Perceptual a t ~ dMotor Skills, 2003, 97,590-604
l'crceptual and Motor Skills 2003
INCREMENTAL EXERCISE, PLASMA CONCENTRATIONS OF CATECHOLAMINES, REACTION TIME, AND MOTOR TIME DURING PERFORMANCE O F A NONCOMPATIBLE CHOICE RESPONSE TIME TASK ' TERRY McMORRIS, MARK TALLON. CRAIG WILLIAMS
Utliuersity College Chichesier JOHN SPROULE
STEVE DRAPER
Uniuersity of Edir~brrrgh
University of Gloz~cestershire
JON SWAIN, JULIA POTTER, NEVILLE CLAYTON
Universliv College Chichester Szimmaty.-The primary purpose was to examine the effect of incremental exercise on a noncompatible response time task. Participants ( N = 9 ) undertook a 4-choice noncompatible response time task under 3 conditions, following rest and d u r ' i g exercise at 70% and 100% of their maximum power output. Reaction and movement rimes were the dependent variables. illaxirnum power output had been previously established on an incremental test to exhaustion. A repeated-measures multivariate a n d ysis of variance yielded a significant effect of exercise intensity on the task, but observation of the separate univariate repeated-measures analyses of variance showed that only movement time was significantly affected. Post hoc Tukey tests indicated movement time during maximal intensity exercise was significantly faster than in the other nvo conditions. The secondary purpose of the study was to assess whether increases in plasma concentrations of adrenaline and nor-adrenaline during exercise and power output would act as predictor variables of reaction and movement times during exercise. Catecholamine concentrations were based on venous blood samples taken during the maximum power output test. None of the variables were significant predictors of reaction time. Only power output was a significant predictor of movement rime (R2= .24). There was little support for the notion that peripheral concentrations of catecholarnines directly induce a central nervous system response.
A large amount of research has examined the effect of incremental exercise on the performance of various cognitive sk~lls,especially choice reaction time (see Tomporowski & Ellis, 1986; McMorris & Graydon, 2000, for reviews). Reaction time is generally considered to be the time that elapses from the presentation of a stimulus to the beginning of an overt response. While it is of interest, it is only part of the total response time. Response time
'Please address correspondence to Dr. T . Mchlorris, Centre for Sports Science and Medicine. University College Chichester, College Lane, Chichester, West Sussex PO19 6PE, UK or e-mail (
[email protected]).
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includes reaction time and movement time, the time taken to complete the movement (Magill, 1998; Schmidt & Lee, 1999). In mhtary, sports, and workplace situations concern is not only reaction time but also movement time. In such situations individuals not only have to decide what action to take, they must carry out the motor act. Therefore, this study examined both reaction time and movement time. The authors are aware of only two previous studies that have examined the effect of exercise on both reaction time and movement time. Levitt and Gutin (1971) examined 20 participants' >-choice reaction time and movement time at rest and while walking/running on a treadmd at intensities which elicited heart rates of 115, 145, and 175 bpm. O n the reaction time task, participants faced a display of five lights and five buttons, in a semicircle. Each button was 1-in. in front of a light. Following a warning signal one of the lights would be illuminated. Participants were instructed to press the button in front of the ~Lluminatedlight as quickly as possible. The participant began the hand movement from a central position which was 5 in. from each button. Mean reaction time at 115 bpm was significantly slower than that at 175 bpm. There were no other significant differences for reaction time. The only significant result for movement time was speed at rest which was significantly slower than that at 175 bpm. Wilhams, Pottinger, and Shapcott (1985) compared reaction time and movement time of three different groups of participants (N=90). Group 1 undertook a verbal task before being tested on the reaction time and movement time tests, while Group 2 undertook an arm-cranlung activity that elicited a power output of 10 W. Group 3, also, carried out the arm-cranking task but at a power output of 75 W. The test was similar to that of Levitt and Gutin (1971) except that there were eight choices and the distance to be moved was 20 in. The performance of the groups did not differ significantly for either variable. The equivocal nature of the findings for choice reaction time in these two studies is in line with the findmgs for the effect of exercise on the performance of, what Humphreys and Revelle (1984) termed, information transfer tasks, i.e., tasks which require the recognition of an unambiguous stimulus followed by a compatible response, i.e., the button to be depressed was the one corresponding to the illuminated light (Tomporowski & Ellis, 1986; McMorris & Graydon, 2000). For tasks that require the use of short-term memory, results have shown unequivocally that heavy exercise induces an improvement in reaction time (McGlynn, L a u g h h , & Bender, 1977; McGlynn, L a u g h h , & Rowe, 1977; McMorris & Graydon, 1996a, 1996b, 1997a, 1997b; A r c e h , Delignitres, & Brisswalter, 1998; McMorris, Myers, MacGillivary, Sexsmith, Fallowfield, Graydon, & Forster, 1999). In the present study the cognitive task was a noncompatible response time task, designed
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T. McMORRIS, ET AL.
to place a greater demand on short-term memory than those used in the Levitt and Gutin (1971) and Williams, et al. studies (1985), which were information-transfer tasks. Such a task was chosen because mhtary and sports situations generally include the use of short-term memory rather than simply being information-transfer tasks. The present study, also, differed from these studies in two other significant ways. Williams, et al. (1985) did not take into account individual differences in fitness. Power outputs of 10 W and 75 W are undoubtedly different, but the amount of difference experienced by the participants would be dependent on what percentage of the individual's maximum power output is represented by each workload. Similarly, in the Levitt and Gutin study (1971) the key factor is the percentage of maximum heart rate rather than the actual heart rate. Therefore, in the present study participants were tested at rest and while exercising at 70% and 100% of their own maximum power output. The use of exercise at maximal intensity is another way in which the present study differs from the previous studies. As stated earlier, research into the effect of incremental exercise on short-term memory tasks has unequivocally demonstrated a significant improvement in performance from rest to that during exercise a t maximum power output. In such tasks, the participant has only to prepare a cognitive response. When the response also requires a motor act, opto-motor integration includes not only perception and decision making but also preprogramming of a motor response, thus making it a more complex task than in the previous studies where the response was vocal or a finger depression. The present study set out to examine the effect of incremencal exercise on choice reaction time when the task required a motor response, as this is more realistic in real Me situations. The present study also set out to examine the effect of moderate and maximal intensity exercise on movement time in a response time task. Levitt and Gutin (1971) reported a positive effect for movement time during exercise at 175 bpm. It remains to be seen whether this improvement in performance would continue as exercise intensity increases or whether an invertedU effect would be demonstrated, as would be suggested by arousal-performance theories (e.g., Kahneman, 1973; Humphreys & Revelle, 1984). While reaction time and movement time are of importance in such a task, so is accuracy, i.e., the participants' abdity to choose the correct answer. With the exception of one study (McMorris & Graydon, 1997a), no significant effect of exercise on accuracy of performance in short-term memory tasks has been shown (McGlynn, L a u g h h , & Bender, 1977; McGlynn, L a u g h h , & Rowe, 1977; McMorris & Graydon, 1996a, 1996b, 1997b; Arcelin, et al., 1998; McMorris, et a/., 1999). Although these findings are quite consistent, they do not seem to con-
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firm the arousal-performance theories (e.g., Yerkes & Dodson, 1908; Kahneman, 1973; Humphreys & Revelle, 1984), which all predict an inverted-U effect. Indeed, Humphreys and Revelle explicitly stated that tasks requiring the use of short-term memory are the most likely to be inhibited by high arousal. Eysenck (1992) claimed that well learned tasks might be performed without disruption under high stress. This may account for the results of McMorris and associates (McMorris & Graydon, 1996a, 1996b, 1997a, 1997b; McMorris, et al., 1999) who tested soccer players on soccer-specific tests. It does not, however, account for the findings of McGlynn, L a u g h h , and Bender (1977), McGlynn, L a u g h h , and Rowe (1977), and Arcelm, et al. (1998), who used tasks not familiar to the participants. As McGlynn and associates did not report examining habituation effects, it is possible that this affected their results. Moreover, Arcelin, et al. did not include maximal intensity exercise in their study. Therefore, it was decided to include the examination of a possible effect of incremental exercise on accuracy of performance in the present study. Theoretically an inverted-U effect would be expected. The secondary purpose of this study was to examine the ability of increases, from resting values, in plasma concentrations of adrenahe and noradrenaline, and power output to predict changes in reaction time and movement time. During exercise, feedback from the cardiorespiratory system and muscles is detected by the Sympathetic Nervous System, which then stimulates secretion of the catecholamines, adrenaline, and nor-adrenalme, by the adrenal medulla (Pliszka, McCracken, & Maas, 1996). These catecholamines are involved in a wide range of activities, in the Peripheral Nervous System, that regulate responses to exercise (Genuth, 1998; Astrand & Rodahl, 2002). However, peripheral concentrations of adrenahe and nor-adrenaline are also known to increase due to sympathetic nervous system responses to emotional and cognitive stress (Frankenhaeuser & Jarpe, 1963; Sothmann, Hart, & Horn, 1991). This fact led Cooper (1973) and Chmura, Nazar, and Kaciuba-Usciko (19941, using a somewhat circular argument, to claim that, when one exercises, peripheral increases in catecholamine concentrations would lead to increases in central nervous system concentrations. This may occur in one of two ways. Studies with animals have shown that peripherally circulating adrenaline and nor-adrenalme cross the blood brain barrier during exercise (Brown, Payne, K m , Moore, Krebs, & Martin, 1979; McGaugh, 1983). While this may occur in humans, it is thought that the most Uely reason for a central nervous system increase is that activation of the sympathetic nervous system, by peripheral feedback, stimulates secretion of nor-adrenahe in the adrenal cortex, hypothalamus, and brain stem (Genuth, 1998). This is particularly important because nor-adrenaline is the major neurotransmitter in the nor-adrenergic pathway, which controls the efficiency of workmg memory -
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(Etnier & Landers, 1995). This is the basis of the argument for exercise affecting the efficiency of cognitive functioning. There is some circumstantial evidence to support the argument that peripheral and central concentrations are highly related. During exercise, plasma concentrations of adrenaline and nor-adrenalme increase exponentially, and the point at which a significant change in the rate of increase of concentrations is observed is termed the catecholamine threshold (Hughson, Green, & Sharratt, 1995). Chrnura, et a/. (1994) and McMorris, et 01. (1999) found significant decreases in reaction time following the thresholds, thus supplying support for the notion that peripheral increases are related to central nervous system increases. This, however, does not prove that the peripheral concentrations are indicative of central nervous system concentrations. It could be that more central factors, e.g., perceptions of stress or discomfort, induce nor-adrenaline secretion in the central nervous system. It is the activation of the sympathetic nervous system, due to peripheral responses to exercise, that is of interest here. If exercise directly affects cognitive performance, i.e., plasma catecholamines cross the blood brain barrier or directly stimulate secretion i n the central nervous system, one would expect plasma concentrations to be significant predictors of response time, particularly the reaction time component. It may, however, be that the effect of exercise on cognition is indirect. Several authors (e.g., Parfitt, Hardy, & Pates, 1995; Kerr, Fujiyima, & Campano, 2002) have argued that exercise is a stressor and as such directly induces secretion of catecholamines in the central nervous system. This could account for the findings of Brisswalter, Arcelm, Audiffren, and Delignitres (1997) who showed that subjects, who were used to exercising, showed a linear improvement in reaction time during incremental exercise while subjects, who were not used to exercising, showed an inverted-U effect. This was despite the fact that all were exercising at the same percentage of their own maximum power output. The participants, who were used to exercising at maximal intensity, probably did not perceive the discomfort as threatening. Therefore there would be no or little direct effect on the sympathetic nervous system. However, i£ the subjects, unused to exercising, had an affective response that was negative, there would be central nervous system secretion of-nor-adrenalme. IF this is the case then plasma concentrations of adrenalme and nor-adrenalme will not be significant predictors of reaction time and movement time. Only one study (Peyrin, Pequinot, Lacour, & Fourcade, 1987) attempted ,to assess increases in plasma concentrations of adrenaline and nor-adrendine to predict cognitive functioning on a short-term memory task. Adrenah e and nor-adrenalme did not significantly predict performance. Peyrin, et al. did, however, find that adrenaline and metadrenaline combined and 3 methoxy 4-hydroxy phenylglycol (MHPG) were significant predictors for an
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information-transfer task, RZ=.36 for both variables. The authors examined actual catecholamine concentrations and performance rather than changes from the at rest baseline measures. It would appear that changes in catecholamine concentrations and response times, rather than actual concentrations and response times, would be the important factors as each individual has different baseline values for each variable. Therefore, in the present study we examined the ability of increases in plasma catecholamine concentrations to predict changes in reaction time and motor time. While the major concern of the secondary purpose of this study was the effect of plasma concentrations of adrenahe and nor-adrenaline on reaction time and movement time, the a b h t y of power output to predct cognitive performance was also examined It is increases in power output that cause adrenal medulla secretion of adrenahe and nor-adrenalme Increases in power output also induce other changes that may be more mportant than adrenaline and nor-adrenaline. It is outside the scope of this study to examine all the possible factors, but if power output significantly predicts reaction time or movement time, but the catecholamines do not, then this would indicate that other factors are responsible. If none of the variables can pre&ct performance then it would appear more likely that the effect of exercise on response time is indirect rather than direct. To summarize, the primary purpose of this study was to examine the effect of exercising at 70% and 100% maximum power output on reaction time and movement time in a noncompatible response time task. The study also examined whether increases in plasma concentrations of adrenaline and nor-adrenaline ~redictedreaction and movement times. The abhty of power output to predict these variables was also measured, as it was thought that ~ e r i ~ h e r factors al other than catecholamine increases might affect cognitive pertormance.
Participants Participants ( N = 9 ) were male undergraduate and postgraduate Sports Science students, mean age 22.2 (SD=2.1) yr., mass 68.02 (SD=27.42) kg, height 1.80 (SD =5.95) m. All were volunteers and signed informed consent forms. Prior to undertakmg the test they completed medcal questionnaires. These were repeated prior to each exercise bout. Participants were informed that they were free to leave the experiment at any time. Noncompatible Choice Response Time Test Participants sat on a Monark 814E (Monark Crescent, Varberg, Sweden) cycle ergometer, on the handle bars of which was mounted a board containing four lights, numbered 1-4, with a button directly below each
light. The buttons were numbered 1-4, with number 1 being below light number 1 and so on. The participants depressed a small lever, 6 cm. long. The lever was 8 cm from the center of the handlebars on the same side as the participant's preferred hand. Participants were told to keep the lever depressed until they saw one of the lights illuminated. On seeing the light illuminated they were to release the lever and press the appropriate button. Button 3 was to be pressed when Light 1 was ~Lluminated,Button 4 for Light 2, Button 1 for Light 3 , and Button 2 for Light 4. For right-handed participants, Button 1 was 30.5 cm from the lever, Button 2 was 28 cm away, Button 3 was 27 cm away, and Button 4 was 27 cm away. The distances were reversed for left-handed participants. Releasing the lever measured reaction time and the time from releasing the lever to pressing the button was movement time. The dependent variables were mean reaction time, mean movement time, and number of errors, the amount of times the participant pressed the wrong button. A pilot study showed that it took between 120 and 160 trials to eluninate a learning or habituation effect. As the test was to be undertaken in three conditions, a p r e h i n a r y study was carried out to determine the reliabhty of the test. Ten participants in the reliabdity study were also sports science undergraduate and postgraduate students. Following 160 habituation trials, the participants undertook three sets of 20 trials. Each set of 20 constituted one test. In each set of 20 there were five responses to each of the four buttons. Participants were not informed of this, but it was necessary as the distances from the lever to the buttons differed for each button. This study was necessary to ensure that there would be no further habituation effect following a plateau after 160 practice trials. Maxrinu~nPower Output Test
Participants undertook an incremental exercise test to exhaustion to determine their maximum power output. The test followed the protocol described by McMorris and Keen (1994), but with the addition that venous blood samples were drawn. Prior to participants commencing the maximum power output test their heighr. and body mass were recorded and a cannula was inserted into a prominent forearm vein, by a State Registered Nurse. The participants then sat on a Monark 814E cycle ergometer, for 5 min. prior to exercising, to allow resting measures to be taken. A 5-ml blood sarnple was taken at rest, after 4-min. exercise, and then every 2 min. thereafter until cessation of the test. Samples were taken by a trained phlebotomist. The sample was immediately dispensed into lithium heparii tubes and placed on ice until subsequent analysis. The cannula was kept potent by flushing with 5 ml of sterile saline. Whole blood lactate concentrations were ascertained with an automated lactate analyzer (2300 StatPlus analyzer, Yel-
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low Springs Industries, USA) and 50 pl of ethyleneglycolbis(oxonitrilo)tetraecetic acid-glutathione anti-oxidant was added. The samples were then centrifuged for 5 min. at 1900 g in a refrigerated centrifuge (8000 series, Centurion Scientific, Ford, UK), after which the plasma was removed and stored at -85°C. Plasma adrenalme and nor-adrenaline concentrations were analyzed using liquid/liquid clean up procedure followed by separation using h~gh-performanceliquid chromatography and electrochemical detection (Forster &. Macdonald, 1999). Heart rate was continuously monitored by short-range telemetry (Sports Tester PE-3000 monitor, Polar Electro, Kernpele, Fmland) and recorded at rest and every 2 min. during exercise. The participants commenced the test at a resistance of 35 W to which 28 W were added every 2 min. Participants were instructed to pedal at a cadence of 70 rpm (actual cadence was recorded every 2 min.). The test was terminated when the participant was unable to maintain the required pedal cadence. Mean power recorded over the final 2 min. was taken to represent maximum power output (McMorris & Keen, 1994). Seventy percent rnaxin~umpower output was calculated. A d r e n a h e and nor-adrenalme thresholds were calculated using a modified log-log technique (Beaver, Wasserman, & Whipp, 1985).
Procedure One week after completing the maximum power output test, participants undertook the noncompatible choice-response timed test at rest, while exercising at the power outputs calculated to elicit 70% and 100% maximum power output. To control for possible circadian rhythm and dietary effects, each participant undertook the test at the same time of day as in the maximum power output test and was instructed to follow the same diet as the week previous. O n entering the laboratory participants were fitted with the heart-rate monitor and sat on the cycle ergometer prior to heart rate being assessed. They were given 160 habituation trials in four blocks of 40 trials, with 1-min. rest in between each block. For the actual test they were examined on 20 trials. The first set of trials was undertaken 1 min. after completing the habituation trials. This was the at rest condition. On completion of the first test, participants began cyclmg. The protocol was the same as for the maximum power output test except that blood samples were not taken. Also, for some participants, slight alterations in the load increments had to be made to ensure that each participant was workmg at the required power output to elicit 70% maximum power output. When participants reached this exercise level, they undertook the second set of 20 trials. Participants continued c y c h g throughout. The same procedure was carried out when the participants reached their previously determined maximum power output.
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Blood samples were not taken during the response time test because it was impractical for the participant to give blood at the same time that he was being tested. It was not deemed necessary to take blood during this test as catecholamine responses, at different exercise intensities, will not differ significantly from one test to another unless the participant has undertaken a rigorous training program (Sothmann, et al., 1991) or is in an altered physiological state, e.g., hypoxia (Hughson, e t al., 1995).
Statistical Treatment Reliability of the noncompatible response time test was measured by the Intraclass test of reliability by analysis of variance (Baumgartner, 1989). Comparison of performance on the noncompatible response time test a t rest, during exercise at 70% and 100% maximum power output was examined by a repeated-measures multivariate analysis of variance, with reaction time and movement time as the dependent variables. Follow-up separate univariate repeated-measures analyses of variance were carried out on each of the dependent variables. Effect sizes for the multivariate analysis of variance and analyses of variance were calculated by the ~1~method. To examine differences between each of the conditions post hoc Tukey tests were undertaken. Effect sizes for the post hoc tests were measured using Cohen d. Power at p = .05 (1988) was also calculated. Hierarchical multiple regression analyses were used to examine the ability of changes from rest to during exercise, in nor-adrenaline and adrenalme plasma concentrations and power output during exercise, to act as predctor variables for reaction time and movement time during exercise. As the number of participants is small, effect sizes and statistical power are reported for nonsignificant ( p > .05) as well as significant results, in accordance with Cohen (1994). Cohen recommended this as the chances of a Type I1 error are high with such a small sample. Similarly, under normal circumstances a population of nine would be considered too small for undert a h g a hierarchical multiple regression with two independent variables. However, as each participant was examined in two different conditions, this gave a population of 18, which would be acceptable (Clark-Carter, 1997). Donner and C u n n ~ n ~ h a (1984) m point out that the use of multiple measures violates the assumption of multiple regression from the same p~rr~cip;mts analyses that the population is independent. According to Donner and Cunningham, the use of multiple measures results in inflation in the standard error and, therefore, a greater ldcelihood of a Type I error. In such circumstances, Donner and Cunningham recommended that the residual variation between subjects should be compared to the residual variation within subjects, and were there a significant difference between the two, then the Inflation Factor of Scott and Holt (1982) should be applied to correct for the use of nonindependent subjects.
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RESULTS The results of the preluninary study showed that there were very few errors made. One participant had two errors in the second set of trials and one in the first set. Another participant had one error in the second set of trials. There were no other errors; therefore, reliabhty for number of errors was not calculated. Performances on Trials 1-3 were compared using a multivariate analysis of variance. There were no significant differences. Intraclass reliability coefficients of .81 and .98 were found for reaction time and movement time, respectively. The mean heart rates at rest and during exercise at 70% and 100% maximum power output were 68 (SD= 9), 150 (SD = 1I), and 179 (SD= 11) bpm, respectively. The mean power output at 70% maximum power output was 196.8 W (SD= 18.7) and 280.8 W (SD=30.6) at 100% maximum power output. Mean adrenaline and nor-adrenalme plasma concentrations at rest, 70%, and 100% maximum power output are shown in Table 1. TABLE 1 IMFANSAND STANDARDDEVIATIONS OF PLASMA ADRENALINE A N D NOR-ADRENALINE CONCENTRATIONS ( N M O L . L-I) AT REST A N D DURING ~ R C I S AT E 70% A N D 100% MAXIMUM POWER OUTPUT
M
SD
70% Maximum Power Output
M
SD
M
SD
0.40 2.34
0.27 0.64
0.88 4.72
0.48 1.32
4.83 21.56
3.81 10.97
Rest
Adrenaline Nor-adrenaline
100% Maximum Power Output
The number of errors were few. One participant made three errors at rest and one in each of the other two conditions. Only one other participant made an error. Therefore, number of errors was not included in the statistical treatment. The multivariate analysis of variance indicated a significant effect for exercise intensity (A,,,,=.319, F=5.79, p
