cognitive tasks, while simple tasks remain unaffected [9,12,13,17,19]. In these studies no specific emphasis was given on the changes in thermoregulation occurring during repeated cold exposures. It is known that repeated exposures to cold result in acclimation. Depending on the type and intensity of cold exposure the first acclimation responses (especially habituation of thermal sensations) may develop within a couple of days [20]. Examples of cold habituation responses are for example a reduced vasoconstriction and blood pressure, higher skin temperatures, delayed onset and reduced intensity of shivering, dampened release of circulating stress hormones and less intense sensations of cold and thermal discomfort [21,22]. A reduction in stress and discomfort may have a positive effect on cognitive performance due to a reduced amount of distraction. At present it is not known whether possible changes occurring in thermoregulation caused by repeated cold exposures are associated with cognitive performance. The aim of the present study was to determine the effect of non-hypothermic cold exposure on cognitive performance and assess its association with thermoregulation. We were specifically interested in examining the effects of moderate cold exposure on different types of cognitive tasks and on the performance strategy (accuracy, efficiency, reaction time) of each task. We also wished to test the hypothesis that repeated cold exposures stimulate acclimation responses, which could result in reduced stress and possibly increased cognitive performance over time. 2. Material and methods The tests were performed in Oulu, Northern Finland (65- N 25- E) in September October Ten young healthy men volunteered as test subjects. Their mean age was 22.5T1.6 (meantsd) years, height 180.8T7.2 cm, weight 72.4T7.3 kg, body mass index 22.3 T1.6, body fat % 17.1T1.9 and VO 2max 53.1T6.1 ml min 1 kg 1. The subjects were informed of the nature, purpose and possible risks/inconvenience caused by the experiment. A medical examination was conducted to confirm that they were healthy. A written consent to participate in the study was obtained before starting the experiments. The ethics committee of the University of Oulu and Northern Ostrobothnia Hospital District approved the experimental protocol. During the experiments the subjects were lightly clad in shorts, socks and athletic shoes. They performed the cognitive tests each day first under control conditions in a climatic room (13 m 2 ) in which temperature was adjusted to 25.0T0.3 -C. The duration of the stay in control conditions was 90 min of which the last 20 min were used to perform the cognitive tests. Immediately after this the same subjects were exposed to cold (10.0T0.3 -C) in another climatic room (27 m 2 ) for 120 min each day and the cognitive tests were performed in the cold after 100 min of exposure. In both of these climatic chambers the relative humidity was 50T3% and air velocity less than 0.2 m/s. The experiments were performed between 8:00 and 16:00 and started at the same time of the day for each subject. The experimental protocol is described in Fig Measured variables Skin temperatures were measured using thermistors (NTC DC 95, Digi Key, USA) from 10 sites: forehead, upper back, chest, abdomen, upper arm, lower arm, back of the hand, VO 2 Thermal sensations BP VO 2 Thermal sensations BP SUBJECTS 1-10 CONTROL (25 C) 90 min COLD (10 C) 120 min... x 10 consecutive days cognitive tests min T sk, Trect HR cognitive tests min T sk, T rect HR Fig. 1. Study design. Ten subjects performed the cognitive tests on 10 consecutive days at control (25 -C) and cold (10 -C) conditions.

3 168 T.M. Mäkinen et al. / Physiology & Behavior 87 (2006) anterior thigh, dorsal side of the foot and calf. Mean skin temperature (T sk ) was calculated from the 10 sites as an area weighed average [23]. In addition, finger skin temperature (T fing ) was measured from the dorsal side of the middle finger. Rectal temperature (T rect ) was measured 10 cm beyond the anal sphincter with a YSI401 probe (Yellow Springs Instrument Co.,Yellow Springs, USA). Skin and rectal temperature values were recorded at 1-min intervals with a datalogger (Smart- Reader 8+, ACR Systems, Canada). Means of the temperatures were calculated for the period when the subjects were performing the cognitive tests (duration 20 min). Thermal sensations for the whole body, trunk, hands and feet were assessed using a 9-degree subjective judgment scale [24], ranging from 4 (extremely hot) to 4 (extremely cold). Thermal comfort was assessed using a 5-degree scale ranging from 0 (comfortable) to 5 (extremely uncomfortable) [24]. The assessment was performed immediately after the subjects had completed the cognitive test after 120 min of cold exposure. Oxygen consumption (VO 2 ) was measured under control conditions (25 -C) and at 10 -C after being exposed to cold for 60 min. The subjects were sitting during the measurements. For determining VO 2, a portable analyzer (Cortex Biophysik, MetaMax 3B, Germany) employing a breath-by-breath system was used. The duration of each measurement was 10 min. The average from the last 5 min was used for the analyses. Heart rate (HR) was measured continuously throughout the experiments using a Polar Sport Tester monitoring device (Polar Electro Inc., Finland). Systolic (SBP) and diastolic (DBP) blood pressure was measured from sitting subjects immediately after completing the cognitive tests using an ambulatory blood pressure monitoring device (Meditech ABPM-04, Meditech Ltd., Hungary) Cognitive performance For assessing cognitive performance the Automated Neuropsychological Assessment Metric [25] for Isolated and Confined Environments (ANAM-ICE) version was administered. Subtests of the ANAM system have been designed to assess attention and concentration, mental flexibility, spatial processing, cognitive processing efficiency, mood, arousal/ fatigue level, and memory. The ANAM test program was translated into Finnish. The subjects were introduced to the test battery prior to the experiments. For each of the cognitive tests the percentage of accurate response, response times (RT) for the correct responses, and efficiency were determined. The efficiency, or throughput, is a measure which includes both speed and accuracy in one score. It is computed as the number of correct responses times 100 divided by response time. The duration for performing the ANAM test battery was 20.5T0.2 min and included the following tasks: Code substitution and code substitution delayed These ANAM tasks are derived from the WAIS-R, Digit Symbol, and Symbol Digit Modalities Test [26] and designed to measure ability for sustained attention and concentration, verbal learning, and numeric and symbolic facility. In the code substitution task, strings of 9 symbols and 9 digits are displayed across the upper portion of the screen and arranged so that the digit string is immediately below the symbol string. There is one digit corresponding to each symbol. During a test a test pair (symbol and digit) is presented at the bottom of the screen, below the coding strings. The objective is to indicate if the test pair matches the associated pair in the coding strings at the top of the screen, below the coding strings. After the learning trial, an associative recognition memory trial is presented immediately and at the end of the battery of cognitive tasks (delayed). The procedure is essentially the same; however, the comparison coding strings are not displayed. Only the test stimuli are presented, and the subject has to indicate whether or not the displayed pair is correct or incorrect based on their recollection of the paired associates presented during the learning trial Logical reasoning This task of abstract reasoning and verbal syntax [27] requires a subject to compare a single sequence (e.g., & precedes #) and a pictorial relation (e.g. & #) to determine if the former is an accurate description of the latter. This task requires the ability to determine whether various simple sentences correctly describe the relational order of the two symbols Matching-to-sample In this task, a single 44 matrix (i.e. a checkerboard) is presented on a computer screen. For each presentation of the matrix, the number of cells that are shaded varies at random. After a delay, the grid is replaced with two similar patterns, one of which is the original. This test of attention, spatial and short-term or working memory, requires the subject to correctly identify which comparison matrix matches the sample matrix Continuous performance This is a continuous recall task requiring encoding and storage and use of the working memory [28]. The subject is required to continuously monitor a randomized sequence of letters presented one at a time and to determine if the probe letter matches the target letter that immediately preceded it. They are requested to press a different key if the probe letter does not match the target letter Simple reaction time This task measures simple visuomotor mental flexibility. The test presents a simple stimulus on the screen. The participant is then instructed to press a specified response key each time the stimulus is present. The accuracy on this task was 100% for all participants; hence, only measures of efficiency and response time are calculated Sternberg Memory Search (Sternberg 6) This test is based on Sternberg s [29] paradigm of reaction time and measures information processing. Encoding, catego-

4 T.M. Mäkinen et al. / Physiology & Behavior 87 (2006) rization, response selection, execution, and visual and shortterm memory are assessed. The subject is presented with a set of 6 letters (designated as the memory set) and is required to memorize them. Subsequently, similar and dissimilar letters are presented on the screen one at a time. The subject indicates whether or not the probe letter matches any of the memory set items. Each successive administration of the test uses a unique memory set Statistical analysis The effect of exposure period on skin and rectal temperatures, VO 2, BP, HR and catecholamines was tested by the repeated measures ANOVA (within factor: day of exposure 1 10). Separate days were compared by simple contrasts (equivalent to paired t-tests). The effect of temperature (control versus cold) was tested by paired samples t-tests. Medians of thermal sensations were calculated. The effect of the temperature exposure on thermal sensations was examined by Wilcoxon s Signed Rank tests. The effect of exposure period on thermal sensations was examined using the Kendall s W test. Cognitive performance measures were compared by temperature exposure (control versus cold) and by day of testing using paired-sample t-tests. A repeated measures ANOVA was conducted to determine if cognitive performance changed over the 10-d period and whether there was a significant association with temperature exposure. Spearman correlation coefficients were calculated to assess the associations between cognitive performance and the different physiological measures. Principal components factor analysis revealed the existence of a single factor for accuracy (accounting for 52.7% of the variance) and two factors for efficiency (accounting for 54.8% and 15.3% of the variance) and response time (accounting for 50.0% and 16.1% of the variance) when all cognitive tasks were combined. The factors for efficiency and response time with the largest percent of variance accounted for were comprised of the six tasks measuring complex cognitive processes (code substitution, code substitution delayed, logical reasoning, matching-to-sample, continuous performance, and Sternberg 6). The second factor for efficiency and response time included only one task (simple reaction time) which measures simple cognitive processing. A pooled time series method was used for multivariate analyses of the independent effects of test order (a measure, ranging from 1 to 20 of the point at which a specific cognitive test was administered over the 10-d period (2 tests per day)), exposure to cold and physiological measures of thermoregulation on test accuracy, efficiency and response time of all of the cognitive tasks combined using a least squares dummy variable regression model and fixed effects [30]. For each dependent variable, the following variables were entered into the regression equation prior to the entry of the independent variables: 1) a set of n 1 dummy variables to represent each participant, thereby removing all variance caused by differences between persons, leaving only variance caused by change within-persons over time to be explained; 2) a variable for the lag (i.e., previous test s value during the 24-h period) of the dependent variable to eliminate serial dependency by assuming a first-order correlation in the series and to control for learning effects; and 3) a variable for the sequence of experimental condition to eliminate any linear effects arising from the repeated responses to this measure. To avoid multicollinearity, the variables with the strongest correlation with the combined measures of cognitive task accuracy, efficiency and response time within each group of perceptual (thermal sensations in hands) and physiological (T rect,o 2 intake, DBP, and HR) measures of thermoregulation were entered into the model. DBP and HR were both included because of a low correlation between the two variables (r = 0.02). Statistical significance was set at p < Results 3.1. Thermoregulation during repeated cold exposures Mean values of T rect, T sk, T fing, and HR measured during the cognitive tests (duration 20 min) under control and cold conditions are presented in Table 1. During each cold exposure T rect decreased by C (p <0.01), T sk by C (p <0.001) and T fing C (p <0.001) compared with control conditions. In the cold VO 2 increased from 17% to 26% and was significantly higher in cold compared with control conditions on day 10 (t = 2.821, p <0.05) (Table 1). Visible shivering was observed in some of the subjects during the cognitive tests. Under control conditions, SBP decreased by 9 mm Hg by day 10 (t = 2.6, df =9, p < 0.05) and DBP by 8 mm Hg (t = 2.5, df = 9, p < 0.05) compared with the first day. In the cold, SBP was significantly higher by mm Hg ( p < 0.01) and DBP was significantly higher by mm Hg ( p <0.01), compared with control. However, BP did not change significantly over the 10-d exposure period in the cold. The general thermal sensation (assessed after 2 h of cold exposure) changed from cold (day 1) to cool (day 10) in the course of the 10-d exposure period ( p <0.05) (Table 1). The median thermal sensations of the hands were cold and did not change over the 10-d period Effects of 10-d exposure period on cognitive performance Comparisons of cognitive tasks accuracy (% correct responses) over the 10-d period revealed no significant changes under control conditions (data not shown). However, in the cold significant improvements in accuracy over time were observed in the code substitution ( F(1, 9) = 2.77, p < 0.05), code substitution delayed ( F(1, 9) = 2.52, p < 0.05), logical reasoning ( F(1,9)= 3.53, p < 0.05), and Sternberg 6 tasks ( F(1,9)=3.05, p <0.01). Cognitive task efficiency improved under control conditions in the code substitution ( F(1,9)=6.33, p <0.01), logical reasoning ( F(1, 9) = 5.32, p < 0.01), continuous performance ( F(1,9)=9.66, p <0.01), and simple reaction time tasks

5 170 T.M. Mäkinen et al. / Physiology & Behavior 87 (2006) Table 1 Rectal and skin temperatures, O 2 intake, BP, HR, thermal sensations and thermal comfort during the cognitive test (n =10, meants.e.) Parameter Day 1 Day 5 Day 10 Control 10 -C Control 10 -C Control 10 -C T rect 37.1T T0.1 a 37.1T T0.1 a 37.1T T0.1 a T sk 32.5T T0.2 b 32.5T T0.2 b 32.4T T0.3 b T fing 28.8T T0.4 b 29.6T T0.3 b 29.7T T0.5 b O 2 intake l/min 0.3T T T T T T0.02 c SBP 134T4 150T5 a 128T4 d 149T4 b 125T4 d 147T4 a DBP 82T3 92T4 a 77T3 89T3 a 74T2 d 93T4 c HR 70T2 68T3 74T4 69T3 c 70T2 67T4 Thermal sensation e General 0 3 a a 1 2 a,d Hands 0 3 a 1 3 a 1 3 a Comfort f 0 2 a 0 2 a 0 1 a a Significantly different from control, p <0.01. b Significantly different from control, p < c Significantly different from control, p <0.05. d Significantly different from the same exposure on day 1, p <0.05. e Thermal sensations: 1=slightly warm, 0=neutral, 1=slightly cool, 2=cool, 3=cold. f Thermal comfort: 0=comfortable, 1=slightly uncomfortable, 2=uncomfortable. ( F(1,9)=3.36, p <0.05). In cold, efficiency was significantly improved during the 10-d exposure period in the following tasks: code substitution ( F(1,9)=4.79, p <0.01), logical reasoning ( F(1,9)=7.69, p <0.001), matching-to-sample ( F(1,9)= 5.31, p <0.001), and continuous performance ( F(1,9)=9.68, p <0.001). Response times were significantly shorter under control conditions only on the continuous performance task ( F(1,9)=8.64, p <0.01). In the cold, response time declined significantly on the code substitution ( F(1,9)=3.84, p <0.001), logical reasoning ( F(1, 9) = 8.49, p < 0.001), matching-to-sample ( F(1,9)=3.60, p < 0.001), continuous performance ( F(1,9)= 5.69, p <0.001), simple reaction time ( F(1,9)=3.07, p <0.05), and Sternberg 6 tasks ( F(1,9)=3.21, p <0.01). When comparing the magnitude of changes occurring in cognitive performance over the 10-d exposure period between control and cold conditions only a few differences were observed. Efficiency improved more under control conditions in the code substitution (day 1 day 10, t = 2.384, p <0.05) and matching-to-sample tasks (day 1 day 10, t = 2.264, p <0.05) than in cold conditions. On the other hand, response times were considerably shorter under cold conditions in the logical reasoning task (day 1 day 5, t = 3.031, p <0.05) compared with control conditions. An example of changes in efficiency and response times during the 10-d exposure period in a complex (logical reasoning) and simple (simple reaction time) task is presented in Fig Effects of cold exposure on cognitive performance When examining the individual tests cognitive task accuracy was significantly worse in cold compared with control conditions on the code substitution delayed and the Sternberg 6 tasks on day 5 ( p <0.05) and on the continuous performance task on day 10 (Table 2). Efficiency on the code substitution delayed task was significantly worse on both days 5 and 10 (t = 2.397, p < 0.05). There were no significant differences in efficiency in the other tasks between control and cold. Response time on the logical reasoning task was significantly faster after exposure to cold on days 5 and 10. The continuous performance task was also performed faster on day 5 under cold compared with control conditions. In contrast, on day 10, response time was significantly longer on the code substitution delayed task (t = 2.323, p <0.05) under cold compared with control conditions. Test order was inversely associated with accuracy on the code substitution delayed task and with response time on six of the seven tasks. It was positively associated with efficiency on five of the seven tasks (Table 3). Exposure to cold was inversely associated with accuracy on the code substitution, code substitution delayed, and continuous performance tasks, and with efficiency on the code substitution delayed and simple reaction time tasks, and positively associated with response time on the simple reaction time task Thermoregulation and cognitive performance The associations between cognitive performance and thermoregulation are presented in Table 4. T rect correlated positively with accuracy on three tasks (code substitution, continuous performance, Sternberg 6) and response time on six of the seven tasks. However, it was also inversely associated with efficiency on every task. T sk and/or T fing correlated positively with accuracy on two tasks (code substitution delayed, continuous performance), and with efficiency on one task (simple reaction time), and negatively with response time on one task (simple reaction time). However, lower skin temperatures were also associated with a greater efficiency and faster response times on the logical reasoning task and longer response time on the simple reaction time task (Table 4).

6 T.M. Mäkinen et al. / Physiology & Behavior 87 (2006) Median reaction time (ms) Median reaction time (ms) Logical reasoning -reaction time Day of exposure Simple Reaction Time Test -reaction time control cold control cold Day of exposure Efficiency % Efficiency % Logical reasoning -efficiency Day of exposure Simple reaction time -efficiency Day of exposure control cold control cold Fig. 2. Performance efficiency and response times in a complex (logical reasoning) and simple (simple reaction time) task during the 10-day exposure to cold (n =10, meants.e.). Oxygen intake correlated positively with performance response time in five out of seven tasks and negatively with efficiency in four of the tasks (Table 4). SBP and DBP were both inversely associated with accuracy on three tasks (code substitution, continuous performance, and Sternberg 6), and inversely associated with efficiency and positively associated with response time on the simple reaction time task. DBP was positively associated with efficiency and inversely associated with response time on the code substitution, matching-to-sample, and Sternberg 6 tasks. HR correlated positively with accuracy and response time on the code substitution delayed task and negatively with accuracy on the continuous performance and response time on the Sternberg 6 task. A general thermal sensation of cold was inversely associated with accuracy on the code substitution, code substitution delayed, and continuous performance tasks; inversely associated with efficiency in the logical reasoning and simple reaction time tasks; and positively associated with response time on the simple reaction time task (Table 4). Sensations of cold in the hands were inversely associated with accuracy in three tasks (code substitution, code substitution delayed, continuous performance) and with efficiency in four tasks (code substitution, code substitution delayed, logical reasoning, simple reaction time), positively associated with response time in two tasks (logical reasoning, simple reaction time) and negatively with the code substitution task Model of cognitive performance and thermoregulation Results of regression analysis identifying independent predictors of cognitive performance accuracy, efficiency, and response time of the simple reaction time task which assesses simple cognitive processing and all complex cognitive tasks combined are presented in Table 5. Low T rect was a significant independent predictor of increased efficiency ( p < 0.001) and reduced response time ( p <0.001) in performance of the simple reaction time task. High DBP was a significant independent predictor of reduced efficiency ( p <0.001) and increased response time ( p <0.01), and an increased HR was a significant independent predictor of increased efficiency ( p < 0.01) and reduced response time ( p <0.05) on this task as well. Repetition of the cognitive tests (test order) was a significant independent predictor of increased efficiency ( p < 0.001) and shorter response time in performance of the complex cognitive tasks ( p <0.001). Exposure to cold was a significant independent predictor of increased accuracy ( p < 0.01) and response time ( p < 0.001) and decreased efficiency ( p < 0.001). Low T rect was a significant independent predictor of increased efficiency ( p <0.001) and shorter response time ( p <0.001). High DBP was a significant independent predictor of decreased accuracy ( p <0.001) and response time ( p <0.05). A lowered HR in the cold was a significant independent predictor of decreased accuracy ( p <0.001) and response time ( p <0.05). Thermal sensation of cold in the hands was a significant

7 172 T.M. Mäkinen et al. / Physiology & Behavior 87 (2006) Table 2 Mean (TSE) cognitive task accuracy, efficiency and response times on days 1, 5, and 10 at control (25 -C) or cold (10 -C) conditions Tasks Day 1 Day 5 Day 10 Control 10 -C Control 10 -C Control 10 -C Accuracy (% correct) Code substitution 98.1T T T T T T0.7 Code sub delayed 93.0T T T T4.4* 91.9T T4.7 Logical reasoning 49.6T T T T T T0.8 Matching-to-sample 96.7T T T T T T0.0 Continuous performance 95.9T T T T T T0.9* Sternberg T T T T1.0* 97.8T T1.1 Efficiency Code substitution 67.0T T T T T T4.3 Code sub delayed 67.0T T T T6.2* 70.9T T7.5* Logical reasoning 17.1T T T T T T2.2 Matching-to-sample 44.4T T T T T T7.0 Continuous performance 130.6T T T T T T7.4 Simple reaction time 243.1T T T T T T5.4 Sternberg T T T T T T4.2 Response time (ms) Code substitution 855T62 846T64 789T60 774T27 747T53 763T45 Code sub delayed 763T54 820T80 767T67 793T69 723T65 820T91* Logical reasoning 1653T T T T81* 1365T T110* Matching-to-sample 1234T T T T T T115 Continuous performance 434T20 429T18 398T17 385T15* 364T15 362T17 Simple reaction time 232T5 241T6 227T5 231T3 222T6 227T5 Sternberg 6 585T26 589T27 572T26 557T31 527T23 540T21 * Significantly different from control, p <0.05. Table 3 Spearman s correlations coefficients of cognitive performance, the number of tests performed (test order), and exposure (temperature) Tasks Test sequence Cold exposure Accuracy (% correct) Code substitution *** Code substitution delayed 0.16* 0.19** Logical reasoning Matching-to-sample Continuous performance *** Sternberg Efficiency Code substitution 0.17* 0.09 Code substitution delayed * Logical reasoning 0.31*** 0.04 Matching-to-sample 0.23** 0.01 Continuous performance 0.39*** 0.08 Simple reaction time 0.34*** 0.22** Sternberg Response time (ms) Code substitution 0.18* 0.06 Code substitution delayed Logical Reasoning 0.33*** 0.01 Matching-to-sample 0.19** 0.01 Continuous performance 0.36*** 0.03 Simple reaction time 0.22** 0.36*** Sternberg * 0.05 * p <0.05. ** p <0.01. *** p < independent predictor of decreased accuracy ( p < 0.05) and shorter response time ( p <0.05). 4. Discussion The present study investigated the effects of single and repeated cold exposure on cognitive performance and found signs of both decreased and improved cognitive performance. The differential outcomes were mainly related to changes in performance strategy Effect of cold exposure on cognitive functioning We used a cold exposure which caused general and local cold thermal sensations and discomfort, superficial skin cooling ( 6 7 -C), a higher M and an elevated BP ( mm Hg) compared with control conditions. The rectal temperature dropped approximately 0.4 -C which indicates that deep body cooling had initiated. With this type of cold exposure both a decline and an improvement in cognitive performance were observed. The differential outcomes are related to changes in performance strategy which deviated between the different tasks. Cold exposure was inversely associated with accuracy on three tasks (code substitution, code substitution delayed, continuous performance) and efficiency on two tasks (code substitution delayed, simple reaction time), and directly associated with response time in one task (simple reaction time). When all the different tasks were combined (regres-

8 T.M. Mäkinen et al. / Physiology & Behavior 87 (2006) Table 4 Spearman s correlations coefficients of cognitive performance and physiological measures of thermoregulation Tasks Thermal sensation Temperature Metabolism Cardiovascular General Hands T rect T sk T fing O 2 intake SBP DBP HR Accuracy (% correct) Code substitution 0.32*** 0.28*** 0.19* ** 0.31*** 0.08 Code substitution delayed 0.15* 0.23** *** 0.19** *** Logical reasoning Matching-to-sample <0.01 Continuous performance 0.29*** 0.31*** 0.30*** 0.21** 0.18* *** 0.38*** 0.19* Sternberg *** * 0.21** 0.14 Efficiency Code substitution * 0.27*** *** * 0.07 Code substitution delayed * 0.21** * Logical reasoning 0.16* 0.19* 0.29*** 0.15* * Matching-to-sample *** * * 0.08 Continuous performance *** Simple reaction time 0.24*** 0.19* 0.20** 0.25*** 0.22** *** 0.32*** 0.11 Sternberg ** * 0.15 Response time (ms) Code substitution * 0.24*** *** * 0.12 Code substitution delayed *** * * Logical reasoning * 0.30*** 0.17* * < Matching-to-sample *** * * 0.07 Continuous performance *** Simple reaction time 0.32*** 0.30*** *** 0.35*** 0.29** 0.36*** 0.34*** 0.11 Sternberg *** ** 0.20 * p <0.05. ** p <0.01. *** p < sion analysis) cold exposure was a significant independent predictor of longer response times and decreased efficiency. These results are consistent with studies demonstrating longer response times in the cold [3,6,14,15]. Some of the changes in thermoregulation caused by the cold exposure were associated with the observed decrement in cognitive performance. These associations were found between cognitive performance and cold thermal sensations, reduced Table 5 Regression analysis of cognitive performance accuracy, efficiency, and response time Accuracy Efficiency Response time B S.E. Beta B S.E. Beta B S.E. Beta Simple cognitive task a Test order Cold exposure Thermal sensation in hands Rectal temperature 33.24*** *** Diastolic blood pressure 0.87*** ** Heart rate 0.93** * O 2 intake < Complex cognitive tasks Test order *** *** Cold exposure 28.95*** *** *** Thermal sensation in hands 5.34** * Rectal temperature *** *** Diastolic blood pressure 0.58*** * Heart rate 0.86*** < < * O 2 intake a The simple reaction time task. This task had 100% accuracy in this study; hence, a regression model of accuracy on this task was not calculated. * p <0.05. ** p <0.01. *** p <0.001.

9 174 T.M. Mäkinen et al. / Physiology & Behavior 87 (2006) skin and rectal temperature, increased O 2 intake, increased BP and decreased HR in the cold. The association between these thermoregulatory parameters on cognitive performance deviated between the different cognitive tasks. The observed correlation coefficients ranged between 0.1 and 0.4 explaining approximately 15% of the variance between thermoregulation and cognitive performance. These findings suggest that cold exposure had a negative effect on both simple as well as complex cognitive skills requiring sustained attention and concentration, verbal learning, numeric and symbolic facility, reasoning and operation of the working memory. Our results are in accordance with previous studies where even brief, apparently non-hypothermic exposures to cold have resulted in impaired cognitive performance [4 6,8,9,11]. In the present study also a simple cognitive task (simple reaction time) was adversely affected by cold exposure, which is inconsistent with a previous study where specifically the performance of complex cognitive tasks decreased by cold water immersion, while simple tasks remain unaffected [19]. On the other hand, our previous study where subjects were exposed to moderate cold (10 -C) for several hours showed a decreased accuracy in the simple reaction time task [18]. The different results are probably related to the variability in the study designs, type (water or air), duration and intensity of cold exposure and the clothing used. Certain findings from this study offer partial support for the hypothesis that exposure to cold may also be associated with improved cognitive performance as was observed in our previous study [18]. Most often these changes were manifested as reduced response times and an increased overall efficiency in the cold. Furthermore, when all tasks were combined (regression analysis) we observed an improved cognitive task accuracy. In addition to the negative and positive effects described above, we observed two distinct patterns of mixed effects of cold exposure on cognitive performance. In the first pattern, cold exposure resulted in an increased accuracy, but also with a longer response time and a decreased overall efficiency when all the different cognitive tasks were combined (Table 5). In the second pattern, a cold-related increase in blood pressure was associated with a decrease in response time, but a decrease in accuracy as well. Both patterns would appear to be consistent with the speed accuracy tradeoff strategy where some studies have reported shorter response times [9,11,12,17], but also more errors in the cold [13,17] Repeated cold exposures and cognitive performance In general the observed changes in thermoregulation over the acclimation period were relatively modest. In fact, the cold habituation responses were more evident during the initial cooling phase (first 30 min), after which the differences evened out at the end of the exposure (data not presented). Although T sk increased by 0.4 -C and T fing by 0.9 -C when compared between the last and first day of exposure, the changes were not significant. The subjects experienced less intense general sensations to cold which is a characteristic habituation response demonstrated also in a previous study employing a similar exposure protocol [20]. No changes in metabolic rate or HR over the exposure period were observed. BP decreased significantly under control conditions suggesting that the subjects were less stressed at the end of the 10-d exposure period. One reason for not being able to demonstrate significant differences is partially due to the relatively small sample size, which could have precluded our ability to have sufficient power to detect statistically significant differences. To our knowledge, this is the first study to follow cognitive performance in cold for such a long period. We found that cognitive performance was significantly improved over time both under control and cold conditions, suggesting a learning effect. One of the few studies using a multiple cold exposure design (three repetitions on separate weeks) found that matching to sample performance decreased in the cold but remained the same throughout the repetitions [9]. In our study when examining what caused the improvement in cognitive performance over time, it was found in general that performance accuracy did not change markedly, with the exception of the continuous performance task, in which accuracy improved with each test repetition. The most considerable changes were that response times were shorter, which improved the overall performance efficiency. In some of the tests these changes tended to stabilize after approximately five days of exposure to either control or cold conditions. There were no marked differences in the change in cognitive performance between control and cold over the exposure period. Performance efficiency improved more over time at control conditions in two complex cognitive tasks, but not on the other tasks. Furthermore, response times decreased more in the cold over the 10-d exposure period in the logical reasoning task, but not on any other task. These results suggest that the repeated cold exposures and observed changes in thermoregulation, thermal sensations and comfort had only a very small effect on cognitive performance Model of cognitive performance and thermoregulation Two distinct explanations for the changes in cognitive performance during cold exposure have been presented. The negative effects of cold exposure and cold-related physiological changes on cognitive performance are consistent with the distraction hypothesis [5,7,14,31]. In the present study support for the distraction hypothesis was derived from the observation that decreased skin temperatures and thermal sensations of cold were associated with longer response times and a decreased efficiency in the simple reaction time task which measures simple visuomotor response times. The observed cold-related increases in diastolic blood pressure and decreases in heart rate were also significant independent predictors of reduced efficiency and increased response time in performance of this task (Table 5). It is possible that especially simple cognitive tasks are susceptible to the distraction caused by the cold exposure as was shown in our previous study [18]. In addition, cold exposure and the thermal sensation of cold were inversely associated with accuracy and efficiency and positively associated with response time on a number of tasks of complex cognitive performance.

10 T.M. Mäkinen et al. / Physiology & Behavior 87 (2006) Furthermore, cold exposure was a significant independent predictor of an improvement in accuracy, but also longer response times and a decrease in efficiency when all complex tasks were combined. The observed cold-related discomfort and shivering could consume central attention resources resulting in longer response times due to the fact that the participants had to concentrate more on the given task. The positive effects of cold exposure and cold-related physiological changes on cognitive performance are consistent with the arousal hypothesis in which cold exposure results in an initial improvement in performance before it results in a performance decrement [12,13,15,32]. Support for the arousal hypothesis is derived from the observation that in our study response times were shorter and efficiency increased in the cold. This phenomenon was observed when examining the association between T rect and cognitive performance. This would suggests that with a slight decline in core body temperature (from 37.1 to C), participants became more aroused or engaged in performing the task, viewed the cold as a challenge and devoted greater attention in completing all tasks. It is possible that with regard to T rect, the initial temperature indicated some stress, and that the level to which T rect dropped in cold is in fact a normal core temperature and more optimal with regards to cognitive performance. A previous cold water immersion study demonstrated that an initial cooling (not causing a marked drop in T rect ) improved cognitive performance of complex tasks [19]. Eventually, if the core temperature would have dropped further in our study, adverse performance outcomes would probably have been observed. The second pattern of arousal was illustrated by shorter response times, but unaltered efficiency. At the same time performance accuracy declined. This phenomenon was observed when examining the associations between cold thermal sensation of hands, a lowered HR in cold, and an increased DBP and cognitive performance. This pattern is also consistent with the arousal hypothesis. However, the decline in accuracy, despite a faster response time, may be an indicator that the individual is approaching a form of mental exhaustion and has abandoned his or her efforts to devote sustained attention to the task. Although not presented in detail in this study, it is known that some of the hormonal responses related with exposure to cold may also be connected to changes in cognitive performance. Acute cold stress activates the autonomic nervous system associated with increased levels of circulating norepinephrine (NE) [33]. In most cases the circulating epinephrine (E) levels remain unchanged in cold. The increased release of the CNS catecholamines, NE and dopamine may reduce the overall neurotransmitter release and have an adverse effect on cognition [8]. A previous study demonstrated that combining cold and cognitive performance resulted in increases in both NE and E levels [34]. Cold exposure also stimulates the secretion of thyroid hormones to increase metabolic heat production. Increases in plasma TSH levels are not usually obtained in short-term exposures to cold where the drop in T rect is less than 1 -C [33]. However, prolonged or severe exposure to cold alters the thyroid function including elevated TSH levels and/or enhanced TSH response to thyrotropin releasing hormone (TRH) stimulation and a lowered serum free T 3 concentration [35]. These responses may be associated with a disruption in cognitive performance. This is supported by the fact that administration of T 4 improves matching to sample performance during a prolonged Antarctic residence [36]. It is, however, unlikely that thyroid hormones would have affected cognitive performance in our study because a previous study employing the same cold exposure did not find any changes in thyroid hormone secretion [20]. In conclusion, exposure to cold was associated with improved accuracy, but also longer response times, leading to decreased efficiency. In contrast, some of the thermoregulatory parameters were independent predictors of decreased accuracy, but also shorter response time, leading to increased efficiency. No clear pattern of an effect of cold on a specific cognitive task (e.g. short-term memory, attention, executive functioning) was observed. Efficiency for performing the cognitive tasks was significantly improved and response times decreased over the 10-d period both under control and cold exposures, suggesting a learning effect. The observed small changes in thermoregulation, thermal sensations and discomfort had little, if any effect on cognitive performance. It is suggested that moderate cold exposure affects cognitive performance negatively through the mechanisms of distraction and both positively and negatively through the mechanisms of arousal caused by the cold exposure. Acknowledgements This study was supported by the Graduate School of Circumpolar Wellbeing, Health and Adaptation coordinated by the Centre for Arctic Medicine at the University of Oulu, and, in part, by a grant from the National Science Foundation of the United States (OPP ). We would like to thank the test subjects for their dedication to this study. The experiments performed during this study comply with the current laws of Finland. References [1] Palinkas LA. Mental and cognitive performances in the cold. Int J Circumpolar Health 2001;60(3): [2] Pilcher JJ, Nadler E, Busch C. Effects of hot and cold temperature exposure on performance: a meta-analytic review. Ergonomics 2002;15: 45(10): [3] Coleshaw SRK, van Someren RNM, Wolff AH, Davis HM, Keatinge WR. 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