Elsevier

Neuroscience

Volume 215, 26 July 2012, Pages 59-68
Neuroscience

Differential effects of acute and regular physical exercise on cognition and affect

https://doi.org/10.1016/j.neuroscience.2012.04.056Get rights and content

Abstract

The effects of regular exercise versus a single bout of exercise on cognition, anxiety, and mood were systematically examined in healthy, sedentary young adults who were genotyped to determine brain-derived neurotrophic factor (BDNF) allelic status (i.e., Val–Val or Val66Met polymorphism). Participants were evaluated on novel object recognition (NOR) memory and a battery of mental health surveys before and after engaging in either (a) a 4-week exercise program, with exercise on the final test day, (b) a 4-week exercise program, without exercise on the final test day, (c) a single bout of exercise on the final test day, or (d) remaining sedentary between test days. Exercise enhanced object recognition memory and produced a beneficial decrease in perceived stress, but only in participants who exercised for 4 weeks including the final day of testing. In contrast, a single bout of exercise did not affect recognition memory and resulted in increased perceived stress levels. An additional novel finding was that the improvements on the NOR task were observed exclusively in participants who were homozygous for the BDNF Val allele, indicating that altered activity-dependent release of BDNF in Met allele carriers may attenuate the cognitive benefits of exercise. Importantly, exercise-induced changes in cognition were not correlated with changes in mood/anxiety, suggesting that separate neural systems mediate these effects. These data in humans mirror recent data from our group in rodents. Taken together, these current findings provide new insights into the behavioral and neural mechanisms that mediate the effects of physical exercise on memory and mental health in humans.

Highlights

► Regular physical exercise enhanced recognition memory and decreased stress. ► Effects were only detected in participants who exercised on the final day of testing. ► An acute, single bout of exercise did not affect memory. ► Improvements in memory were only apparent in BDNF Val homozygotes. ► Exercise-induced changes in cognition were not correlated with mood/anxiety.

Introduction

Physical exercise of various intensities and durations can enhance cognition across the lifespan of humans (Cotman and Berchtold, 2002). For example, the amount of exercise during young adulthood can predict cognitive performance later in life (Dik et al., 2003). Similarly, long-term exercise can improve cognition (Davis et al., 2011), including executive function (Angevaren et al., 2008, Erikson and Kramer, 2009), and memory (Pérusse et al., 1997, Flöel et al., 2010), and decrease the risk for dementia (Colcombe and Kramer, 2003, Larson, 2008). However, there is significant variability in these findings due to differences in the exercise regimen and cognitive assessment (Kramer et al., 2005). Moreover, the literature is primarily comprised of retrospective rather than prospective studies (Lawlor and Hopker, 2001, Smith et al., 2010).

Among the few studies designed to test for a causal relationship between exercise and cognition, most used a single bout of exercise (Coles and Tomporowski, 2008, Hillman et al., 2009) and focused on executive function more than memory per se. Moreover, most studies report effects within 30 min of exercising, when effects on physiological arousal are still increased (Ferris et al., 2007, Winter et al., 2007). Thus, it is difficult to determine whether changes in cognition are due to mechanism(s) that are unique to exercise per se, or simply reflect differences due to generalized heightened arousal. The distinction between the effects of exercise and arousal is particularly important because of the unique constellation of neural mechanisms that are activated by each. For instance, the metabolic demands associated with exercise are associated with changes in MAP/ERK and CAMKII signaling as well as increases in ghrelin and UCP-2, all of which are regulated by brain-derived neurotrophic factor (BDNF; Molteni et al., 2002, Ding et al., 2006). By comparison, these neural changes would not necessarily be activated – or not in the same pattern – as a result of general autonomic arousal, which is typically associated with central and peripheral catecholaminergic regulation (Audiffren, 2009). Moreover, there has been no systematic and direct comparison between the effects of acute and regular exercise in the same study, which would further provide an opportunity to draw distinctions between any underlying mechanisms that are unique to exercise (which may develop over time in response to repeated bouts of exercise) versus those that result from arousal.

It also remains unclear whether the effects of exercise on cognition can be dissociated from changes in mood and anxiety. Several studies have demonstrated that exercise can positively affect mental health (Annesi, 2004, Larun et al., 2006, Tkacz et al., 2008), and a recent meta-analysis reported that exercise interventions lasting 3–12 weeks effectively reduce anxiety measures in sedentary participants with a chronic illness (Herring et al., 2010). However, not all exercise interventions have been shown to produce positive affective changes (Lennox et al., 1990). Further, although single bouts of exercise affect mood and anxiety (Berger and Owen, 1998, Hansen et al., 2001), assessment has typically taken place immediately after exercise. Finally, though previous studies have examined the efficacy of exercise to treat emotional disorders, little is known about the effects of exercise on psychiatrically healthy participants.

Substantial research has also focused on the neural substrates that underlie the behavioral effects of exercise. Rodent studies have demonstrated that an increase in BDNF mediates the cognitive effects of exercise (Van Hoomissen et al., 2004, Vaynman et al., 2004, Hopkins and Bucci, 2010). Moreover, a polymorphism in the human BDNF gene (Val66Met; Egan et al., 2003, Frielingsdorf et al., 2010) alters activity-dependent release of BDNF and affects learning, memory, and emotion (Egan et al., 2003, Hajcak et al., 2009, Lau et al., 2010, Soliman et al., 2010). It is currently unknown whether the allelic status of BDNF influences the degree to which an individual may benefit from exercise.

We addressed several of these issues by testing the effects of a single bout of exercise versus a 4-week exercise regimen on cognition and mood/anxiety in healthy, sedentary young adults. Participants were evaluated on a recognition memory task modified from one used to demonstrate exercise-induced improvements in rats (Hopkins and Bucci, 2010, Hopkins et al., 2011), thus enhancing the translational value of the study. Evaluations were conducted before and after the exercise intervention (or no exercise), and DNA samples were collected to determine if BDNF genotype influences the effects of exercise.

Section snippets

Participants

Seventy-five healthy young adults (ages 18–36) were recruited for this study based on sedentary lifestyle, which was defined as not having engaged in 20 min or more of purposeful physical activity more than two times a month over the previous 6 months; a definition at least strict as reported in other studies (Pérusse et al., 1997, Schachter et al., 2003). All participants were undergraduates from Dartmouth College or individuals recruited from the local Hanover, NH community. Prior to

Results

Of the 75 participants initially enrolled in the study, 21 were excluded from the analyses due to discontinuation (n = 10), compliance issues (n = 3), depression level (BDI score > 15; n = 4), incorrect task assignment (n = 3), and outlier on task performance (n = 1; object recognition accuracy data were more than 2 standard deviations from the mean on both Visits 1 and 2, as were BDI and STAI-Y1 data). Of the remaining 54 participants (average age = 20.6 ± 0.4 years), 13 were in the 0W− group (12 females/1

Discussion

We found that an acute exercise session combined with a regular exercise regimen augmented recognition memory and decreased perceived stress in sedentary, healthy young adults. In contrast, a single bout of exercise alone had no effect on recognition memory and increased self-reported stress. Further, the data indicate that a common genetic polymorphism may have an important role in the influence that exercise has on memory since the effects were only observed in participants who were

Conclusion

The present report presents data illustrating the beneficial effects of exercise on measures of cognition and psychological well-being in healthy individuals, and offers data identifying a genetic mediator of these effects. These data are more compelling because they broadly replicate previous findings in rats, showing a similar BDNF mediation of improvement in recognition memory as well as reduced anxiety-like behavior following exercise (Hopkins and Bucci, 2010, Hopkins et al., 2011). Given

Acknowledgements

This research was supported by a grant from the Rockefeller Center at Dartmouth College (DB & MH) and NIH grants R01MH082893 (DB) and R01MH080716 (PW). The authors thank Dr. Gregory Tsongalis and colleagues for processing the DNA samples, and Rachel Eggleston, Jennifer Buchholz, Matthew Miner, Dallis Fox, and Cynthia Akagbosu for assistance in collecting the data.

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