Elsevier

Neuroscience

Volume 194, 27 October 2011, Pages 84-94
Neuroscience

Cognitive, Behavioral, and Systems Neuroscience
Research Paper
Physical exercise during adolescence versus adulthood: differential effects on object recognition memory and brain-derived neurotrophic factor levels

https://doi.org/10.1016/j.neuroscience.2011.07.071Get rights and content

Abstract

It is well established that physical exercise can enhance hippocampal-dependent forms of learning and memory in laboratory animals, commensurate with increases in hippocampal neural plasticity (brain-derived neurotrophic factor [BDNF] mRNA/protein, neurogenesis, long-term potentiation [LTP]). However, very little is known about the effects of exercise on other, non-spatial forms of learning and memory. In addition, there has been little investigation of the duration of the effects of exercise on behavior or plasticity. Likewise, few studies have compared the effects of exercising during adulthood versus adolescence. This is particularly important since exercise may capitalize on the peak of neural plasticity observed during adolescence, resulting in a different pattern of behavioral and neurobiological effects. The present study addressed these gaps in the literature by comparing the effects of 4 weeks of voluntary exercise (wheel running) during adulthood or adolescence on novel object recognition and BDNF levels in the perirhinal cortex (PER) and hippocampus (HP). Exercising during adulthood improved object recognition memory when rats were tested immediately after 4 weeks of exercise, an effect that was accompanied by increased BDNF levels in PER and HP. When rats were tested again 2 weeks after exercise ended, the effects of exercise on recognition memory and BDNF levels were no longer present. Exercising during adolescence had a very different pattern of effects. First, both exercising and non-exercising rats could discriminate between novel and familiar objects immediately after the exercise regimen ended; furthermore there was no group difference in BDNF levels. Two or four weeks later, however, rats that had previously exercised as adolescents could still discriminate between novel and familiar objects, while non-exercising rats could not. Moreover, the formerly exercising rats exhibited higher levels of BDNF in PER compared to HP, while the reverse was true in the non-exercising rats. These findings reveal a novel interaction between exercise, development, and medial temporal lobe memory systems.

Highlights

▶Physical exercise during adolescence had more durable effects on object memory and BDNF levels than exercise during adulthood. ▶Exercise during adolescence versus adulthood differentially affected BDNF levels in perirhinal cortex and hippocampus. ▶The data reveal a novel interaction between exercise, development, and medial temporal lobe memory systems involved in familiarity and recollection.

Section snippets

Experiment 1: exercise during adulthood

Experiment 1 was designed to replicate the finding that the effect of exercise on object recognition memory in adult male rats is transient (Hopkins and Bucci, 2010b). Recognition memory was tested immediately after 4 weeks of access to a running wheel and again 2 weeks after access to the running wheels was removed. The levels of BDNF protein in the PER and HP were measured at each time point 24 h after the memory test session.

Experiment 2: exercise during adolescence

The goal of Experiment 2 was to test whether a similar pattern of

Novel object recognition

As shown in Table 1, rats in the exercising and non-exercising groups exhibited comparable amounts of time exploring the objects during the sample session when tested immediately after the 4-week exercise period (P>0.8), as well as when they were tested with a new set of objects 2 weeks after exercise ended (P>0.3). Thus, exercise did not alter general exploratory behavior at either time point.

The discrimination ratios during the object recognition test sessions are illustrated in Fig. 1. When

Discussion

Experiment 1 replicated the finding that object recognition memory was enhanced in exercising rats versus non-exercisers immediately after a 4-week exercise regimen during adulthood, but not 2 weeks after the exercise regimen ended (Hopkins and Bucci, 2010b). Similarly, BDNF levels were increased in exercising rats compared to non-exercising rats immediately after exercise ended, consistent with prior research (Molteni et al., 2002, Adlard et al., 2004, Berchtold et al., 2005), but there were

Conclusion

Based on the present data and a growing literature focused on understanding how exercise-induced changes in neurobiology lead to cognitive improvement, we have put forth a model whereby physical exercise non-specifically primes cortical neuroplastic processes and pathways, effectively lowering the salience threshold for learning to occur in the brain region(s) that is/are engaged during a given experience. While this cognitive enhancement seems quite transient when exercise takes place during

Acknowledgments

This research was supported by NIH grant R01MH082893, a Dartmouth College Rockefeller Center Research Grant, and a Hodgson Undergraduate Research Award.

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    These authors contributed equally to this study.

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