Journals of Gerontology: MEDICAL SCIENCES Cite journal as: J Gerontol A Biol Sci Med Sci 2014 September;69(9):1109–1116 doi:10.1093/gerona/glu095

© The Author 2014. Published by Oxford University Press on behalf of The Gerontological Society of America. All rights reserved. For permissions, please e-mail: [email protected]. Advance Access publication July 14, 2014

The Effects of an 8-Week Hatha Yoga Intervention on Executive Function in Older Adults Neha P. Gothe,1,4 Arthur F. Kramer,2,3 and Edward McAuley1,2 1 Department of Kinesiology and Community Health, Beckman Institute for Advanced Science and Technology, and 3 Department of Psychology, University of Illinois, Urbana-Champaign. 2

Present address: Division of Kinesiology, Health and Sport Studies, Wayne State University, Detroit, Michigan.

4

This study was registered at Clinical Trials.gov (NCT01650532). Address correspondence to Neha P. Gothe, PhD, Division of Kinesiology, Health and Sport Studies, Wayne State University, Detroit, MI 48202. Email: [email protected]

Background.  Few scientific studies have examined movement-based embodied contemplative practices such as yoga and their effects on cognition. The purpose of this randomized controlled trial was to examine the effects of an 8-week Hatha yoga intervention on executive function measures of task switching and working memory capacity. Methods.  Community-dwelling older adults (N = 118; mean age = 62.0) were randomized to one of two groups: a Hatha yoga intervention or a stretching–strengthening control. Both groups participated in hour-long exercise classes 3×/ week over the 8-week study period. All participants completed established tests of executive function including the task switching paradigm, n-back and running memory span at baseline and follow-up. Results. Analysis of covariances showed significantly shorter reaction times on the mixed and repeat task switching trials (partial η2 = .04, p < .05) for the Hatha yoga group. Higher accuracy was recorded on the single trials (partial η2 = .05, p < .05), the 2-back condition of the n-back (partial η2 = .08, p < .001), and partial recall scores (partial η2 = .06, p < .01) of running span task. Conclusions. Following 8 weeks of yoga practice, participants in the yoga intervention group showed significantly improved performance on the executive function measures of working memory capacity and efficiency of mental set shifting and flexibility compared with their stretching–strengthening counterparts. Although the underlying mechanisms need to be investigated, these results demand larger systematic trials to thoroughly examine effects of yoga on executive function as well as across other domains of cognition, and its potential to maintain or improve cognitive functioning in the aging process. Key Words:  Yoga intervention—Cognition—Older adults—Working memory. Received December 19, 2013; Accepted May 20, 2014 Decision Editor: Stephen Kritchevsky, PhD

Y

oga is a commonly practiced, mind–body activity that has components centering on meditation, breathing, and postures. In recent U.S.  surveys of adults, 7.5% reported having used yoga at least once in their lifetime and 3.8%–5.1% reported having used it in the previous 12 months (1,2). The use of yoga and other complementary and alternative medicine therapies is becoming increasingly popular, especially among older adult populations who use these alternative therapies for aging-related chronic conditions such as back pain, arthritis, anxiety, depression, and cancer (3–6). Although yoga practice involves physical postures that mimic stretching, balance, and strength exercises, which result in physical benefits (7), it also includes an active attentional component of breathing and meditation practice. Given the age-related declines in cognitive function (8), little is known about the potential of yoga in maintaining or enhancing cognitive function in older adults.

A considerable corpus of research exists that has extensively examined the effects of physical activity on cognition and executive functions. However, majority of these studies have examined the role of aerobic training. Colcombe and Kramer (9) in their meta-analysis reviewed randomized controlled trials (RCTs) conducted with sedentary healthy older adults and found that executive control processes (g  =  0.68, p < .05) showed the largest benefit from aerobic fitness training. More recently, Smith and colleagues (10) conducted a meta-analysis to examine this relationship and reported that individuals randomly assigned to receive aerobic exercise training demonstrated modest improvements in executive function (g = 0.123, p < .018) and working memory (g = 0.128, p < .026). Regardless of the methodological differences, both these meta-analyses suggest that participation in aerobic physical activity can help improve cognitive function. However, compared with 1109

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this extensive body of work on aerobic training and cognition, far fewer scientific studies or RCTs have examined movement-based embodied contemplative practices such as yoga (11–14) or tai-chi (15). Oken and colleagues (12) conducted a RCT examining the effects of yoga on cognition in healthy older adults, but found no relative improvements in cognitive function. The authors acknowledged two major reasons that explain these null findings: (i) recruitment of physically active seniors that may have resulted in a ceiling effect and (ii) the dose of exercise that was one session per week is lower compared with more frequent sessions employed in other successful RCTs (9,10). More recently, Hariprasad and colleagues (14) conducted a 6-month RCT with residents of elderly homes and found significant cognitive improvements in attention and processing speed, verbal and visual memory, working memory, and inhibitory control. The authors acknowledged the lack of an active control group, high dropout rate, and the need to examine effects of yoga on community-dwelling older adults. Given the paucity of yoga–cognition RCTs and to address limitations of previous studies, the purpose of this RCT was to examine the effects of an 8-week Hatha yoga intervention on executive function in community-dwelling older adults. We recruited sedentary healthy older adults and structured the dose of exercise to match the physical activity literature with training sessions held 3×/week. We also used three established measures of executive function that have been extensively used in physical activity research: the task switching paradigm (16), the n-back task (17,18), and the running memory span task (19). The primary outcomes were mean reaction time (RT) and accuracy (AC) scores on the three executive function measures. We hypothesized that regular, structured Hatha yoga practice, which included components of physical movements, breathing, and meditation, would lead to significant improvements on executive function measures following the 8-week trial in a sample of sedentary healthy community-dwelling older adults.

Methods Participants Figure 1 shows the flow of participants through the trial. Participants (N = 118, males = 26; mean age = 62.0 ± 5.6) were low active, healthy community-dwelling older adults who volunteered to participate in an 8-week exercisebased RCT. They were recruited between March 2012 and January 2013 through University of Illinois LISTSERV, fliers, community groups, and postings and screened to determine eligibility for the study. In order to participate in the trial, participants had to be between 55 and 79 years of age, English speaking, report being sedentary for at least the previous 6 months ( 0 and total recall score presented performance on trials where m = 0. N-back task.—Working memory was also assessed with a modified serial n-back task (17,18) that involved two consecutive phases: 1-back and 2-back. Each phase required the participants to discriminate between a sequence of letters that served as stimuli. In the 1-back condition, the participant was instructed to respond as quickly and accurately as possible if the current letter was the same as the previous

trial for the 1-back condition, and two trials previous for the 2-back condition. A  practice block of 13 stimuli and five experimental blocks of 20 stimuli each were presented for each of the two conditions. All stimuli letters were in white, small caps, Arial size 72, approximately 3 cm tall, presented one at a time on a computer screen with a black background for a duration of 2000 ms with a fixed 1,500 ms intertrial interval. AC on the 1- and 2-back conditions was examined. Data Analysis Data were analyzed using SPSS 20.0 (IBM Corp., Armonk, NY). Prior to all hypothesis testing, independent sample t-tests were conducted to examine whether significant mean differences existed in demographic, health, and physical activity variables among the two groups at baseline. A series of repeated measures analyses of covariance controlling for age, education, attendance, and baseline performance were employed to explore intervention effects for all the executive function measures. Results Participant Characteristics Of the 118 participants, n  =  61 were randomized to the yoga intervention group and n = 57 to the stretching– strengthening control as shown in Figure  1. The mean Telephone Interview for Cognitive Screening score for the total sample was 30.65 (range = 24–38, ±3.27), which was well above the cut-off of 21, which is considered indicative of cognitive deficiency. Individuals were also screened for depressive symptomology using the Geriatric Depression Scale and scored below the cut-off point of greater than or equal to 5 with a mean of 1.05 (range = 0–4, ±1.22). Table  1 shows the participant characteristics by group. Within both groups, the majority of the participants were female, married, working full time, well-educated, and relatively affluent. Approximately 20% of the study participants represented minority groups. An independent samples t-test showed no significant differences between conditions on any of these characteristics (all p ≥ .20) including baseline Telephone Interview for Cognitive Screening, Geriatric Depression Scale, self-reported health, or leisure time physical activity (all p ≥ .19). Approximately, one third of the participants in both groups had tried yoga previously (range: 6–40 years ago, between 1 and 12 yoga classes) but were no longer practicing at the time of the trial. The average attendance at the yoga classes was 80.82% (19.2 ± 3.8 sessions) and was not significantly different from the stretching–strengthening exercise classes at 81.29% (19.4 ± 3.8 sessions). The overall attrition rate was 8.47% with 108 participants successfully completing the intervention and follow-up assessments. A series of t-tests were conducted to determine whether the completers differed from the dropouts (n  =  10) on any demographic or baseline measures.



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Table 1.  Baseline Characteristics of Older Adults in the Yoga and Stretching–Strengthening Control Groups*

Age (mean, SD) Sex (n, %)  Females  Males Race (n, %)   African American  Asian   American Indian/Alaskan Native   More than one race  Caucasian Education (n, %)   College degree Income (n, %)  40,000 Marital status (n, %)  Married  Separated/divorced  Widowed  Single   Partnered/significant other Employment status (n, %)  Retired   Working part time   Working full time  Unemployed Yoga experience (n, %)   Had tried it in the past   Would probably try it TICS-M (mean, SD) Overall self-rated health (mean, SD) Leisure time physical activity score (mean, SD)

Table 2.  Means and Standard Deviations of the Executive Function Variables for the Yoga and Control Groups at Baseline and Follow-up

Yoga

Control

n = 61

n = 57

Pre

Yoga Post

Pre

Post

ANCOVA

62.1 (±5.82)

62.0 (±5.39)

n = 61

n = 58

n = 57

n = 50

p Value

49 (80.3) 12 (19.7)

43 (75.4) 14 (24.6)

7 (11.5) 2 (3.3) 0 (0) 1 (1.6) 51 (83.6)

4 (7.0) 2 (3.5) 2 (3.5) 3 (5.3) 46 (80.7)

14 (23) 47 (77)

25 (43.8) 32 (56.2)

  Repeat AC (%)

11 (17.9) 50 (82.1)

16 (28.2) 41 (71.8)

724.01 ±100.47 0.94 ±.10 1171.3 ±176.86 0.87 ±.16 998 ±169.35 0.89 ±.14

714.97 ±121.53 0.98 ±.05 1084.52 ±163.48 0.94 ±.08 941.48 ±147.51 0.95 ±.07

730.29 ±111.10 0.92 ±.09 1151.29 ±182.78 0.84 ±.22 1003.33 ±191.02 0.86 ±.22

747 ±114.07 0.94 ±.11 1120.73 ±153.98 0.88 ±.21 994.59 ±190.00 0.88 0.21

Running span   Partial recall score

34 (55.7) 15 (24.6) 7 (11.5) 3 (4.9) 2 (3.3)

39 (68.4) 11 (19.3) 4 (7) 2 (3.5) 1 (1.8)

  Total recall score

15.61 ±6.86 29.48 ±8.93

17.97 ±6.68 31.64 ±8.71

16.89 ±5.85 29.3 ±8.32

16.76 ±6.81 29.68 ±9.24

13 (21.3) 15 (24.6) 32 (52.5) 1 (1.6)

13 (22.8) 13 (22.8) 30 (52.6) 1 (1.8)

0.97 ±.05 0.8 ±.18

0.98 ±.03 0.87 ±.11

0.96 ±.05 0.84 ±.13

0.97 ±.06 0.82 ±.17

Task switching   Single RT (ms)   Single AC (%)   Mixed RT (ms)   Mixed AC (%)   Repeat RT (ms)

N-back   1-Back AC (%)   2-Back AC (%)

18 (29.5) 43 (70.5) 30.86 (±3.29) 2.10 (±.7)

20 (35.1) 37 (64.9) 30.42 (±3.25) 2.28 (.73)

1.15 (±1.32)

1.22 (±1.54)

Control

.08 .02 .04 .09 .04 .10

.01 .11

.18 .003

Note: AC = accuracy; ANCOVA = analysis of covariance; ms = milliseconds; RT = reaction time.

Analysis revealed that there were no significant differences on any of the demographic or baseline cognitive outcomes (all p > .05).

paradigm. A significant mean difference favoring the yoga group was observed on the mixed block [F(1,101) = 3.98, p = .04, partial η2 = .04]. The yoga participants were more efficient in switching between the odd-even and low-high tasks compared with the controls. Within the mixed block of trials, the yoga group also showed significantly faster RTs on the repeat [F(1,101)  =  4.16, p  =  .04, partial η2  =  .04]. Significant group differences were also observed on single block AC [F(1,101) = 5.09, p = .02, partial η2 = .05]. The yoga group was more accurate on the single block and a similar trend although nonsignificant was observed on the mixed block of trials [F(1,103) = 2.96, p = .09, partial η2 = .02].

Cognitive Outcomes The mean RT, AC, and test scores for the executive function measures are presented in Table 2. Adjusted follow-up means from the analysis of covariances are also presented in Table 2. No significant baseline differences were found between the two groups (all p > .05), and the RT variables from the task switching test were normally distributed (Shapiro–Wilk statistic p ≥ .13).

Running Memory Span The repeated measures analysis of covariance showed a significant group effect for the partial recall score [F(1,101) = 6.82, p = .01, partial η2 = .06] with the yoga group demonstrating higher partial recall scores compared with the controls. The total recall score on the running span approached significance [F(1,101) = 2.49, p = .11, partial η2 = .02] indicating a similar trend favoring the yoga group.

Task Switching The analysis of covariance showed a significant group effect on mixed and repeat RT conditions of the task switching

N-Back Task No significant mean differences were observed on 1-back AC [F(1,101) = 1.82, p = .18, partial η2 = .02]. However,

Notes: TICS-M = Telephone Interview for Cognitive Screening-modified. *No significant group differences observed at baseline,

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a significant group difference was seen on 2-back AC [F(1,101) = 9.24, p = .003, partial η2 = .08], with the participants in the yoga group exhibiting higher AC on the 2-back condition at follow-up compared with the stretching– strengthening controls. Although the yoga group showed improved AC, no speed-AC trade-off or group differences were observed on RTs for either conditions of the n-back. Discussion The purpose of this RCT was to investigate the efficacy of an 8-week Hatha yoga intervention for improving cognition, particularly executive function in a healthy, low active community-dwelling adult population. Following 8 weeks of regular structured yoga practice, participants in the yoga intervention group showed significantly improved performance on the executive function measures of working memory capacity and efficiency of mental set shifting and flexibility as compared with their stretching–strengthening counterparts. Executive functions are multifaceted, and in an effort to mirror the aerobic training and cognition findings, established cognitive tasks representing domains of executive function were employed in this study. The results are promising and demand rigorous RCTs to replicate these findings and examine cognitive benefits of yoga across other established cognitive measures used in the physical activity literature. Using Cohen’s (25) classification of magnitude of effect sizes, this study demonstrates a small to moderate effect of yoga on executive function. The partial η2’s in this study ranged from .02 to .08 for the cognitive variables. Some variables approached significance (total recall from the running span, mixed AC from task switch, 1-back AC from the n-back) but did not show a significant group difference in this sample. These borderline results may be explained by potential ceiling effects as our sample consisted of healthy older adults without any cognitive impairment, the sample size, and short-term duration (8 weeks) of the study. However, all the results of this trial, taken together, should serve as a platform to design and power future trials to thoroughly investigate yoga effects on executive function as well as other domains of cognition. Hatha yoga is the most common form of yoga practiced in North America and involves the practice of physical postures in conjunction with awareness of the breath to help develop mental focus and to connect the mind, body, and spirit (26). It requires focused effort in moving through the poses, controlling the body, and breathing at a steady rate. In addition, breathing and meditation exercises are practiced to calm and focus the mind and develop greater selfawareness (27). It is plausible that this focus on one’s body and mind during yoga practice may have generalized to situations outside of the yoga classes resulting in an improved ability to focus and sustain attention on the task at hand without getting distracted. The yoga participants exhibited

a significantly greater number of processing runs involving accurate and sustained working memory discriminations. They were also able to maintain focus and accurately retrieve information from working memory under conditions that require more cognitive resources and continual updating and manipulation of information. A growing body of research evidence supports the belief that certain yoga techniques may improve physical and mental health through downregulation of the hypothalamic–pituitary–adrenal axis and the sympathetic nervous system (28). Yoga has been shown to have immediate psychological effects including decreased anxiety (29), depression (30), and stress (31) and positive changes in perceived quality of life (32). These studies suggest that yoga has an immediate quieting effect on the sympathetic nervous system/hypothalamic–pituitary–adrenal axis response to stress. It is well known that stress and anxiety affect cognitive performance, and the 8-week yoga intervention may have resulted in improved psychological states, which led to enhanced cognitive performance on the executive function tasks. In the physical activity–cognition literature, experiencing novel activities (33) and anaerobic interventions have been shown to have unique cognitive benefits on brain structure and function (34). From this neuroscientific perspective, tasks that involve mind wandering, memory consolidation, thought focused inwards to the self (self-referential thinking), and taking the perspective of others into one’s own view of the world have been associated with the default mode network, the regions that are active when individual is at rest but not focused on the outside world (35,36). There is evidence that supports a relationship between the default mode network and executive function, where increased activation has been associated with better working memory performance in young adults (36), and better performance on a range of executive function tasks in older adults (34,37–39). Although participants in both groups learnt new postural exercises, the breathing and meditative practices of yoga closely parallel the self-referential thoughts and involve learning and consolidation functions that have been associated with the default mode network. Future research should explore the structural and functional brain changes as a result of yoga in an effort to identify the neurobiological underpinnings of the yoga–cognition relationship. This 8-week trial systematically examined the effect of Hatha yoga on executive function in sedentary, healthy, community-dwelling older adults. The intervention involved a combination of postures, breathing, and meditative exercises. The multifaceted nature of this intervention is intriguing as it demands further enquiry to identify the active agent leading to improved cognitive performance. Further scientific efforts that compare yoga with other physical activity interventions that have been demonstrated to improve executive function are warranted. Another strength of this work is the stretching–strengthening control group that served as



YOGA AND EXECUTIVE FUNCTION

an active control exercise group, which has been a drawback of the yoga literature. Although this study contributes to the sparse yoga–cognition literature, there are some limitations to this work. The sample primarily consisted of Caucasian females with a fair representation of minority groups. From a generalizability and dissemination perspective, similar trials need to be implemented for larger samples of minority groups, males as well as older adults from lower socioeconomic status and educational levels. The participation rate was comparable to physical activity interventions targeting community-dwelling older adults (12,15,40). Individuals who were physically active were excluded from this study (n = 31). Walking is a common form of activity for older adults, and the effects of yoga in conjunction with walking for such active older adults needs to be investigated. Although this trial was successful in examining short-term effects of yoga, the absence of a longer follow-up timepoint is a limitation, which should be addressed in future trials. Determining the duration and frequency of yoga practice will enable researchers to establish standards and clinicians to recommend yoga practice to patients. Future RCTs need to explore the possible underlying mechanisms and neuroscientific and biophysiological determinants of the yoga– cognition relationship. In conclusion, the 8-week Hatha yoga intervention was successful in improving working memory capacity and mental set flexibility among older adults. Although this RCT successfully demonstrated the beneficial effects following 8 weeks, a longer follow-up period will enable researchers to thoroughly examine trajectories of change over the life span. Clearly, yoga research is still in its nascent stages, and with its increasing popularity, researchers need to adopt rigorous systematic approaches and advanced neuroimaging techniques to examine its cognitive benefits and underlying mechanisms. Funding This work was supported by the National Institute on Aging at the National Institutes of Health (2R01 AG20118). Acknowledgments The authors would like to thank yoga instructors Jennifer Allen and Steven Willette, and exercise specialists Jordan Orr and Merril Idiyalil for supervising the exercise groups. References 1. Barnes PM, Powell-Griner E, McFann K, Nahin RL. Complementary and alternative medicine use among adults: United States, 2002. Semin in Integr Med. 2004;2:54–71. doi:10.1016/j.sigm.2004.07.003 2. Saper RB, Eisenberg DM, Davis RB, Culpepper L, Phillips RS. Prevalence and patterns of adult yoga use in the United States: results of a national survey. Altern Ther Health Med. 2004;10:44–49. 3. Cherniack EP, Senzel RS, Pan CX. Correlates of use of alternative medicine by the elderly in an urban population. J Altern Complement Med. 2001;7:277–280. doi:10.1089/107555301300328160 4. Astin JA, Pelletier KR, Marie A, Haskell WL. Complementary and alternative medicine use among elderly persons: one-year analysis of a Blue Shield Medicare supplement. J Gerontol A Biol Sci Med Sci. 2000;55:M4–M9. doi:10.1093/gerona/55.1.M4

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