Differential effects of adolescent and adult-initiated exercise on cognition and hippocampal neurogenesis

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Date
2019-09-22
Authors
O'Leary, James D.
Hoban, Alan E.
Murphy, Ashley
O'Leary, Olivia F.
Cryan, John F.
Nolan, Yvonne M.
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Wiley
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Abstract
Adolescence is a critical period for postnatal brain maturation and thus a time when environmental influences may affect cognitive processes in later life. Exercise during adulthood has been shown to increase hippocampal neurogenesis and enhance cognition. However, the impact of exercise initiated in adolescence on the brain and behavior in adulthood is not fully understood. The aim of this study was to compare the impact of voluntary exercise that is initiated during adolescence or early adulthood on cognitive performance in hippocampal-dependent and -independent processes using both object-based and touchscreen operant paradigms. Adult (8 week) and adolescent (4 week) male Sprague-Dawley rats had access to a running wheel (exercise) or were left undisturbed (sedentary control) for 4 weeks prior to behavioral testing and for the duration of the experiment. Results from touchscreen-based tasks showed that reversal learning was enhanced by both adult and adolescent-initiated exercise, while only exercise that began in adolescence induced a subtle but transient increase in performance on a location discrimination task. Spontaneous alternation in the Y-maze was impaired following adolescent onset exercise, while object memory was unaffected by either adult or adolescent-initiated exercise. Adolescent-initiated exercise increased the number of hippocampal DCX cells, an indicator of neurogenesis. It also promoted the complexity of neurites on DCX cells, a key process for synaptic integration, to a greater degree than adult-initiated exercise. Together the data here show that exercise during the adolescent period compared to adulthood differentially affects cognitive processes and the development of new hippocampal neurons in later life.
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Neurogenesis , Running , Touchscreen operant behavior , Touchscreen operant platform , Dentate granule cells , Social isolation , Object recognition , Pattern separation , Aerobic fitness , Spontaneous alternation , Memory impairment , Brain development , BDNF
Citation
O'Leary, J. D., Hoban, A. E., Murphy, A., O'Leary, O. F., Cryan, J. F. and Nolan, Y. M. (2019) 'Differential effects of adolescent and adult-initiated exercise on cognition and hippocampal neurogenesis', Hippocampus, 29(4), pp. 352-365. doi: 10.1002/hipo.23032
Copyright
© 2018 Wiley Periodicals, Inc. This is the peer reviewed version of the following article: O'Leary, JD, Hoban, AE, Murphy, A, O'Leary, OF, Cryan, JF, Nolan, YM. Differential effects of adolescent and adult‐initiated exercise on cognition and hippocampal neurogenesis. Hippocampus. 2019; 29: 352– 365, which has been published in final form at https://doi.org/10.1002/hipo.23032 This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Self-Archiving.