ReviewThe effects of cardiovascular exercise on human memory: A review with meta-analysis
Introduction
The American College of Sports Medicine defines cardiovascular exercise as the “type of physical activity that uses large muscle groups, can be maintained continuously and is rhythmic in nature” (ACSM, 2010). Besides the well-established benefits that the practice of this type of exercise has on different elements of the physical well-being (Penedo and Dahn, 2005), a growing body of research has recently evidenced the positive role that cardiovascular exercise plays in maintaining or even enhancing different aspects of cognition (Hillman et al., 2008). The general view is that cardiovascular exercise produces positive effects on the performance of some cognitive tasks, especially those tasks requiring executive-control that involve the activation of frontal areas of the brain (Colcombe and Kramer, 2003). The vast majority of studies assessing the effects of cardiovascular exercise on cognition, however, have primarily employed neuropsychological tasks targeting mainly attention, decision-making and speed processing (e.g. simple or choice reaction time). In contrast, much less emphasis has been placed on investigating the effects of this type of exercise on cognitive tasks involving memory (Erickson et al., 2011). Furthermore, since there is a paucity of studies examining how cardiovascular exercise affects human learning (Holzschneider et al., 2012), there exist no consensus in regards to whether the beneficial effects that cardiovascular exercise shows on the performance of tasks involving executive-control (Colcombe and Kramer, 2003, Kramer et al., 1999) can be extended to other cognitive tasks requiring the acquisition and retention of newly acquired information.
Recent data have revealed that the practice of cardiovascular exercise triggers a cascade of neurobiological mechanisms that may have an enhancing effect on memory processing in humans (Cotman and Berchtold, 2002, Cotman et al., 2007). For example, two bouts of 3 min of intense treadmill running performed before practicing an associative vocabulary task have been shown to increase the peripheral concentration of catecholamines involved in the consolidation of memory such as dopamine (Chowdhury et al., 2012) and epinephrine (Cahill and Alkire, 2003), accelerate the rate of vocabulary learning by 20% and optimize long-term word recall (Winter et al., 2007). In a more recent investigation, Segal et al. (Segal et al., 2012) showed that 6 min of moderate to intense cycling performed after the presentation of 20 images was sufficient to enhance image recall in a group of healthy elderly as well as in patients with mild cognitive impairment. Notably, the improvement of visual memory was associated to an increase in the post-exercise concentration of norepinephrine, another catecholamine involved in the regulation of emotional memory (Segal and Cahill, 2009). Furthermore, a longitudinal randomized controlled trial (RCT) including 120 elderly subjects showed that 12 months of moderate intensity cardiovascular exercise produced an increase in hippocampal volume which was associated to an improvement in visuo-spatial memory (Erickson et al., 2011). Thus, there exist data suggesting that the positive effects of cardiovascular exercise could also be obtained in other more complex tasks involving memory processing and learning.
Nevertheless, the evidence in support of the use of cardiovascular exercise to improve memory in humans is far from having been established convincingly. Examples of studies showing positive (Hotting et al., 2012), no effects (Madden et al., 1989) or even detrimental effects (Eich and Metcalfe, 2009) of this type of exercise on memory are abundant in the literature. Inconsistencies may stem, in part, from the use of different cardiovascular interventions that trigger specific mechanisms (Hopkins et al., 2012, Kennard and Woodruff-Pak, 2012) with differential effects on different types of memory (Eich and Metcalfe, 2009, Lin et al., 2012). Investigations exploring the effects of cardiovascular exercise on memory have traditionally employed either acute or long-term interventions. By definition, acute interventions involve the performance of a single bout of exercise while long-term interventions consist of multiple single exercise bouts performed at different time points during several weeks or months. In reference to memory processes, however, these two interventions can also be distinguished by the temporal relationship established between the exercise stimulus and the memory formation process. The effects of acute exercise on memory are thought to be time-dependent, with different stages of the formation of memory (i.e. acquisition, consolidation, recall) being facilitated depending on whether the exercise bout is performed before, during or after encoding a specific memory trace (Roig et al., 2012). In contrast, the effects of long-term exercise do not depend on the temporal coupling between the exercise stimulus and the memory formation process but on the cumulative effects that regular bouts of exercise have on the brain machinery responsible for memory processing in general.
The rationale for using acute exercise to improve memory is usually founded upon psychological (Audiffren, 2009) and biological (McMorris, 2009) grounds. Psychological theories argue that a single bout of exercise optimizes the level of arousal and thus may facilitate cognitive processing (Audiffren et al., 2008) and memory consolidation (McGaugh, 2006). Biological theories, in contrast, attribute the benefits of acute exercise to a transient increase of neurotransmitters such as epinephrine (Cahill and Alkire, 2003) and dopamine (Chowdhury et al., 2012), which are thought to play an important role in memory processing. The use of long-term cardiovascular exercise to maintain or improve memory is based on the positive adaptations that regular bouts of exercise have shown to produce on some of the structures (Colcombe et al., 2006) and functions (Voss et al., 2010) of the brain that support memory formation processes (Erickson et al., 2011). Thus, while both paradigms share underlying mechanisms, acute and long-term cardiovascular interventions represent two fundamentally distinct exercise strategies to improve memory (Hopkins et al., 2012).
Previous reviews of the literature have assessed the evidence in support of the use of physical activity to improve and maintain cognition (Angevaren et al., 2008, Smith et al., 2010). However, several studies with new data have appeared since those reviews were published. In addition, the majority of reviews have analyzed the effects of combined exercise interventions (e.g. cardiovascular and resistance exercise) on different cognitive functions in both healthy and diseased elderly subjects (van Uffelen et al., 2008). Unless appropriate subgroup analyses are conducted, pooling together studies with different populations, interventions and outcomes tend to increase the heterogeneity of the analysis and compromises the outcome of the review. To our knowledge, a comprehensive meta-analysis exploring independently the effects of either acute or long-term cardiovascular interventions on different types of memory in healthy subjects is currently lacking. The comparison between these two types of interventions has important practical implications due to the potential selective effects of acute and long-term cardiovascular exercise on different types of memory (Hopkins et al., 2012). We therefore performed an updated meta-analysis of the literature to assess the evidence in support of the benefits of each of these two exercise strategies on human memory. To gain further insight into the specific mechanisms modulating the relationship between cardiovascular exercise and memory we stratified the meta-analysis into different types of memory and conducted subgroup analyses to explore potential effect moderators. We also discussed potential biological mechanisms underlying the effects of acute and long-term cardiovascular exercise on memory. This meta-analysis was reported following the guidelines of the Preferred Reporting Items for Systematic Reviews and Meta-analyses (Moher et al., 2009).
Section snippets
Search strategy
Two of the authors (MR, SN) performed independently the electronic search on the following databases: PubMed (1951–present), MEDLINE (1894–present), PsychINFO (1981–present), EMBASE (1970–present) and SPORTDiscus (1985–present). Reference lists of previous reviews containing studies related to the topic of interest were also screened. The electronic search was not language restricted but it was limited to studies completed on human subjects. The search included between-subjects designs such as
Reporting bias
Funnel plots including studies with short (Fig. 1) and long-term (Fig. 2) cardiovascular interventions and their effects on memory in general showed a very symmetrical distribution. This distribution indicates that the intervention effects estimated in smaller studies did not differ from those estimated in larger studies (Higgins and Green, 2011). Therefore, we found no evidence of small-study effects that could suggest a high risk of reporting (e.g. publication) bias at study level. The fact
Acute and long-term cardiovascular exercise have differential effects on different types of memory
In line with the results of previous reviews assessing the effects of physical activity on other cognitive functions (Chang et al., 2012, Smith et al., 2010) our meta-analysis showed that, in general, cardiovascular exercise had small to moderate effects on memory. However, a more stratified analysis of the data revealed that acute interventions produced a relatively large improvement in some aspects of long-term memory (Fig. 4) while the effects on short-term memory were more moderate. In
Conclusions
Acute and long-term cardiovascular interventions show differential effects on memory. Acute exercise produces moderate to large effects on long-term memory and more moderate effects on short-term memory whereas long-term cardiovascular exercise does not have any significant effect on long-term memory and produces only small improvements in short-term memory. We argue that both interventions represent two distinct but complementary strategies to improve memory. Acute exercise improves memory in
Limitations
Given the small number of comparisons and complex interaction between different moderators the results of moderator analyses should be interpreted with caution. For example, although young-adults with moderate fitness levels tended to show the largest effects on memory we could not confidently determine the exact role of age and physical fitness in modulating the effects of cardiovascular exercise on memory. Similarly, it would have been too speculative with the data available to discuss how
Directions for further research
Most rodent studies exploring the mechanisms of exercise on memory have investigated the effects of long-term cardiovascular exercise on hippocampal-related memory tasks (Vaynman et al., 2004). More animal studies exploring potential mechanisms underlying the effects of different types of cardiovascular exercise on different types of memory and learning are therefore necessary. The use of animal models would be especially useful to study the temporal patterns delineating the effects of acute
Acknowledgments
We specially thank Drs. Michel Audiffren (Université de Poitiers, France), Sabrina Segal (University of California Irvine, USA), Tracey Covassin (Michigan State University, USA), Áine Kelly (Trinity College Dublin, Ireland) and Tomas Gualtieri (North Carolina Neuropsychiatry Clinic, USA) for providing data necessary for conducting the meta-analysis. We also want to thank Henriette Arnoldus (Copenhagen University) for her diligent support during the process of retrieval of papers.
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