Physiology & Behavior 8

Effect of repeated exposures to cold on cognitive performance in humans

Tiina M. Makinen a,*, Lawrence A. Palinkas b, Dennis L. Reeves c, Tiina Paakkonen d,

Hannu Rintamaki d,e, Juhani Leppaluoto d, Juhani Hassi a

a Centre for Arctic Medicine, Thule Institute, University of Oulu, P.O. Box 5000, FIN-90014, Finlandb School of Social Work, University of Southern California, Los Angeles, CA, USA

c Clinvest Inc., USAd Department of Physiology, University of Oulu, Finlande 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 (Trect) 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 Trect (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. Trect, 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 environ-

mental temperatures may significantly affect cognitive perfor-

mance [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

0031-9384/$ - see front matter D 2005 Elsevier Inc. All rights reserved.

doi:10.1016/j.physbeh.2005.09.015

* Corresponding author. Tel.: +358 8 537 6208; fax: +358 8 537 6203.

E-mail address: tiina.makinen@oulu.fi (T.M. Makinen).

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 non-

hypothermic, 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

7 (2006) 166 – 176

T.M. Makinen et al. / Physiology & Behavior 87 (2006) 166–176 167

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 perfor-

mance due to a reduced amount of distraction. At present it is

not known whether possible changes occurring in thermoreg-

ulation caused by repeated cold exposures are associated with

cognitive performance.

SUBJECTS 1-10

cognitive tests70-90 min•Tsk, Trect•HR

COLD (CONTROL (25 °C) 90 min

•Thermal sensati•BPVO2

Fig. 1. Study design. Ten subjects performed the cognitive tests on 10

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 specif-

ically 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- N25- E) in September–October 2003. 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 22.3T1.6, body fat % 17.1T1.9 and VO2 max

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 Ostroboth-

nia 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 m2) 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 m2) 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. 1.

2.1. 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,

...... x 10 consecutive days

cognitive tests100-120 min•Tsk, Trect•HR

10 °C) 120 min

•Thermal sensations•BP

onsVO2

consecutive days at control (25 -C) and cold (10 -C) conditions.

T.M. Makinen et al. / Physiology & Behavior 87 (2006) 166–176168

anterior thigh, dorsal side of the foot and calf. Mean skin

temperature (Tsk) was calculated from the 10 sites as an area

weighed average [23]. In addition, finger skin temperature

(Tfing) was measured from the dorsal side of the middle finger.

Rectal temperature (Trect) 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 (VO2) 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 VO2, 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).

2.2. Cognitive performance

For assessing cognitive performance the Automated Neu-

ropsychological Assessment Metric [25] for Isolated and

Confined Environments (ANAM-ICE) version was adminis-

tered. 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 20.5T0.2min and included the following tasks:

2.2.1. 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.

2.2.2. 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.

2.2.3. Matching-to-sample

In this task, a single 4�4 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.

2.2.4. 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.

2.2.5. 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.

2.2.6. Sternberg Memory Search (Sternberg 6)

This test is based on Sternberg’s [29] paradigm of reaction

time and measures information processing. Encoding, catego-

T.M. Makinen et al. / Physiology & Behavior 87 (2006) 166–176 169

rization, response selection, execution, and visual and short-

term 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.

2.3. Statistical analysis

The effect of exposure period on skin and rectal tempera-

tures, VO2, 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 temper-

ature 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 associa-

tions between cognitive performance and the different physi-

ological 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

(Trect, O2 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 <0.05.

3. Results

3.1. Thermoregulation during repeated cold exposures

Mean values of Trect, Tsk, Tfing, and HR measured during

the cognitive tests (duration 20 min) under control and cold

conditions are presented in Table 1. During each cold

exposure Trect decreased by 0.3–0.4 -C ( p <0.01), Tsk by

6–6.4 -C ( p <0.001) and Tfing 15.3–16.1 -C ( p <0.001)

compared with control conditions. In the cold VO2 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 condi-

tions, 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 16–22 mm Hg ( p <0.01) and DBP was signifi-

cantly higher by 10–19 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.

3.2. 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

Table 1

Rectal and skin temperatures, O2 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

Trect 37.1T0.1 36.7T0.1a 37.1T0.1 36.7T0.1a 37.1T0.04 36.7T0.1a

Tsk 32.5T0.2 26.0T0.2b 32.5T0.1 26.0T0.2b 32.4T0.2 26.4T0.3b

Tfing 28.8T1.7 13.5T0.4b 29.6T1.1 13.5T0.3b 29.7T0.7 14.4T0.5b

O2 intake l/min 0.3T0.01 0.4T0.03 0.3T0.02 0.4T0.03 0.3T0.02 0.4T0.02c

SBP 134T4 150T5a 128T4d 149T4b 125T4d 147T4a

DBP 82T3 92T4a 77T3 89T3a 74T2d 93T4c

HR 70T2 68T3 74T4 69T3c 70T2 67T4Thermal sensatione

General 0 �3a 0.5 �2a 1 �2a,d

Hands 0 �3a 1 �3a 1 �3a

Comfortf 0 2a 0 2a 0 1a

a Significantly different from control, p <0.01.b Significantly different from control, p <0.001.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.

T.M. Makinen et al. / Physiology & Behavior 87 (2006) 166–176170

(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-sam-

ple (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. 2.

3.3. 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.

3.4. Thermoregulation and cognitive performance

The associations between cognitive performance and

thermoregulation are presented in Table 4. Trect 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. Tsk and/or Tfing

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).

15161718192021222324252627282930

Eff

icie

ncy

%E

ffic

ien

cy %

control coldLogical reasoning

-efficiency

1 2 3 4 5 6 7 8 9 10 1 2 3 4 5 6 7 8 9 10

1 2 3 4 5 6 7 8 9 101 2 3 4 5 6 7 8 9 10

1000

1100

1200

1300

1400

1500

1600

1700

1800

1900

2000M

edia

n r

eact

ion

tim

e (m

s)M

edia

n r

eact

ion

tim

e (m

s)

Day of exposure

Day of exposure Day of exposure

Day of exposure

control cold

Logical reasoning-reaction time

215

220

225

230

235

240

245

250

255

260

265

270

275

280

control cold

Simple reaction time-efficiency

200

205

210

215

220

225

230

235

240

245

250 control cold

Simple Reaction Time Test-reaction time

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.).

T.M. Makinen et al. / Physiology & Behavior 87 (2006) 166–176 171

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.

3.5. 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 Trect 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 indepen-

dent predictor of increased accuracy ( p <0.01) and response

time ( p <0.001) and decreased efficiency ( p <0.001). Low

Trect 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

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 98.1T0.8 97.5T0.8 96.7T1.2 95.4T0.6 96.9T0.4 96.4T0.7

Code sub delayed 93.0T4.8 88.6T5.0 89.4T4.6 82.2T4.4* 91.9T5.1 88.6T4.7Logical reasoning 49.6T1.0 50.0T1.5 51.7T0.9 51.3T1.4 48.8T1.5 49.6T0.8

Matching-to-sample 96.7T1.5 95.3T1.7 96.0T1.1 97.3T1.1 97.3T1.5 100.0T0.0

Continuous performance 95.9T0.7 94.7T1.2 97.7T0.5 96.1T0.9 97.0T0.7 95.9T0.9*

Sternberg 6 99.5T0.3 98.3T1.1 98.3T0.8 96.3T1.0* 97.8T1.0 96.8T1.1

Efficiency

Code substitution 67.0T4.4 68.0T4.7 72.7T4.6 71.0T3.2 76.7T5.5 73.4T4.3

Code sub delayed 67.0T4.6 59.9T7.7 63.5T6.6 53.7T6.2* 70.9T5.9 60.7T7.5*Logical reasoning 17.1T1.2 17.4T0.7 23.3T1.9 23.1T1.8 22.7T1.5 25.1T2.2

Matching-to-sample 44.4T4.0 52.8T3.4 53.1T6.4 55.8T5.4 57.4T5.2 64.8T7.0

Continuous performance 130.6T6.0 130.5T5.0 144.7T7.2 146.5T5.7 158.1T6.8 157.9T7.4

Simple reaction time 243.1T7.8 238.3T7.3 252.4T6.2 250.8T3.9 264.3T7.4 258.0T5.4Sternberg 6 98.3T4.9 94.2T5.3 99.6T4.7 99.1T6.3 107.7T5.0 102.4T4.2

Response time (ms)

Code substitution 855T62 846T64 789T60 774T27 747T53 763T45

Code sub delayed 763T54 820T80 767T67 793T69 723T65 820T91*

Logical reasoning 1653T126 1769T120 1474T123 1307T81* 1365T123 1242T110*

Matching-to-sample 1234T135 1172T101 1152T160 1061T142 1013T130 946T115Continuous 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 �0.12 �0.26***

Code substitution delayed �0.16* �0.19**

Logical reasoning �0.06 0.02

Matching-to-sample 0.13 �0.01

Continuous performance 0.09 �0.25***

Sternberg 6 �0.11 �0.09

Efficiency

Code substitution 0.17* �0.09

Code substitution delayed 0.01 �0.15*

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 6 0.13 0.02

Response time (ms)

Code substitution �0.18* 0.06

Code substitution delayed �0.06 0.09

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 6 �0.15* �0.05

* p <0.05.

** p <0.01.

*** p <0.001.

T.M. Makinen et al. / Physiology & Behavior 87 (2006) 166–176172

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.

4.1. Effect of cold exposure on cognitive functioning

We used a cold exposure which caused general and local

cold thermal sensations and discomfort, superficial skin cool-

ing (¨6–7 -C), a higher M and an elevated BP (¨10–20 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, conti-

nuous 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-

Table 4

Spearman’s correlations coefficients of cognitive performance and physiological measures of thermoregulation

Tasks Thermal sensation Temperature Metabolism Cardiovascular

General Hands Trect Tsk Tfing O2 intake SBP DBP HR

Accuracy (% correct)

Code substitution �0.32*** �0.28*** 0.19* 0.10 0.11 �0.04 �0.20** �0.31*** �0.08

Code substitution delayed �0.15* �0.23** 0.13 0.24*** 0.19** �0.11 �0.08 �0.06 0.28***

Logical reasoning 0.03 0.04 �0.04 �0.02 �0.01 �0.03 �0.02 �0.04 �0.01

Matching-to-sample �0.3 �0.06 0.12 0.01 0.04 �0.03 �0.04 �0.08 <0.01

Continuous performance �0.29*** �0.31*** 0.30*** 0.21** 0.18* �0.10 �0.28*** �0.38*** �0.19*

Sternberg 6 �0.10 �0.13 0.24*** 0.11 0.09 �0.07 �0.16* �0.21** �0.14

Efficiency

Code substitution �0.20 �0.23* �0.27*** 0.04 0.03 �0.34*** �0.05 0.15* 0.07

Code substitution delayed �0.14 �0.17* �0.21** 0.04 0.04 �0.23* �0.13 0.05 �0.08

Logical reasoning �0.16* �0.19* �0.29*** �0.15* 0.09 �0.21* �0.08 0.05 �0.03

Matching-to-sample �0.06 �0.07 �0.30*** �0.05 �0.13 �0.21* �0.06 0.17* �0.08

Continuous performance �0.14 �0.11 �0.27*** �0.02 0.06 �0.14 �0.11 �0.05 �0.09

Simple reaction time �0.24*** �0.19* �0.20** 0.25*** 0.22** �0.11 �0.32*** �0.32*** 0.11

Sternberg 6 �0.01 �0.01 �0.20** �0.07 �0.01 �0.04 0.08 0.18* 0.15

Response time (ms)

Code substitution 0.14 �0.19* 0.24*** �0.05 �0.05 0.31*** 0.01 �0.18* �0.12

Code substitution delayed 0.11 0.13 0.29*** 0.03 0.02 0.23* 0.10 �0.12 0.19*

Logical reasoning 0.14 0.17* 0.30*** 0.17* 0.09 0.19* <0.01 �0.09 0.04

Matching-to-sample 0.06 0.07 0.32*** 0.05 0.12 0.22* 0.09 �0.16* 0.07

Continuous performance 0.08 0.5 0.29*** 0.06 �0.03 0.11 0.03 �0.05 �0.09

Simple reaction time 0.32*** 0.30*** 0.11 �0.41*** �0.35*** 0.29** 0.36*** 0.34*** �0.11

Sternberg 6 0.01 �0.02 0.26*** 0.10 0.05 0.01 �0.12 �0.22** �0.20

* p <0.05.

** p <0.01.

*** p <0.001.

T.M. Makinen et al. / Physiology & Behavior 87 (2006) 166–176 173

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].

Table 5

Regression analysis of cognitive performance accuracy, efficiency, and response tim

Accuracy Efficie

B S.E. Beta B

Simple cognitive taska

Test order – – – 0.

Cold exposure – – – �7.

Thermal sensation in hands – – – 0.

Rectal temperature – – – �33.

Diastolic blood pressure – – – �0.

Heart rate – – – 0.

O2 intake – – – 0.

Complex cognitive tasks

Test order �0.37 0.23 �0.14 4.

Cold exposure 28.95*** 7.70 0.74 �92.

Thermal sensation in hands 5.34** 1.70 0.55 �7.

Rectal temperature 6.61 5.05 0.14 �108.

Diastolic blood pressure �0.58*** 0.16 �0.39 1.

Heart rate 0.86*** 0.17 0.45 <0.

O2 intake �46.28 24.35 �0.20 �119

a The simple reaction time task. This task had 100% accuracy in this study; h

* p <0.05.

** p <0.01.

*** p <0.001.

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

e

ncy Response time

S.E. Beta B S.E. Beta

58 0.38 0.14 �0.25 0.22 �0.10

22 12.68 �0.12 12.88 7.27 0.34

38 2.79 0.03 1.04 1.60 0.11

24*** 8.33 �0.44 26.24*** 4.78 0.57

87*** 0.26 �0.38 0.45** 0.15 0.32

93** 0.28 0.31 �0.40* 0.16 �0.22

83 40.11 <0.01 41.73 23.00 0.19

54*** 1.01 0.39 �62.73*** 12.32 �0.41

99*** 33.74 �0.53 1365.51*** 410.84 0.60

02 7.44 �0.16 128.48* 90.53 0.23

50*** 22.16 �0.51 1460.84*** 269.79 0.52

24 0.70 0.19 �19.89* 8.46 �0.23

01 0.76 <0.01 15.27* 9.22 0.14

.39 106.76 �0.12 1716.43 1299.92 0.13

ence, a regression model of accuracy on this task was not calculated.

T.M. Makinen et al. / Physiology & Behavior 87 (2006) 166–176174

skin and rectal temperature, increased O2 intake, increased BP

and decreased HR in the cold. The association between these

thermoregulatory parameters on cognitive performance de-

viated 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 learn-

ing, 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 (regres-

sion 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].

4.2. 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

Tsk increased by 0.4 -C and Tfing 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 perfor-

mance 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.

4.3. 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 effi-

ciency 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.

T.M. Makinen et al. / Physiology & Behavior 87 (2006) 166–176 175

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 Trect and cognitive performance. This

would suggests that with a slight decline in core body

temperature (from 37.1 to 36.7 -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 Trect, the initial temperature

indicated some stress, and that the level to which Trect 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 Trect) improved cognitive perfor-

mance 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 ob-

served 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 perfor-

mance. Acute cold stress activates the autonomic nervous

system associated with increased levels of circulating norepi-

nephrine (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 Trectis 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 T3

concentration [35]. These responses may be associated with a

disruption in cognitive performance. This is supported by the

fact that administration of T4 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 thermoregu-

lation, 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-0090343). 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.

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