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Treadmill walking during vocabulary encoding improves verbal long-term memory

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Many anecdotal reports suggest that physical activity is beneficial for problem solving or memorizing of new information. For example, simultaneous promenading and reciting of text passages used to be a relevant part of the daily routine of ancient philosophers and monks. Pacing up and down the room during declarative learning and promenading while restructuring a complex problem has been reported to be helpful [1]. Hence, various field reports have indicated that simultaneous motor activity may enhance cognitive resources.

In the current article we distinguish between physical exercise and motor activity. We use the term motor activity to refer to any movements of very low intensity, i.e. finger tapping or promenading, while the term exercise is exclusively used for motor activity with an intensity of at least 46% VO2max which should induce changes in physical fitness and health [2]. With regard to the latter, there is increasing evidence that single bouts of physical exercise prior to a specific task improve cognitive functions. This has been shown for the speed of information processing [3-5], executive functions such as performance in Eriksen flanker task, Trail making test, or Stroop interference [6, 7], enhanced cognitive flexibility [8], and mnemonic functions such as working memory [9, 10], or long term memory [11-13]. There is evidence that the timing of exercise relative to a memory task modulates its effect. Labban and Etnier [14] showed that an acute exercise bout of moderate intensity prior to, but not after exposition to memory items resulted in a significantly better memorization compared to no exercise. Additionally, Salas et al. [12] found that walking (approximately moderate intensity, i.e. “the walking speed one would use when late to an appointment”, p. 509) prior to encoding but not prior to retrieval enhanced performance in a free recall task. Hence, acute exercise seems to be particularly beneficial for memory if temporally close to encoding. However, Winter et al. [13] found that although high-intensity exercise prior to learning results in faster vocabulary acquisition, neither high- nor low-intensity exercise led to enhanced vocabulary retention on the same day, after 1 week or after 8 months. In a similar vein, Coles and Tomporowski [11] found no positive effect of moderate-intensity bicycling prior to a free-recall test in comparison to sitting on a cycling ergometer or watching an educational documentary. With regard to simultaneous motor activity, a dual task effect might result in lower performance (for a comprehensive overview see [15]). Several studies have shown that low-intensity walking during memorizing impairs performance even in young and healthy adults (e.g. [15-18]; however see [19] for contrary effects in 9-year-olds). Results from our lab indicate the opposite: in two learning studies and an attention allocation experiment, low- and moderate-intensity simultaneous bicycling resulted in better performance compared to being sedentary [20-22]. In the current experimental series we investigated the effect of treadmill walking during vocabulary encoding on subsequent memory performance. We specifically aimed to investigate the effect of very low-intensity motor activity (approx. < 50% VO2max), i.e. far below the intensity levels typically investigated in studies on exercise and cognitive performance.

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The search for endocrinological parameters mediating the effect of physical activity on mnemonic processes has focused on the brain-derived neurotrophic factor (BDNF) [13, 23]. Several studies have indicated that BDNF levels are associated with cognitive processes such as memory (e.g., [24, 25]), and that acute exercise of at least moderate intensity elevates both serum and plasma BDNF in humans (e.g., [13, 26-31]). However, in our study on moderate-intensity bicycling during vocabulary encoding we did not find significant correlations between serum BDNF and learning performance [20], possibly because the motor activity was not sufficiently intense. This is in line with our observation that only high-, but not low-intensity bicycling results in a (transient) increase of BDNF in serum [29]. We measured BDNF in the first of the present two experiments because of its putative relevance for cognitive performance. However we did not expect it to be modulated by the present low-intensity motor activity.

Instead we tested in the second experiment an alternative explanation for the positive effect of exercise on cognition i.e., the arousal hypothesis (e.g. [32]). In a review, Tomporowski [33] found evidence for the relationship between cognition and physical arousal following the Yerkes-Dodson law [34]. Levitt & Gutin [35] reported faster reaction times for moderately increased heart rates, but slower reaction times at highly increased heart rates. According to a model by Kahneman [32] simultaneous low-intensity exercise increases the arousal level which in turn increases the resources available to perform a cognitive task. If on the other hand exercise withdraws resources necessary to perform the cognitive task, this should result in interference. In this case, the mental workload required by exercise would be too high to manage the cognitive task (cf. [36]). Furthermore physical exercise, at least at high intensity levels, has been reported to increase psycho-physiological stress which in turn increases the arousal level [37]. This affects salivary cortisol responses reflecting individual stress levels [38]. Hence, motor activity in combination with a cognitive task should increase the “participants’ arousal” and stress levels which may lead to deflections in salivary cortisol concentrations. Indeed Almela et al. [39] have shown that a higher stress-related cortisol response negatively influences memory performance in middle-aged women. However, others found beneficial effects of stress on memory (e.g. [40]). We investigated this issue in the current series of experiments.

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Taken together, previous experiments on physical exercise and long-term memory as well as their endocrinological substrates have yielded inconsistent results. Our own data have indicated that physical activity during encoding is particularly beneficial for vocabulary learning, even for low to medium exercise intensity. In the current study, we further reduced exercise intensity resulting in an experimental condition where subjects were motorically active with minimal cardio-vascular load. Hence, we tested the anecdotal effect of promenading on cognition under controlled experimental conditions. In contrast to our previous studies [20, 22], we tested equal numbers of male and female participants. Hence, we overcame a limitation of previous exercise studies testing either male or female subjects, or where the factor sex has not been parallelized (e.g. [10, 13, 14]). This is an important issue as previous studies have indicated that females may show better episodic memory functions than males [41, 42]. Furthermore, we applied a within-subject design to assess the effect of slow treadmill walking on auditory vocabulary encoding, thus increasing the statistical power compared with between-subject designs. In the first experiment we measured BDNF in serum because of its putative relevance for cognitive performance, even though we did not expect it to be modulated by the present low-intensity activity. In a second experiment we followed the stress-arousal hypothesis and collected salivary cortisol.

We hypothesized that participants would show better learning performance during walking compared to the sedentary condition. However, previous studies showed that treadmill exercise may require cognitive resources, and hence subjects who are less familiar or confident on a treadmill might perform worse. In a recent review, Lambourne and Tomporowski [43] concluded that simultaneous cycling improved cognitive performance whereas simultaneous treadmill exercise deteriorated performance. This discrepancy was attributed to increased demands of treadmill exercise on keeping balance and on upper and lower limb coordination, possibly interfering with cognitive task demands. Hence, we asked the participants to rate how safe they felt on the treadmill to control for this issue. In line with our previous results, we expected BDNF in serum not to be elevated by walking. However, salivary cortisol should be increased in the walking condition compared to the sedentary condition due to increased arousal. Furthermore, performance in vocabulary tests should correlate positively with changes in salivary cortisol during encoding.

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