Perceptual & Motor Skills: Learning & Memory 2014, 118, 1, 63-72. © Perceptual & Motor Skills 2014
INFLUENCE OF ACUTE HIGH-INTENSITY AEROBIC INTERVAL EXERCISE BOUT ON SELECTIVE ATTENTION AND SHORT-TERM MEMORY TASKS1, 2 CHRISTIANO R. R. ALVES, VICTOR H. TESSARO, LUIS A. C. TEIXEIRA, KARINA MURAKAVA, HAMILTON ROSCHEL, BRUNO GUALANO, AND MONICA Y. TAKITO School of Physical Education and Sport University of São Paulo, Brazil Summary.—Acute moderate intensity continuous aerobic exercise can improve specific cognitive functions, such as short-term memory and selective attention. Moreover, high-intensity interval training (HIT) has been recently proposed as a time-efficient alternative to traditional cardiorespiratory exercise. However, considering previous speculations that the exercise intensity affects cognition in a U-shaped fashion, it was hypothesized that a HIT session may impair cognitive performance. Therefore, this study assessed the effects of an acute HIT session on selective attention and short-term memory tasks. 22 healthy middle-aged individuals (M age = 53.7 yr.) engaged in both (1) a HIT session, 10 1 min. cycling bouts at the intensity corresponding to 80% of the reserve heart rate interspersed by 1 min. active pauses cycling at 60% of the reserve heart rate and (2) a control session, consisting of an active condition with low-intensity active stretching exercise. Before and after each experimental session, cognitive performance was assessed by the Victoria Version of the Stroop test (a selective attention test) and the Digit Span test (a short-term memory test). Following the HIT session, the time to complete the Stroop “Color word” test was significantly lower when compared with that of the control session. The performances in the other subtasks of the Stroop test as well as in the Digit Span test were not significantly different. A HIT session can improve cognitive function.
Selective attention can be defined as the prioritization of information for further processing (Stroop, 1935; Scerif, 2010), while short-term memory is the capacity of holding information in mind for a short period of time (Cowan & AuBuchon, 2008). Both the selective attention and the shortterm memory are important cognitive functions implicated in a variety of daily living activities (Lewandowsky, Oberauer, & Brown, 2009; Scerif, 2010). The positive relationship between cognitive function and physical fitness has been known for decades (Spirduso, 1975; Hillman, Erickson, & Kramer, 2008). There is a consistent body of literature showing that an acute bout of aerobic exercise can improve specific cognitive functions, such as short-term memory and selective attention (Brisswalter, Collardeau, & René, 2002; TomAddress correspondence to Christiano R. R. Alves, Av. Prof. Mello Moraes, 65 – Cidade Universitária, 05508-030, São Paulo, SP, Brazil or e-mail ([email protected]). 2 All authors declare no conflict of interest. 1
DOI 10.2466/22.06.PMS.118k10w4
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porowski, 2003; Lambourne & Tomporowski, 2010; Yanagisawa, Dan, Tsuzuki, Kato, Okamoto, Kyutoku, et al., 2010; McMorris, Sproule, Turner, & Hale, 2011). However, an inverted U-relationship has been observed between the activation level of the central nervous system and the exercise workload, suggesting that the intensity of the exercise is a key factor in the regulation of exercise-induced cognitive responses (Brisswalter, Collardeau, & René, 2002; Kashihara, Maruyama, Murota, & Nakahara, 2009). In this regard, an acute, moderate intensity continuous aerobic exercise can promote a beneficial effect on speed processing, selective attention, and aspects of inhibitory control (Hogervorst, Riedel, Jeukendrup, & Jolles, 1996; Yanagisawa, et al., 2010; Alves, Gualano, Takao, Avakian, Fernandes, Morine, et al., 2012). Conversely, high-intensity exercise (i.e., intensity above the anaerobic threshold) may decrease the cognitive performance in some (e.g., reaction time; Chmura, Nazar, & Kaciuba-Uściłko, 1994) but not all tasks (e.g., visual capacity; Bard & Fleury, 1978). Tomporowski (2003) suggested that the high-intensity exercise-induced cognition impairment may be due to mental fatigue. Nonetheless, the effects of a high-intensity exercise interspersed by recovery intervals (i.e., socalled high-intensity interval training – HIT) on cognitive function are little known. HIT describes physical exercise, i.e., characterized by brief, intermittent bursts of vigorous activity, interspersed by periods of rest or low-intensity exercise. HIT has been recently proposed as a time-efficient alternative to traditional cardiorespiratory exercise. An efficient HIT protocol consists of 10 × 60 sec. work bouts at a constant-load intensity that elicits ∼90% of maximal heart rate (HR; that correspond to ∼80% of the reserve HR), interspersed with 60 sec. of recovery (Gibala, Little, Macdonald, Hawley, 2012). Some evidence indicates that HIT can induce rapid phenotypic changes in both the cardiopulmonary system (Kemi & Wisloff, 2010; Dunham & Harms, 2011; Smart, Dieberg, & Giallauria, 2013) and in the skeletal muscle (Little, Safdar, Wilkin, Tarnopolsky, & Gibala, 2010) that resemble those of traditional endurance training (i.e., moderate-intensity continuous aerobic exercise). However, studies investigating the effects of HIT on cognitive function are scarce. In this respect, Lemmink and Visscher (2005) did not observe changes on reaction times in eight trained soccer players who undertook an 8 min. HIT protocol (40 sec. of high-intensity exercise interspersed with 20 sec. of low-intensity exercise). Winter, Breitenstein, Mooren, Voelker, Fobker, Lechtermann, et al., (2007) reported improvements on learning speed in 30 healthy young males who performed a HIT session comprised by two sprints at increasing speed separated by a 2 min. break. The authors attributed their findings to elevated levels of BDNF and catecholamines (i.e.,
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dopamine, epinephrine, norepinephrine) which, along with increased cerebral blood flow, has been suggested to be the underlying mechanisms of acute exercise-induced cognitive function activation (Cooper, 1973; McMorris, 2009). However, it is noteworthy that the exercise protocols applied in the aforementioned may not have been sufficiently intensive to affect executive function negatively. Given that traditionally a HIT protocol is higher-intensity, one could expect an impairment in cognitive function after a single session of this type of exercise. Hypothesis. HIT may have negative effects on cognition, so an acute HIT session was expected to worsen selective attention and short-term memory in healthy middle-aged adults. METHOD Participants A convenience sample was recruited from a community center-supervised physical fitness program. A convenience sample of 22 healthy volunteers were selected (M age = 53.7 yr., SD = 4.7; M body mass index = 25.7, SD = 3.1; 9 men, 13 women). Volunteers were excluded if they were smokers or were diagnosed with depression, neuromuscular, cerebral, cardiovascular, or color vision dysfunction at medical examination. Additionally, none of them were taking any drugs at least three months prior to the beginning of the experimental protocol. The study was approved by the local ethical committee, and informed consent was obtained from all of the volunteers. Study Design This is a randomized, counterbalanced, and cross-over trial. The volunteers were required to perform one familiarization session to the cognitive tasks. One week after these procedures, the volunteers randomly performed two experimental sessions on separate occasions (seven days apart). The experimental sessions were: (1) a HIT session and (2) a control session. Cognitive function was assessed before (PRE) and immediately after (POST) each experimental session (Fig. 1). Cognitive Function Tasks Considering that both selective attention and short-term memory are important cognitive functions implicated in a variety of daily living activities (Lewandowsky, et al., 2009; Scerif, 2010), the Victoria version of the Stroop test was applied as well as the Digit Span test in the current study. The Victoria version of the Stroop test (Spreen & Strauss, 1998) is a short version that uses three conditions as follows: naming the color of dots (i.e., “Color” condition), of neutral words (i.e., “Non-color word”
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FIG. 1. Experimental design. HIT = high-intensity interval training.
condition), and of color words printed in incongruent colors (i.e., “Color word” condition). Each condition contains 24 items. This is a paperbased task with four different possible colors. In the “Non-color word” and mainly in the “Color word” condition, the normal tendency to read the word, rather than the color of the ink in which the words are printed, elicits a significant slowing in reaction time called interference. Consequently, the Stroop test is considered a valid measure of selective attention and the susceptibility to interference from conflicting stimuli (Stroop, 1935; Spreen & Strauss, 1998; Alvarez & Emory, 2006; Sibley, Etnier, & Le Masurier, 2006; Bayard, Erkes, & Moroni, 2011). Performance was assessed based on both the time to complete each condition and the number of errors. The interference effect was calculated as the time for completion in the conditions “Color word” minus “Color” (Spreen & Strauss, 1998). The Digit Span test was applied to assess short-term memory (Wechsler, 1987). The test consists of two subtasks, one of which requires the participant to repeat orally a sequence of digits forward and another one that requires that the individual repeat a sequence backwards. In the two subtasks, the number of digits increases progressively (e.g., 16; 283; 5273; 26158; 715294; 8472936). The maximal number of digits in both tasks is limited to seven. Performance was assessed based on the number of digits that the volunteers could repeat. The Stroop test was always administered prior to the Digit Span test by the same trained researcher. Experimental Sessions The acute HIT session consisted of a 3 min. warm-up (cycling at 60% of the reserve HR) on the cycle ergometer (Monark®, Brazil), followed by ten 1 min. cycling bouts at the intensity corresponding to 80% of the heart rate (HR) reserve (i.e., HR reserve = HR max – HR min). The 1 min. bouts were interspersed by 1 min. active pauses (i.e., with participants cycling at 60% of the reserve HR). After the completion of the ten 1 min. bouts, a 2 min. cool-down period with participants cycling at 60% of the reserve HR took place (adapted from Gibala, et al., 2012). The control session was
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designed to be an active-comparator session. It comprised 10 min. of instructions about the benefits of regular exercise training on overall health (e.g., quality of life, cardiovascular function, and weight management), followed by 15 min. of low-intensity active stretching exercise. No specific instructions about the effects of exercise training on cognition were provided to avoid any “placebo” effect. All of the procedures were conducted in the same setting and in the presence of a fitness professional. Heart rate was also monitored throughout the experimental sessions by a transmitter (model S810, Polar Electro Oy, Kempele, Finland). Statistical Analysis After the normality and homogeneity of the variance were confirmed, a mixed-model analysis for repeated-measures was conducted, considering condition (HIT, control) and time (PRE, POST) as fixed factors and subjects as a random factor. Whenever significant effects were found, a Tukey adjustment was used for multiple comparison purposes. The absolute change (pre- to post-test change) for the Stroop test (time and errors), Digit Span test (number of correct digits), and HR were also calculated. Student's t tests were used to compare the changes (post minus pre values) between groups. The effect size for the within-condition analysis (pre- to post-test changes) were calculated using Cohen's d (Cohen, 1988), where the difference between post- and pretest was divided by the pretest standard deviation. Significance was set at p < .05. RESULTS Table 1 shows the HR response in the experimental protocols. As expected, HR was significantly higher during and after (p < .001) the HIT when compared with the control session. Figure 2 illustrates performance on the Stroop test and the Digit Span test. No significant between-condition differences were observed at baseline (PRE) for both the Stroop and the Digit Span tests (p > .05), and no order-effects were observed in this study (p > .05). Mixed-model ANOVA showed a significant condition by time interaction (F1, 42 = 7.46, p = .009) in the time to complete the Stroop “Color word” test. However, the post hoc test indicated no between-group differences at the post-test (p = .78). Importantly, a significant within-condition effect was observed for the HIT (p = .0002; Cohen's d HIT = –0.53), but not for the control condition (p = .86; d Control = –0.12). In addition, changes analysis indicated that the time to complete the Stroop “Color word” test was significantly lower in the HIT session than in the control session (t = 2.52, p = .02). Furthermore, change analyses showed that the interference effect was significantly lower in the HIT section than in the control section (t = 2.34, p = .02).
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C. R. R. ALVES, ET AL. TABLE 1 HEART RATE AT BASELINE AND IN RESPONSE TO EXPERIMENTAL SESSIONS Participants
Heart Rate (HR), beats/min Resting HR
M
SD
68.45
8.73
50% of HR reserve
117.18
4.76
80% of HR reserve
146.32
3.99
Estimated maximal HR
166.23
4.74
Control Session
Exercise Session
M
SD
M
SD
HR before experimental condition
82.52
9.80
84.33
11.03
M HR of experimental condition
82.05
7.23
133.05
11.63*
HR after experimental condition 79.05 10.72 *Statistically different when compared to control condition.
100.24
14.33*
FIG. 2. Stroop test and Digit Span test performance. A, C, and E: M ± SD for time in “Color,” “Non-color word,” and “Color word” conditions, respectively. D and E: M ± SD for “Forward” and “Backward” conditions, respectively. *Absolute change statistically different between HIT and Control (p = .02). HIT = high-intensity interval training.
The mixed-model analyses indicated no significant between-condition differences in the time to complete the Stroop “Color” (F1, 42 = 1.02, p = .31) and the Stroop “Non-color word” tests (F1, 42 = 0.67, p = .41). Likewise, no significant differences were found by the absolute change analysis in relation to the Stroop “Color” (t = 1.01, p = .32; Cohen's d: HIT = –0.28,
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Control = 0.00) and the Stroop “Non-color word” (t = 0.86, p = .39; Cohen's d: HIT = –0.53, Control = –0.42) conditions. The number of errors was not significantly different between the HIT and control conditions in the Stroop “Color” (F1, 42 = 0.51, p = .48), the “Noncolor word” (F1, 42 = 0.14, p = .71), and the “Color word” tests (F1, 42 = 0.12, p = .73). Similarly, delta changes were not significantly different in the Stroop “Color” (t = 0.70, p = .49; Cohen's d: HIT = 0.00, Control = 0.64), the “Non-color word” (t = 0.37, p = .58; Cohen's d: HIT = –0.15, Control = 0.00), and the “Color word” tests (t = 0.41, p = .43; Cohen's d: HIT = 0.00, Control = –0.12). Mixed-model and delta analysis did not indicate any significant difference with respect to the number of correct digits in the Digit Span “Forward” (F1, 42 = 0.13, p = .72; t = 0.31, p = .72; Cohen's d: HIT = –0.05, Control: 0.06; respectively) and “Backward” tests (F1, 42 = 0.98, p = .32; t = 0.92, p = .65; Cohen's d: HIT = 0.08, Control = –0.10; respectively). DISCUSSION The objective of this study was to assess the effects of an acute HIT session on selected parameters of cognitive function (i.e., selective attention and short-term memory performance) in middle-aged adults. The main finding was that the HIT session improved the performance in the Stroop “Color Word” test, which has been thought to be a measure of selective attention and the susceptibility to interference from conflicting stimuli. Conversely, the HIT session did not improve the performance in the Digit Span “Forward” and “Backward” tests, both being considered as measures of short-term memory. The influence of the intensity of an acute bout of exercise on cognition has been previously examined (Brisswalter, et al., 2002; Tomporowski, 2003). Some authors have speculated that the exercise intensity affects cognitive performance in a U-shaped fashion, meaning that a moderate-intensity exercise would improve cognition whereas high-intensity exercise would impair cognitive performance (Brisswalter, et al., 2002; Kashihara, et al., 2009). In line with this assumption, Chmura, et al. (1994) observed gradual improvements in the reaction time (as assessed by an audio-visual five-choice reaction task) when participants exercised up to approximately 75% of their VO2 peak. Thereafter, the reaction time impaired rapidly, exceeding the resting value by 18%, suggesting that intensity seems to play a role in the effects of an acute exercise session on some aspects of cognitive performance. However, apparently in contrast to the U-shaped hypothesis, no deterioration in cognitive measures was detected after an acute session of HIT in the present study (actually, improvements in selective attention were noted), corroborating previous data involving higherintensity exercise, in which cognition parameters remained unaffected or even improved (Bard & Fleury, 1978; Lemmink & Visscher, 2005; Winter,
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et al., 2007). Therefore, one may argue that exercise intensity itself does not exert a major role in exercise-induced cognitive modulation. Possibly, exercise-induced fatigue plays a more important role on the cognitive responses to an exercise bout. Since we did not assess fatigue in this study, further studies should test the influence of exercise-induced fatigue upon cognition following a variety of exercise types (e.g., continuous, intermittent, strength, aerobic, combined-type) under different intensities and durations. Furthermore, no exercise-induced changes were observed in the “Forward” and the “Backward” subtasks of the Digit Span test, corroborating previous findings with depressive participants who undertook an acute moderate-intensity aerobic exercise session (Vasques, Moraes, Silveira, Deslandes, & Laks, 2011). However, it is important to note that the participants showed very high scores on the Digit Span test at baseline; thus, one cannot rule out the possibility of a “ceiling effect” for this test. A growing body of literature has supported the efficacy of HIT in promoting health-related benefits in several healthy and ill individuals, including improvements in body composition and cardiovascular system, and beneficial adaptation in skeletal muscle. Interestingly, the current results expand the current literature by showing that an acute HIT did not impair cognitive performance; on the contrary, HIT seems to be able to improve the performance on a selective attention task, but not on a shortterm memory one, in healthy middle-aged adults. REFERENCES
ALVAREZ, J. A., & EMORY, E. (2006) Executive function and the frontal lobes: a meta-analytic review. Neuropsychology Review, 16, 17-42. DOI: 1.1007/s11065-006-9002-x ALVES, C. R. R., GUALANO, B., TAKAO, P. P., AVAKIAN, P., FERNANDES, R. M., MORINE, D., & TAKITO, M. Y. (2012) Effects of acute physical exercise on executive functions: a comparison between aerobic and strength exercise. Journal of Sport and Exercise Psychology, 34, 539-549. BARD, C., & FLEURY, M. (1978) Influence of imposed metabolic fatigue on visual capacity components. Perceptual & Motor Skills, 47, 1283-1287. DOI: 10.2466/PMS.1978.47.3f. 1283 BAYARD, S., ERKES, J., & MORONI, C. (2011) Victoria Stroop test: normative data in a sample group of older people and the study of their clinical applications in the assessment of inhibition in Alzheimer's disease. Archives of Clinical Neuropsychology, 26, 653-661. DOI: 1.1093/arclin/acr053 BRISSWALTER, J., COLLARDEAU, M., & RENÉ, A. (2002) Effects of acute physical exercise characteristics on cognitive performance. Sports Medicine, 32, 555-566. DOI: 10.2165/0000 7256-200232090-00002 CHMURA, J., NAZAR, K., & KACIUBA-UŚCIŁKO, H. (1994) Choice reaction time during graded exercise in relation to blood lactate and plasma catecholamine thresholds. International Journal of Sports Medicine, 15, 172-176. DOI: 10.1055/s-2007-1021042 COHEN, J. (1988) Statistical power analysis for the behavioral sciences. (2nd ed.) Hillsdale, NJ: Lawrence Erlbaum Associates.
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COOPER, C. J. (1973) Anatomical and physiological mechanisms of arousal, with special reference to the effects of exercise. Ergonomics, 16, 601-609. DOI: 10.1080/ 00140137308924551 COWAN, N., & AUBUCHON, A. M. (2008) Short-term memory loss over time without retroactive stimulus interference. Psychonomic Bulletin Review, 15, 230-235. DUNHAM, C., & HARMS, C. A. (2011) Effects of high-intensity interval training on pulmonary function. European Journal of Applied Physiology, 112, 3061-3068. DOI: 2097/ 4133 GIBALA, M. J., LITTLE, J. O., MACDONALD, M. J., & HAWLEY, J. A. (2012) Physiological adaptations to low-volume, high-intensity interval training in health and disease. The Journal of Physiology, 590, 1077-1084. DOI: 0.1113/jphysiol.2011.224725 HILLMAN, C. H., ERICKSON, K. I., & KRAMER, A. F. (2008) Be smart, exercise your heart: exercise effects on brain and cognition. Nature Reviews Neuroscience, 9, 58-65. DOI: 10.1038/nrn2298 HOGERVORST, E., RIEDEL, W., JEUKENDRUP, A., & JOLLES, J. (1996) Cognitive performance after strenuous physical exercise. Perceptual & Motor Skills, 83, 479-488. DOI: 10.2466/pms.1996.83.2.479 KASHIHARA, K., MARUYAMA, T., MUROTA, M., & NAKAHARA, Y. (2009) Positive effects of acute and moderate physical exercise on cognitive function. Journal of Physiological Anthropology, 28, 155-164. DOI: 10.2114/jpa2.28.155 KEMI, O. J., & WISLOFF, U. J. (2010) High-intensity aerobic exercise training improves the heart in health and disease. Journal of Cardiopulmonary Rehabilitation and Prevention, 30, 2-11. DOI: 10.1097/HCR.0b013e3181c56b89 LAMBOURNE, K., & TOMPOROWSKI, P. (2010) The effect of exercise-induced arousal on cognitive task performance: a meta-regression analysis. Brain Research, 23, 12-24. DOI: 10.1016/j.brainres.2010.03.091 LEMMINK K. A. P. M., & VISSCHER, C. (2005) Effect of intermittent exercise on multiplechoice reaction times of soccer players. Perceptual & Motor Skills, 100, 85-95. DOI: 10.2466/PMS.100.1 LEWANDOWSKY, S., OBERAUER, K., & BROWN, G. D. (2009) No temporal decay in verbal shortterm memory. Trends in Cognitive Science, 13, 120-126. DOI: 10.1016/j.tics.2008.12.003 LITTLE, J. P., SAFDAR, A., WILKIN, G. P., TARNOPOLSKY, M. A., & GIBALA, M. J. (2010) A practical model of low-volume high-intensity interval training induces mitochondrial biogenesis in human skeletal muscle: potential mechanisms. The Journal of Physiology, 588, 1011-1022. DOI: 10.1113/jphysiol.2009.181743 MCMORRIS, T., SPROULE, J., TURNER, A., & HALE, B. J. (2011) Acute, intermediate intensity exercise, and speed and accuracy in working memory tasks: a meta-analytical comparison of effects. Physiology & Behavior, 102, 421-428. DOI: 10.1016/j.phys beh.2010.12.007 MCMORRIS, T. (2009) Exercise and decision-making in team games. In T. McMorris, P. D. Tomporowski, & M. Audiffren (Eds.), Exercise and cognitive function. Chichester, UK: Wiley-Blackwell. Pp. 179-192. SCERIF, G. (2010) Attention trajectories, mechanisms and outcomes: at the interface between developing cognition and environment. Developmental Science, 13, 805-812. DOI: 10.1111/j.1467-7687.2010.01013.x SIBLEY, B. A., ETNIER, J. L., & LE MASURIER, G. C. (2006) Effects of an acute bout of exercise on cognitive aspects of Stroop performance. Journal of Sport and Exercise Psychology, 28, 285-299.
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SMART, N. A., DIEBERG, G., & GIALLAURIA, F. (2013) Intermittent vs continuous exercise training in chronic heart failure: a meta-analysis. International Journal of Cardiology, 116(2), 352-358. SPIRDUSO, W. W. (1975) Reaction and movement time as a function of age and physical activity level. Journal of Gerontology, 30, 435-440. SPREEN, O., & STRAUSS, E. (1998) A compendium of neuropsychological tests. (2nd ed.) New York: Oxford Univer. Press. STROOP, J. R. (1935) Studies of interference in serial verbal reactions. Journal of Experimental Psychology, 18, 643-662. DOI: 10.1037/h0054651 TOMPOROWSKI, P. D. (2003) Effects of acute bouts of exercise on cognition. Acta Psychologica, 112, 297-324. DOI: 10.1016/S0001-6918(02)00134-8 VASQUES, P. E., MORAES, H., SILVEIRA, H., DESLANDES, A. C., & LAKS, J. (2011) Acute exercise improves cognition in the depressed elderly: the effect of dual-tasks. Clinics, 66, 1553-1557. DOI: 10.1590/S1807-59322011000900008 WECHSLER, D. (1987) Wechsler memory scale–revised. New York: Psychological Corporation. Pp. 1-150. WINTER, B., BREITENSTEIN, C., MOOREN, F. C., VOELKER, K., FOBKER, M., LECHTERMANN, A., KRUEGER, K., FROMME, A., KORSUKEWITZ, C., FLOEL, A., & KNECHT, S. (2007) High impact running improves learning. Neurobiology of Learning and Memory, 87, 597609. DOI: 10.1016/j.nlm.2006.11.003 YANAGISAWA, H., DAN, I., TSUZUKI, D., KATO, M., OKAMOTO, M., KYUTOKU, Y., & SOYA, H. (2010) Acute moderate exercise elicits increased dorsolateral prefrontal activation and improves cognitive performance with Stroop test. Neuroimage, 50, 1702-1710. DOI: 1.1016/j.neuroimage.2009.12.023 Accepted December 16, 2013.
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INFLUENCE OF ACUTE HIGH-INTENSITY AEROBIC INTERVAL EXERCISE BOUT ON SELECTIVE ATTENTION AND SHORT-TERM MEMORY TASKS1, 2 CHRISTIANO R. R. ALVES, VICTOR H. TESSARO, LUIS A. C. TEIXEIRA, KARINA MURAKAVA, HAMILTON ROSCHEL, BRUNO GUALANO, AND MONICA Y. TAKITO School of Physical Education and Sport University of São Paulo, Brazil Summary.—Acute moderate intensity continuous aerobic exercise can improve specific cognitive functions, such as short-term memory and selective attention. Moreover, high-intensity interval training (HIT) has been recently proposed as a time-efficient alternative to traditional cardiorespiratory exercise. However, considering previous speculations that the exercise intensity affects cognition in a U-shaped fashion, it was hypothesized that a HIT session may impair cognitive performance. Therefore, this study assessed the effects of an acute HIT session on selective attention and short-term memory tasks. 22 healthy middle-aged individuals (M age = 53.7 yr.) engaged in both (1) a HIT session, 10 1 min. cycling bouts at the intensity corresponding to 80% of the reserve heart rate interspersed by 1 min. active pauses cycling at 60% of the reserve heart rate and (2) a control session, consisting of an active condition with low-intensity active stretching exercise. Before and after each experimental session, cognitive performance was assessed by the Victoria Version of the Stroop test (a selective attention test) and the Digit Span test (a short-term memory test). Following the HIT session, the time to complete the Stroop “Color word” test was significantly lower when compared with that of the control session. The performances in the other subtasks of the Stroop test as well as in the Digit Span test were not significantly different. A HIT session can improve cognitive function.
Selective attention can be defined as the prioritization of information for further processing (Stroop, 1935; Scerif, 2010), while short-term memory is the capacity of holding information in mind for a short period of time (Cowan & AuBuchon, 2008). Both the selective attention and the shortterm memory are important cognitive functions implicated in a variety of daily living activities (Lewandowsky, Oberauer, & Brown, 2009; Scerif, 2010). The positive relationship between cognitive function and physical fitness has been known for decades (Spirduso, 1975; Hillman, Erickson, & Kramer, 2008). There is a consistent body of literature showing that an acute bout of aerobic exercise can improve specific cognitive functions, such as short-term memory and selective attention (Brisswalter, Collardeau, & René, 2002; TomAddress correspondence to Christiano R. R. Alves, Av. Prof. Mello Moraes, 65 – Cidade Universitária, 05508-030, São Paulo, SP, Brazil or e-mail ([email protected]). 2 All authors declare no conflict of interest. 1
DOI 10.2466/22.06.PMS.118k10w4
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porowski, 2003; Lambourne & Tomporowski, 2010; Yanagisawa, Dan, Tsuzuki, Kato, Okamoto, Kyutoku, et al., 2010; McMorris, Sproule, Turner, & Hale, 2011). However, an inverted U-relationship has been observed between the activation level of the central nervous system and the exercise workload, suggesting that the intensity of the exercise is a key factor in the regulation of exercise-induced cognitive responses (Brisswalter, Collardeau, & René, 2002; Kashihara, Maruyama, Murota, & Nakahara, 2009). In this regard, an acute, moderate intensity continuous aerobic exercise can promote a beneficial effect on speed processing, selective attention, and aspects of inhibitory control (Hogervorst, Riedel, Jeukendrup, & Jolles, 1996; Yanagisawa, et al., 2010; Alves, Gualano, Takao, Avakian, Fernandes, Morine, et al., 2012). Conversely, high-intensity exercise (i.e., intensity above the anaerobic threshold) may decrease the cognitive performance in some (e.g., reaction time; Chmura, Nazar, & Kaciuba-Uściłko, 1994) but not all tasks (e.g., visual capacity; Bard & Fleury, 1978). Tomporowski (2003) suggested that the high-intensity exercise-induced cognition impairment may be due to mental fatigue. Nonetheless, the effects of a high-intensity exercise interspersed by recovery intervals (i.e., socalled high-intensity interval training – HIT) on cognitive function are little known. HIT describes physical exercise, i.e., characterized by brief, intermittent bursts of vigorous activity, interspersed by periods of rest or low-intensity exercise. HIT has been recently proposed as a time-efficient alternative to traditional cardiorespiratory exercise. An efficient HIT protocol consists of 10 × 60 sec. work bouts at a constant-load intensity that elicits ∼90% of maximal heart rate (HR; that correspond to ∼80% of the reserve HR), interspersed with 60 sec. of recovery (Gibala, Little, Macdonald, Hawley, 2012). Some evidence indicates that HIT can induce rapid phenotypic changes in both the cardiopulmonary system (Kemi & Wisloff, 2010; Dunham & Harms, 2011; Smart, Dieberg, & Giallauria, 2013) and in the skeletal muscle (Little, Safdar, Wilkin, Tarnopolsky, & Gibala, 2010) that resemble those of traditional endurance training (i.e., moderate-intensity continuous aerobic exercise). However, studies investigating the effects of HIT on cognitive function are scarce. In this respect, Lemmink and Visscher (2005) did not observe changes on reaction times in eight trained soccer players who undertook an 8 min. HIT protocol (40 sec. of high-intensity exercise interspersed with 20 sec. of low-intensity exercise). Winter, Breitenstein, Mooren, Voelker, Fobker, Lechtermann, et al., (2007) reported improvements on learning speed in 30 healthy young males who performed a HIT session comprised by two sprints at increasing speed separated by a 2 min. break. The authors attributed their findings to elevated levels of BDNF and catecholamines (i.e.,
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dopamine, epinephrine, norepinephrine) which, along with increased cerebral blood flow, has been suggested to be the underlying mechanisms of acute exercise-induced cognitive function activation (Cooper, 1973; McMorris, 2009). However, it is noteworthy that the exercise protocols applied in the aforementioned may not have been sufficiently intensive to affect executive function negatively. Given that traditionally a HIT protocol is higher-intensity, one could expect an impairment in cognitive function after a single session of this type of exercise. Hypothesis. HIT may have negative effects on cognition, so an acute HIT session was expected to worsen selective attention and short-term memory in healthy middle-aged adults. METHOD Participants A convenience sample was recruited from a community center-supervised physical fitness program. A convenience sample of 22 healthy volunteers were selected (M age = 53.7 yr., SD = 4.7; M body mass index = 25.7, SD = 3.1; 9 men, 13 women). Volunteers were excluded if they were smokers or were diagnosed with depression, neuromuscular, cerebral, cardiovascular, or color vision dysfunction at medical examination. Additionally, none of them were taking any drugs at least three months prior to the beginning of the experimental protocol. The study was approved by the local ethical committee, and informed consent was obtained from all of the volunteers. Study Design This is a randomized, counterbalanced, and cross-over trial. The volunteers were required to perform one familiarization session to the cognitive tasks. One week after these procedures, the volunteers randomly performed two experimental sessions on separate occasions (seven days apart). The experimental sessions were: (1) a HIT session and (2) a control session. Cognitive function was assessed before (PRE) and immediately after (POST) each experimental session (Fig. 1). Cognitive Function Tasks Considering that both selective attention and short-term memory are important cognitive functions implicated in a variety of daily living activities (Lewandowsky, et al., 2009; Scerif, 2010), the Victoria version of the Stroop test was applied as well as the Digit Span test in the current study. The Victoria version of the Stroop test (Spreen & Strauss, 1998) is a short version that uses three conditions as follows: naming the color of dots (i.e., “Color” condition), of neutral words (i.e., “Non-color word”
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FIG. 1. Experimental design. HIT = high-intensity interval training.
condition), and of color words printed in incongruent colors (i.e., “Color word” condition). Each condition contains 24 items. This is a paperbased task with four different possible colors. In the “Non-color word” and mainly in the “Color word” condition, the normal tendency to read the word, rather than the color of the ink in which the words are printed, elicits a significant slowing in reaction time called interference. Consequently, the Stroop test is considered a valid measure of selective attention and the susceptibility to interference from conflicting stimuli (Stroop, 1935; Spreen & Strauss, 1998; Alvarez & Emory, 2006; Sibley, Etnier, & Le Masurier, 2006; Bayard, Erkes, & Moroni, 2011). Performance was assessed based on both the time to complete each condition and the number of errors. The interference effect was calculated as the time for completion in the conditions “Color word” minus “Color” (Spreen & Strauss, 1998). The Digit Span test was applied to assess short-term memory (Wechsler, 1987). The test consists of two subtasks, one of which requires the participant to repeat orally a sequence of digits forward and another one that requires that the individual repeat a sequence backwards. In the two subtasks, the number of digits increases progressively (e.g., 16; 283; 5273; 26158; 715294; 8472936). The maximal number of digits in both tasks is limited to seven. Performance was assessed based on the number of digits that the volunteers could repeat. The Stroop test was always administered prior to the Digit Span test by the same trained researcher. Experimental Sessions The acute HIT session consisted of a 3 min. warm-up (cycling at 60% of the reserve HR) on the cycle ergometer (Monark®, Brazil), followed by ten 1 min. cycling bouts at the intensity corresponding to 80% of the heart rate (HR) reserve (i.e., HR reserve = HR max – HR min). The 1 min. bouts were interspersed by 1 min. active pauses (i.e., with participants cycling at 60% of the reserve HR). After the completion of the ten 1 min. bouts, a 2 min. cool-down period with participants cycling at 60% of the reserve HR took place (adapted from Gibala, et al., 2012). The control session was
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designed to be an active-comparator session. It comprised 10 min. of instructions about the benefits of regular exercise training on overall health (e.g., quality of life, cardiovascular function, and weight management), followed by 15 min. of low-intensity active stretching exercise. No specific instructions about the effects of exercise training on cognition were provided to avoid any “placebo” effect. All of the procedures were conducted in the same setting and in the presence of a fitness professional. Heart rate was also monitored throughout the experimental sessions by a transmitter (model S810, Polar Electro Oy, Kempele, Finland). Statistical Analysis After the normality and homogeneity of the variance were confirmed, a mixed-model analysis for repeated-measures was conducted, considering condition (HIT, control) and time (PRE, POST) as fixed factors and subjects as a random factor. Whenever significant effects were found, a Tukey adjustment was used for multiple comparison purposes. The absolute change (pre- to post-test change) for the Stroop test (time and errors), Digit Span test (number of correct digits), and HR were also calculated. Student's t tests were used to compare the changes (post minus pre values) between groups. The effect size for the within-condition analysis (pre- to post-test changes) were calculated using Cohen's d (Cohen, 1988), where the difference between post- and pretest was divided by the pretest standard deviation. Significance was set at p < .05. RESULTS Table 1 shows the HR response in the experimental protocols. As expected, HR was significantly higher during and after (p < .001) the HIT when compared with the control session. Figure 2 illustrates performance on the Stroop test and the Digit Span test. No significant between-condition differences were observed at baseline (PRE) for both the Stroop and the Digit Span tests (p > .05), and no order-effects were observed in this study (p > .05). Mixed-model ANOVA showed a significant condition by time interaction (F1, 42 = 7.46, p = .009) in the time to complete the Stroop “Color word” test. However, the post hoc test indicated no between-group differences at the post-test (p = .78). Importantly, a significant within-condition effect was observed for the HIT (p = .0002; Cohen's d HIT = –0.53), but not for the control condition (p = .86; d Control = –0.12). In addition, changes analysis indicated that the time to complete the Stroop “Color word” test was significantly lower in the HIT session than in the control session (t = 2.52, p = .02). Furthermore, change analyses showed that the interference effect was significantly lower in the HIT section than in the control section (t = 2.34, p = .02).
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C. R. R. ALVES, ET AL. TABLE 1 HEART RATE AT BASELINE AND IN RESPONSE TO EXPERIMENTAL SESSIONS Participants
Heart Rate (HR), beats/min Resting HR
M
SD
68.45
8.73
50% of HR reserve
117.18
4.76
80% of HR reserve
146.32
3.99
Estimated maximal HR
166.23
4.74
Control Session
Exercise Session
M
SD
M
SD
HR before experimental condition
82.52
9.80
84.33
11.03
M HR of experimental condition
82.05
7.23
133.05
11.63*
HR after experimental condition 79.05 10.72 *Statistically different when compared to control condition.
100.24
14.33*
FIG. 2. Stroop test and Digit Span test performance. A, C, and E: M ± SD for time in “Color,” “Non-color word,” and “Color word” conditions, respectively. D and E: M ± SD for “Forward” and “Backward” conditions, respectively. *Absolute change statistically different between HIT and Control (p = .02). HIT = high-intensity interval training.
The mixed-model analyses indicated no significant between-condition differences in the time to complete the Stroop “Color” (F1, 42 = 1.02, p = .31) and the Stroop “Non-color word” tests (F1, 42 = 0.67, p = .41). Likewise, no significant differences were found by the absolute change analysis in relation to the Stroop “Color” (t = 1.01, p = .32; Cohen's d: HIT = –0.28,
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Control = 0.00) and the Stroop “Non-color word” (t = 0.86, p = .39; Cohen's d: HIT = –0.53, Control = –0.42) conditions. The number of errors was not significantly different between the HIT and control conditions in the Stroop “Color” (F1, 42 = 0.51, p = .48), the “Noncolor word” (F1, 42 = 0.14, p = .71), and the “Color word” tests (F1, 42 = 0.12, p = .73). Similarly, delta changes were not significantly different in the Stroop “Color” (t = 0.70, p = .49; Cohen's d: HIT = 0.00, Control = 0.64), the “Non-color word” (t = 0.37, p = .58; Cohen's d: HIT = –0.15, Control = 0.00), and the “Color word” tests (t = 0.41, p = .43; Cohen's d: HIT = 0.00, Control = –0.12). Mixed-model and delta analysis did not indicate any significant difference with respect to the number of correct digits in the Digit Span “Forward” (F1, 42 = 0.13, p = .72; t = 0.31, p = .72; Cohen's d: HIT = –0.05, Control: 0.06; respectively) and “Backward” tests (F1, 42 = 0.98, p = .32; t = 0.92, p = .65; Cohen's d: HIT = 0.08, Control = –0.10; respectively). DISCUSSION The objective of this study was to assess the effects of an acute HIT session on selected parameters of cognitive function (i.e., selective attention and short-term memory performance) in middle-aged adults. The main finding was that the HIT session improved the performance in the Stroop “Color Word” test, which has been thought to be a measure of selective attention and the susceptibility to interference from conflicting stimuli. Conversely, the HIT session did not improve the performance in the Digit Span “Forward” and “Backward” tests, both being considered as measures of short-term memory. The influence of the intensity of an acute bout of exercise on cognition has been previously examined (Brisswalter, et al., 2002; Tomporowski, 2003). Some authors have speculated that the exercise intensity affects cognitive performance in a U-shaped fashion, meaning that a moderate-intensity exercise would improve cognition whereas high-intensity exercise would impair cognitive performance (Brisswalter, et al., 2002; Kashihara, et al., 2009). In line with this assumption, Chmura, et al. (1994) observed gradual improvements in the reaction time (as assessed by an audio-visual five-choice reaction task) when participants exercised up to approximately 75% of their VO2 peak. Thereafter, the reaction time impaired rapidly, exceeding the resting value by 18%, suggesting that intensity seems to play a role in the effects of an acute exercise session on some aspects of cognitive performance. However, apparently in contrast to the U-shaped hypothesis, no deterioration in cognitive measures was detected after an acute session of HIT in the present study (actually, improvements in selective attention were noted), corroborating previous data involving higherintensity exercise, in which cognition parameters remained unaffected or even improved (Bard & Fleury, 1978; Lemmink & Visscher, 2005; Winter,
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et al., 2007). Therefore, one may argue that exercise intensity itself does not exert a major role in exercise-induced cognitive modulation. Possibly, exercise-induced fatigue plays a more important role on the cognitive responses to an exercise bout. Since we did not assess fatigue in this study, further studies should test the influence of exercise-induced fatigue upon cognition following a variety of exercise types (e.g., continuous, intermittent, strength, aerobic, combined-type) under different intensities and durations. Furthermore, no exercise-induced changes were observed in the “Forward” and the “Backward” subtasks of the Digit Span test, corroborating previous findings with depressive participants who undertook an acute moderate-intensity aerobic exercise session (Vasques, Moraes, Silveira, Deslandes, & Laks, 2011). However, it is important to note that the participants showed very high scores on the Digit Span test at baseline; thus, one cannot rule out the possibility of a “ceiling effect” for this test. A growing body of literature has supported the efficacy of HIT in promoting health-related benefits in several healthy and ill individuals, including improvements in body composition and cardiovascular system, and beneficial adaptation in skeletal muscle. Interestingly, the current results expand the current literature by showing that an acute HIT did not impair cognitive performance; on the contrary, HIT seems to be able to improve the performance on a selective attention task, but not on a shortterm memory one, in healthy middle-aged adults. REFERENCES
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