Forced and voluntary exercise differentially affect brain and behavior

Abstract

Abstract-The potential of physical exercise to decrease body weight, alleviate depression, combat aging and enhance cognition has been well-supported by research studies. However, exercise regimens vary widely across experiments, raising the question of whether there is an optimal form, intensity and duration of exertion that would produce maximal benefits. In particular, a comparison of forced and voluntary exercise is needed, since the results of several prior studies suggest that they may differentially affect brain and behavior. In the present study, we employed a novel 8-week exercise paradigm that standardized the distance, pattern, equipment and housing condition of forced and voluntary exercisers. Exercising rats were then compared with sedentary controls on measures previously shown to be influenced by physical activity. Our results indicate that although the distance covered by both exercise groups was the same, voluntary exercisers ran at higher speed and for less total time than forced exercisers. Although evidence of the neural and behavioral benefits of exercise is accumulating, the optimal type, duration and intensity of long-term physical activity have not been established. Laboratory animal models of chronic exercise are highly variable, with many studies utilizing ad libitum access to voluntary exercise wheels, while others employ comparably short bouts of forced exercise on a treadmill. Not surprisingly, studies of the same outcome measure produce different results, depending on whether a voluntary or forced exercise paradigm is used (for a recent review of these disparities, see Ang and Gomez-Pinilla, 2007). In addition, it is becoming increasingly recognized that no single exercise paradigm is likely to fulfill all therapeutic needs (Ang and Gomez-Pinilla, 2007;Cotman et al., 2007). Thus, it is imperative to study the neural and behavioral effects of different forms of chronic exercise while holding their parameters constant.Human studies have attempted to pinpoint the optimal intensity level at which acute exercise maximally benefits cognition (Winter et al., 2007;McMorris et al., 2008, see Brisswalter et al., 2002 for a useful review), event-related brain potentials (ERP's) (Kamijo et al., 2004b(Kamijo et al., , 2007 and arousal level (Kamijo et al., 2004a). The most beneficial intensity, duration and type of long-term physical activity have not been well-studied in laboratory animals, however. The type of exercise may be particularly important, since several lines of evidence suggest that forced exercise and voluntary exercise exert different effects on the brain and behavior. For example, forced and voluntary exercise differentially affect monoamine neurotransmitters (Dishman, 1997), hippocampal parvalbumin expression (Arida et al., 2004), hippocampal brain-derived neurotrophic factor and synapsin-1 expression (Ploughman et al., 2005), longevity and body composition (Narath et al., 2001), taste aversion learning (Masaki and Nakajima, 2006) and open-field behavior (Burghardt et al., 2004...

Long-term voluntary exercise, representing habitual exercise, lowers visceral fat and alters plasma amino acid levels in mice

“…Habitual voluntary long-term exercise is believed to have a beneficial effect on human behavior and sleep [43,44]. Moreover, rodents using a running wheel voluntarily for a long period showed beneficial effects on behavior [45][46][47]. In a preliminary experiment on novelty-induced activity by means of an open-field test, Ex-mice at 25 weeks of age (exercise for 19 weeks) showed significantly higher values during 10-min observational periods than Se-mice of the same age (Ex-mice vs. Se-mice; 361 ± 31 vs. 252 ± 30 counts, n = 8, p \ 0.05), suggesting that Ex-mice are relatively resistant to anxiety [48,49].…”

Corticosterone and dopamine D2/D3 receptors mediate the motivation for voluntary wheel running in C57BL/6J mice

“…However, by comparing forced and voluntary wheel running, it was shown that both procedures increased behavioural and neurochemical indices of reward, which appeared elicited by distinct mechanisms possibly differentiating the motivation to exercise from its rewarding effects [9]. Furthermore, similar levels of forced and voluntary wheel running were found associated with an increase in hippocampal neurogenesis that was greater in the forced exercise group who also showed increased anxiogenic-like behaviour [10]. Thus, altogether these data suggest that the motivation to exercise can exert effects on brain and behaviour that are independent of exercise levels.…”

Are Voluntary Wheel Running and Open-Field Behavior Correlated in Mice? Different Answers from Comparative and Artificial Selection Approaches

“…It has been shown that intense physical activity subsequently alters behavior in the open-field, but the results are inconsistent, ranging from reduced (Duman et al 2008;Fuss et al 2010), unaffected (Leasure and Jones 2008), to increased locomotion (Burghardt et al 2004) in rodents after voluntary wheel running. Several environmental factors might have contributed to differences among those studies (e.g., the level of physical activity and housing conditions).…”