Order 932343: Does exercise and fitness affect cognitive health

BRIEF REPORT

Exercise and Fitness Modulate Cognitive Function in Older Adults

Chien-Heng Chu National Taiwan Sport University

Ai-Guo Chen Yangzhou University

Tsung-Min Hung National Taiwan Normal University

Chun-Chih Wang and Yu-Kai Chang National Taiwan Sport University

This study investigated the effects of acute exercise on cognitive function and the modulatory role of fitness in the relationship between exercise and cognition. Forty-six healthy older adults, categorized into higher or lower fitness groups, completed the Stroop test after both 30 min of aerobic exercise and a reading control with a counterbalanced order. Our findings demonstrated that acute exercise leads to general improvements in 2 types of cognitive functions and to specific improvements in executive function. Additionally, older adults with initially higher fitness levels experienced greater beneficial effects from acute exercise.

Keywords: aerobic exercise, cognition, executive function, inhibition, Stroop test

The population over 60 years old has rapidly grown and changed the worldwide demographic landscape (Gorman, 2002). This aging population not only experiences the deterioration of physical functions but also suffers from declining brain and cog- nitive functions. Indeed, normal aging is associated with brain volume atrophy of approximately 15% to 25% (Jernigan et al., 2001) and with it the degradation of cognitive processes, including memory, reasoning, and information processing speed (Salthouse, 2004). The influence of acute exercise, defined as a single bout of exercise, on cognitive performance has received substantial atten- tion within younger populations, demonstrating positive changes with small to moderate effects on various types of cognitive performance (Chang & Etnier, 2015; Chang, Labban, Gapin, & Etnier, 2012; Chu, Alderman, Wei, & Chang, 2015; Lambourne & Tomporowski, 2010; McMorris, Sproule, Turner, & Hale, 2011). However, examination of whether the positive effects of acute

exercise extend to older adults has been limited, with ambiguous findings.

Pesce and Audiffren (2011) found that switch performance improved following acute exercise at moderate intensity in both younger and older adult groups. Given that switching is one of the primary executive function aspects, these results suggested that the beneficial effects of acute exercise could extend to higher order cognitive function, regardless of age. In contrast, research that used a similar paradigm (i.e., Alternate Uses test) found partially conflicting findings wherein the positive effects of acute exercise in older adults only partially benefited switching (Netz, Tomer, Axelrad, Argov, & Inbar, 2007). Another study found changes in only basic cognition levels in older adults following acute exercise (i.e., Stroop color condition) and failed to demonstrate an effect on the inhibition- and interference-related executive function aspects (i.e., Stroop inhibition and interference conditions; Barella, Etnier, & Chang, 2010). Notably, these studies measured different cogni- tive functions, implying that the cognition type plays a moderating role in the relationship between acute exercise and cognition. Indeed, Etnier and Chang (2009) proposed that acute exercise effects might differ depending on the specific type of cognitive function and further studies are required that utilize assessments that not only are widely used but also posit multiple cognition subtypes with similar features, such as the Stroop test. Therefore, future research should examine the effects of acute exercise on different cognitive functions derived from similar task character- istics to explore these relationships.

Another potential moderator that must be considered is the participant’s cardiovascular fitness status (Brisswalter, Collardeau, & René, 2002; Chang et al., 2012). Longitudinal studies have indicated that, along with the positive association between cardio- vascular fitness and cognitive function (Etgen et al., 2010), exer-

Chien-Heng Chu, Graduate Institute of Athletics and Coaching Science, National Taiwan Sport University, Taoyuan, Taiwan, Republic of China; Ai-Guo Chen, College of Physical Education, Yangzhou University, Ji- angsu, People’s Republic of China; Tsung-Min Hung, Department of Physical Education, National Taiwan Normal University, Taipei, Taiwan, Republic of China; Chun-Chih Wang and Yu-Kai Chang, Graduate Insti- tute of Athletics and Coaching Science, National Taiwan Sport University.

This research was supported by a portion of Grants NSC 101-2628-H- 179-002 and NSC 102-2420-H-179-001-MY3 from the Ministry of Sci- ence and Technology, Taiwan, to Yu-Kai Chang.

Correspondence concerning this article should be addressed to Yu- Kai Chang, Graduate Institute of Athletics and Coaching Science, National Taiwan Sport University, No. 250, Wenhua 1st Road, Guishan Township, Taoyuan County 333, Taiwan, Republic of China. E-mail: [email protected]

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Psychology and Aging © 2015 American Psychological Association 2015, Vol. 30, No. 4, 842– 848 0882-7974/15/$12.00 http://dx.doi.org/10.1037/pag0000047

842

cise interventions that induced fitness improved specific cognitive function types (Angevaren, Aufdemkampe, Verhaar, Aleman, & Vanhees, 2008; Smith et al., 2010). These superior cognitive- related foundations associated with high cardiovascular fitness may result in larger improvements following acute exercise. A meta-analysis conducted by Chang et al. (2012) indicated that individuals with higher fitness levels received the largest acute exercise benefit effects compared with individuals with low or moderate fitness levels, both immediately and following a delay after exercise. Notably, this viewpoint is primarily based upon studies performed with younger adults. Furthermore, only a few studies have investigated these differences among individuals with different fitness levels (individuals with high fitness levels, but not moderate or low fitness, were typically evaluated; Chang, Chi, et al., 2014; Chang et al., 2012).

Recently, the modulatory role of fitness in acute exercise and cognition in older adults has been preliminarily explored. Pesce, Cereatti, Forte, Crova, and Casella (2011) indicated that road cyclists had better visual attention control and performance in attentional tasks involving executive control compared with a sedentary group during an acute bout of aerobic exercise. Similar fitness-moderated effects of acute exercise on cognitive flexibility were observed (Netz, Argov, & Inbar, 2009). However, these studies focused on highly trained individuals and cognitive per- formance assessed during acute exercise or utilized assessments that examined a single construct.

Whether the effects of acute exercise have general or specific effects on the different cognition types and whether fitness status moderates the magnitude of favorable acute exercise effects on these cognitive performances, particularly in older adults, remain undetermined. The present study examined the effects of acute exercise on two types of cognitive processes derived from the Stroop test (i.e., Stroop congruent and incongruent conditions), where the Stroop incongruent condition is believed to engage a greater amount of executive control than does the Stroop congru- ent condition, which reflects more-basic information processing (e.g., perceptual-motor level; Liotti, Woldorff, Perez, & Mayberg, 2000; Miyake et al., 2000; West & Alain, 1999). Additionally, the acute effects on these cognitive functions were compared between older adults with higher and lower fitness levels to explore the modulatory role of fitness. Acute effects were expected to induce favorable effects on multiple cognition types, and older adults with higher fitness were expected to receive larger acute exercise ben- efits than were older adults with lower fitness.

Method

Participants

Seventy healthy older adults, ages 60 to 70 years, were initially recruited in Taoyuan County, Taiwan. The participants were screened using physical activity readiness and health screening questionnaires and were required to meet the follow- ing criteria: (a) right-hand dominant, (b) no history of neuro- logical or major psychiatric disorders, (c) normal or corrected- to-normal vision, and (d) no color-blindness to minimize the confounders between acute exercise and cognition. Eligible participants completed the Digit Span test (Wechsler, 1997). Then, the participants were categorized into a higher or a lower

fitness group on the basis of a VO2peak that fell above or below the 55th percentile (�35.0 ml/kg/min for men and �29.4 ml/ kg/min for women; American College of Sports Medicine, 2013), resulting in 46 participants, with 22 in the higher fitness group and 24 in the lower fitness group. This study was ap- proved by the university Institutional Review Board, and all participants provided informed consent.

Cardiovascular Fitness Test

Cardiovascular fitness was assessed via a submaximal exercise test according to the YMCA cycle ergometry protocol (Golding, 1989). The protocol was appropriate for adults with a Class A risk stratification (Fletcher et al., 2001). The YMCA protocol includes two to four consecutive 3-min circuits, which have specific work- loads designed to raise the steady-state heart rate between 110 beats/min and 85% of the age-predicted maximal heart rate (e.g., 220-age). To begin, the participant rode a cycle ergometer (Er- goselect 100/200, Ergoline GmbH, Germany) with a workload of 150 kpm/min (25 W) and a 50-rpm pedaling rate. The average heart rate during the last 15–30 s of the final second and third minutes determined the subsequent workloads (e.g., 750 kpm/min, 600 kpm/min, or 300 kpm/min). When the target steady-state heart rate was observed for two consecutive circuits, the VO2peak was calculated on the basis of the slope regarding heart rates, workload, and body mass.

The Stroop test

The Stroop test (Stroop, 1935) is a widely used neuropsycho- logical assessment recommended for adaptation in exercise– cognition research. The computerized Stroop test consists of two types of conditions— congruent and incongruent—and was pre- sented using Stim2 (Neurosoft Labs, Inc., Sterling, VA). In the congruent condition, Chinese words (i.e., 紅 [red], 藍 [blue], and 綠 [green]) were presented in the same color as the meaning of the words. In the incongruent condition, the name of the color word was printed in a different font color. Each stimulus word was presented in equal proportions in the congruent (i.e., 33.3% each for red, blue, and green words) and incongruent (e.g., the word “red” printed in either blue or green color) conditions to minimize specific word facilitation. Each block had 60 target stimuli con- sisting of 38 congruent and 22 incongruent stimuli with mixed presentation. Each 2-cm stimulus was displayed in the center of a 21-in. (53.3 cm) computer screen. Each trial began with the pre- sentation of a fixed cross for 500 ms. Then, either a target- congruent or -incongruent stimulus was presented for 506 ms; the interval between the fixed cross and the target stimulus was 383, 583, or 783 ms in a random order to minimize anticipation. Participants were instructed to respond as quickly and accurately as possible to the color of the presented stimulus by pressing their thumb on one of three buttons on a response pane. Each trial was completed once the target stimulus response was made within 1,000 ms. Response time and accuracy were identified as primary indices. Each participant was required to complete six blocks with a 2-min rest between each block, resulting in a total testing period of approximately 25 min.

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843ACUTE EXERCISE, FITNESS, COGNITION, OLDER ADULT

Experimental Procedures

The participants attended the laboratory individually on three separate days, with at least a 3-day interval between each day and within a 2-week period. On Day 1, participants meeting the inclusion criteria were fit with a Polar HR monitor (Sport Tester PE 3000, Kempele, Finland) and completed a submaximal exercise test with a YMCA cycle ergometry protocol. The participants were then assigned to either the high- or low-fitness group on the basis of their VO2peak (categorized as good or poor, respectively).

The experimental conditions for Days 2 and 3 (i.e., exercise and control days) were performed in a counterbalanced order to control for potential practice and order effects. Each participant was tested at a similar time of day on the 2 days to control confounding due to time of testing (Hasher, Chung, May, & Foong, 2002). On the exercise day, the resting heart rate (HR) was measured by having the participants sit quietly in a chair for 10 –15 min. Then, participants completed practice trials to become familiarized with the test procedure; once an 85% correct rate was achieved, they started the experimental trials. Next, participants were instructed to complete a modified acute cycling ergometer protocol on the basis of Chang et al. (2011). The protocol consisted of three stages: a 5-min warm-up, a 20-min primary exercising stage at 65% heart rate reserve (HRR; the difference between maximal and resting heart rates), and a 5-min cool-down. The peddling rate was set at 70 rpm, and the workload began with 15 W and then increased or decreased gradually until a steady state at the required HR was reached. The participants performed the Stroop test within 5 min of exercise cessation. On the control day, participants completed procedures similar to those on the exercise day, except that participants read a book related to exercise and cognition during treatment. The control condition was intended to maintain a low arousal level compared to the exercise con- dition.

A Polar HR monitor and the Rating of Perceived Exertion (RPE) scale (Borg, 1982) were used to objectively and subjectively confirm the intensity manipulation, respectively. The RPE scale ranges from 6 (no exertion at all) to 20 (maximum exertion). The experimental session lasted approximately one and a half hours each day. Participants were informed about the purpose of the study and compensated with US$15 after completing the overall experimental session.

Statistical Analyses

This study was a randomized control group posttest design. A mixed three-way analysis of variance (ANOVA), with a between- subjects (i.e., group: lower vs. higher fitness) and two within- subject (i.e., treatment: control vs. exercise; Stroop condition: congruent vs. incongruent) were used to analyze response time and accuracy. Multiple comparisons were performed using t tests with Bonferroni adjustments when appropriate. The effect size of the partial eta-square was reported for significant effects derived from the ANOVA. An alpha of 0.05 was set as significant for all analyses.

Results

Participant Characteristics and Exercise Intensity Check

Higher scores in the higher fitness group were observed for only fitness-related variables (see Table 1). The HR values (beats per minute [bpm]) for the lower and higher fitness groups during the primary exercise were 124.8 � 7.2 bpm and 119.5 � 8.8 bpm, respectively, representing 60% to 65% of HRR. Along with the RPE range of 12 to 14, these values suggest that the exercise intensity was appropriate.

Stroop Test Performances

A preliminary analysis was conducted to test the effects of session order. Neither a main effect of session order nor any interaction with session order was observed for any dependent variable, Fs(1, 21) � 1.81, p � .19.

A main effect of the treatment condition revealed a shorter response time for the exercise compared with that for the control condition, F(1, 44) � 169.75, p � .001, partial �2 � 0.79, and a main effect of the Stroop condition revealed a longer response time for the incongruent compared with the congruent condition,(F(1, 44) � 123.91, p � .001, partial �2 � 0.73 (see Table 2).

An interaction between the treatment and fitness was observed, F(1, 44) � 10.17, p � .03, partial �2 � 0.18. The follow-up comparisons revealed that the exercise condition had a shorter response time compared to that of the control condition in both the higher (p � .001) and lower (p � .001) fitness groups. Addition- ally, the higher fitness group demonstrated a shorter response time relative to the lower fitness group in the exercise condition (p � .04) but not the control condition (see Figure 1a).

An interaction between treatment and Stroop condition was also observed, F(1, 44) � 10.17, p � .001, partial �2 � 0.24. The follow-up comparisons revealed that the response time for the incongruent condition was longer than that for the congruent condition in both the exercise (632 � 102 vs. 587 � 83, respec- tively, p � .001) and control (695 � 99 vs. 632 � 82, respectively,

Table 1 Participant Demographics for the Higher and Lower Fitness Groups

Variable

Higher fitnessa

Lower fitnessb

p ESM SD M SD

Age (years) 63.8 2.3 64.9 4.0 .29 Education (years) 9.3 3.5 10.0 4.1 .57 Height (cm) 161.7 8.6 158.2 6.7 .13 Weight (kg) 63.8 8.6 61.8 9.4 .45 BMI (kg.m�2) 24.2 2.5 24.3 3.1 .95 Digit Span Forward 11.5 2.4 11.2 2.5 .69 Digit Span Backward 6.0 2.4 6.7 2.4 .32 VO2peak (mL.kg

�1.min�1) 36.0 1.2 23.5 2.8 .01 5.80�

Resting heart rate (bpm) 65.5 8.7 70.0 6.6 .05 0.58�

Note. ES � effect size with the value of Cohen’s d; BMI � body mass index; bpm � beats per minute. a Sample size � 22 (12 female). b Sample size � 24 (10 female). � p � .05.

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844 CHU, CHEN, HUNG, WANG, AND CHANG

p � .001) conditions. The exercise condition resulted in shorter response times compared to those for the control condition with both the congruent and incongruent conditions (p � .001). An additional paired t test revealed a smaller difference between the congruent and incongruent conditions in the exercise condition relative to the control condition, t(45) � 3.83, p � .001 (see Figure 1b). No three-way interaction was observed.

Regarding accuracy, main effects of treatment and Stroop con- dition were revealed. Higher accuracy for the exercise condition compared to the control condition, F(1, 44) � 5.12, p � .03, partial �2 � 0.11, and lower accuracy for the incongruent condi- tion compared to the congruent condition, F � 28.23, p � .001, partial �2 � 0.41, were observed. Neither the main effect of fitness nor any interaction was significant.

Discussion

This study investigated how cardiovascular fitness moderates two types of cognitive function assessed by the Stroop test, fol- lowing an acute bout of moderate aerobic exercise in an older population. Although participants had a shorter response time and an increased accuracy rate in both conditions of the Stroop test following exercise, reflecting general improvements, acute exer- cise led to additional benefits for executive function by demon- strating a smaller difference between the congruent and incongru-

ent conditions after acute exercise compared to results for the control condition. Moreover, older adults with a higher fitness level performed significantly better following acute exercise than did those with a lower fitness level, suggesting that the level of fitness modulates the relationship between acute exercise and cognition. Thus, older adults with a higher fitness level received disproportionally more benefits from acute exercise than did those with a lower fitness level.

The longer response time and lower accuracy rate in the Stroop incongruent condition relative to the Stroop congruent condition, regardless of treatment conditions, demonstrate the typical Stroop effect (Cohen, Dunbar, & McClelland, 1990). Specifically, com- pared with the congruent condition, in which colors of the char- acters were named in the absence of interference (i.e., presenting automatic activation), greater attentional demand was required to resolve the conflicts between the stimulus meaning and color in the incongruent condition to inhibit the automatic nature of word- reading tendency (Cohen et al., 1990; Milham et al., 2002). Fur- thermore, the initiating response to inhibit the bias toward word reading is also believed to reflect an inhibitory aspect of executive function (Bugg, Jacoby, & Toth, 2008; Nigg, 2000).

Acute exercise not only reduced the response times for both Stroop test conditions but also diminished the interference, sug- gesting that acute exercise led to both general and specific im- provements in cognitive functions. Our findings that these im- provements are associated with acute exercise agree with the findings of many previous studies and confirm that an acute bout of moderate exercise increases cognitive performance requiring different amounts of executive control (Chang, Tsai, Huang, Wang, & Chu, 2014; Hyodo et al., 2012; Sibley, Etnier, & Le Masurier, 2006; Tam, 2013; Yanagisawa et al., 2010). For exam- ple, Tam (2013) reported that, compared with a response time reduction of 10.2% in the congruent condition, a 20.6% reduction was found in the incongruent condition after acute exercise. Chang, Tsai, et al. (2014) also reported that acute exercise im- proved performances in five conditions of the Stroop test (i.e., Stroop congruent, word, neutral, square, and incongruent), in which the largest increase was observed in the incongruent con- dition.

Table 2 Stroop Test Performances of Fitness Groups and Treatment Conditions

Variable

Higher fitness Lower fitness

Control Exercise Control Exercise

M SD M SD M SD M SD

Response time (ms) Congruent 622 67 567 61 642 96 608 99 Incongruent 679 86 602 83 711 109 664 110

Accuracy rate (%) Congruent 92 7 94 5 94 7 95 7 Incongruent 80 15 84 21 86 9 93 6

Figure 1. (a) The response time of the Stroop test is a function of treatment condition and fitness. (b) Stroop differences during the congruent and incongruent conditions between the exercise and control conditions. Error bars represent standard error of the means. � Represents a significant difference between treatments. # Represents a significant difference between fitness group (p � .05).

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845ACUTE EXERCISE, FITNESS, COGNITION, OLDER ADULT

General improvement may be attributed to exercise-induced increases in cerebral blood flow (Heo et al., 2010; Ide & Secher, 2000). That is, brain neuronal activity and metabolism increase during exercise (Ide & Secher, 2000), resulting in elevated cerebral blood flow (Ogoh & Ainslie, 2009). In contrast, specific improve- ments may be interpreted by neuroelectric studies. Acute exercise enlarges the P3 amplitude only in tasks reflecting executive func- tion (Chu et al., 2015; Hillman, Snook, & Jerome, 2003; Kamijo, Nishihira, Higashiura, & Kuroiwa, 2007). These findings from neuroelectric perspectives suggest that acute exercise may benefit cognition through increased attentional resource allocation for tasks requiring greater executive control processes. Taken to- gether, increased cerebral blood flow and attention alterations suggest possible general and specific functional roles in exercise- induced cognitive enhancement.

Another novel finding from the current study was an interaction between treatment and fitness level, namely, the more-fit older adults had superior improvements in the Stroop test than did their less-fit counterparts. This finding is consistent with a previous meta-analysis (Chang et al., 2012) and extends the current knowl- edge regarding older adults with extreme higher fitness status (e.g., highly trained) to those with moderate to high fitness status (Netz et al., 2009; Pesce & Audiffren, 2011). Although the underlying mechanisms remain unknown, potential interpretations based on studies indirectly examining this issue have been proposed. Older adults with higher fitness may maintain better brain structures and functions, providing the foundation for superior benefits from acute exercise. Studies associated with structural and functional magnetic resonance imaging (MRI) have indicated that older adults with higher fitness or long-term exercise training demon- strate larger volumes of several brain regions that are the core of cognitive functions, such as white and gray matter in the ventro- lateral and dorsolateral prefrontal cortexes (Colcombe et al., 2003) and the hippocampus (Erickson et al., 2009), as well as greater activations in similar brain regions during cognitive task perfor- mance (Colcombe et al., 2004). Using an electroencephalogram, Hogan et al. (2013) found that adolescents with high fitness levels experienced greater lower upper alpha and beta coherence after acute exercise, whereas no beneficial acute effect was observed for those with lower fitness levels, implying that the individuals with higher fitness posited better cortical efficiency.

The present study was restricted by several factors. First, a causal relationship between fitness and cognitive performance could not be established because of the cross-sectional design. Additionally, the Stroop test reflected only the interference aspect of inhibition rather than inhibition related to motor suppression (Aron et al., 2007). Therefore, caution should be taken with the generalization of the results. Moreover, Boot, Simons, Stothart, and Stutts (2013) indicated that different expectancy track benefit performances were observed when conducting computer-based games, reflecting that the treatment effect may be confounded by expectancy individual posited. Expectancy has yet to be consid- ered in acute exercise– cognition studies, and future research that considers this confounder is suggested. The disproportionate num- ber of congruent and incongruent trials may also lead to potential bias regarding inhibitory processes. Specifically, more incongruent trials than congruent trials may increase the Stroop effect. Al- though such bias was limited in the present study because the number of trials was constant across groups and conditions, the

percentage of each trial type is worth considering in future study designs.

In conclusion, acute exercise leads to general and specific im- provements for two types of cognitive functions derived from the Stroop test, and the beneficial effects of acute exercise are greater for older adults with higher fitness. These findings are important for older adults and suggest that performing a single bout of exercise can improve cognitive performance. These results also indicate that good fitness levels can maximize these beneficial cognitive effects (i.e., processing speed of cognitive performance) induced by acute exercise.

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Received September 22, 2014 Revision received July 5, 2015

Accepted July 8, 2015 �

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