Elsevier

Neurobiology of Aging

Volume 33, Issue 8, August 2012, Pages 1690-1698
Neurobiology of Aging

Regular paper
Resistance training and functional plasticity of the aging brain: a 12-month randomized controlled trial

https://doi.org/10.1016/j.neurobiolaging.2011.05.010Get rights and content

Abstract

Maintaining functional plasticity of the cortex is essential for healthy aging and aerobic exercise may be an effective behavioral intervention to promote functional plasticity among seniors. Whether resistance training has similar benefits on functional plasticity in seniors has received little investigation. Here we show that 12 months of twice-weekly resistance training led to functional changes in 2 regions of cortex previously associated with response inhibition processes—the anterior portion of the left middle temporal gyrus and the left anterior insula extending into lateral orbital frontal cortex—in community-dwelling senior women. These hemodynamic effects co-occurred with improved task performance. Our data suggest that resistance training improved flanker task performance in 2 ways: (1) an increased engagement of response inhibition processes when needed; and (2) a decreased tendency to prepare response inhibition as a default state. However, we highlight that this effect of resistance training was only observed among those who trained twice weekly; participants of the once-weekly resistance training did not demonstrate comparable response profiles, both in behavioral performance and hemodynamic activity in cortex. In sum, our findings suggest that twice-weekly resistance training in seniors can positively impact functional plasticity of response inhibition processes in cortex, and that it does so in a manner that complements the effects on selective attention that have previously been ascribed to aerobic exercise in seniors.

Introduction

The world's population is aging—at a rate that is unprecedented in human history. Maintaining functional plasticity of the cortex is essential for healthy aging, but how can this be promoted at a population level? One promising approach is exercise, which comes in 2 distinct forms—aerobic training, such as running, and resistance training, such as lifting weights. In rats, aerobic exercise training increased levels of brain-derived neurotrophic factors (Neeper et al., 1995) which, in turn, increased neuronal survival, synaptic development, and plasticity (Barde, 1994, Cotman and Engesser-Cesar, 2002, Lu and Chow, 1999). Neuroanatomical studies show that these central benefits of aerobic exercise training are also found in older adults and were most evident in cortical regions that typically show the greatest age-related declines (Colcombe et al., 2003, Colcombe et al., 2004). However, aerobic exercise training requires relatively healthy joints and a degree of cardiovascular fitness; both of these can be limited in seniors.

In comparison, resistance training is a familiar form of exercise for many Baby Boomers and it is feasible even for those with limited mobility or cardiovascular fitness. Two studies to date have demonstrated the beneficial effect of progressive resistance training on cognitive performance among older adults (Cassilhas et al., 2007, Liu-Ambrose et al., 2010). Specifically, Cassilhas (2007) demonstrated that 6 months of either thrice-weekly moderate- or high-intensity resistance training improved cognitive performance of memory and verbal concept formation among senior men. We recently demonstrated that 12 months of progressive resistance training once- or twice-weekly improved selective attention and conflict resolution, relative to twice-weekly balance and toning exercises in senior women. However, whether resistance training affects functional plasticity is currently unknown.

Studies with intermediate outcome measures from both human trials and laboratory experiments justify examination of resistance training and functional plasticity. In humans, resistance training reduced serum homocysteine (Vincent et al., 2003) and increased levels of insulin-like growth factor 1 (IGF-1) (Borst et al., 2001, Cassilhas et al., 2007). Increased homocysteine levels are associated with impaired cognitive performance (Schafer et al., 2005), Alzheimer's disease (Seshadri et al., 2002), and cerebral white matter lesions (Vermeer et al., 2002). In rat models, elevated levels of homocysteine are neurotoxic (Kruman et al., 2000). In contrast, IGF-1 promotes neuronal growth, survival, and differentiation and improves cognitive performance (Cotman and Berchtold, 2002).

If resistance training had similar, or complementary, positive effects on functional plasticity as aerobic exercise training, it would allow a greater portion of the aging population to utilize another powerful exercise intervention strategy with multiple benefits. Based on the previous work of Colcombe and colleagues (2004) on aerobic exercise training and cortical functioning associated with selective attention and conflict resolution, we hypothesize that resistance training will increase activation in the frontal and parietal cortices—specifically, the middle frontal gyrus, superior frontal gyrus, and superior parietal lobe—and will reduce activation in the anterior cingulate cortex. However, given that no previous studies have examined the potential effect of resistance training on cortical functioning associated with selective attention and conflict resolution, it is possible that we will identify nonoverlapping regions of the brain. Here we report the results of a 12-month randomized controlled trial that suggest that twice-weekly resistance training produces positive effects on functional plasticity among community-dwelling senior women.

Section snippets

Study design

We conducted a randomized, controlled 52-week prospective study of exercise from May 2007 to April 2008. The assessors were blinded to the participants' assignments.

Participants

The sample has been described in detail previously (Liu-Ambrose et al., 2010). Briefly, women who lived in Vancouver, Canada, were eligible for study entry if they: (1) were aged 65 to 75 years; (2) were living independently in their own home; (3) scored ≥ 24 on the Mini Mental State Examination (MMSE); and (4) had a visual acuity

Participants

A total of 88 participants were scanned by fMRI at baseline. Seventeen of the 88 participants did not complete scanning at trial completion. An additional 19 participants were excluded because of: (1) left-handedness (n = 5); (2) excessive head motion (i.e., > 2 mm) during the baseline scan (n = 4) or during the trial completion scan (n = 2); (3) data acquisition problems (e.g., warping in data; n = 5); or (4) 0% accuracy on their performance of the cognitive-challenging task (n = 3). Fifty-two

Discussion

Our findings indicate that senior women who engaged in twice-weekly resistance training significantly improved their performance on the flanker task; this co-occurred with positive functional changes in hemodynamic activity in regions of cortex commonly associated with response inhibition processing in flanker-type tasks—the left anterior insula extending into lateral orbital frontal cortex and the anterior portion of the left middle temporal gyrus (Banich et al., 2000, Boehler et al., 2010, de

Disclosure statement

All authors have nothing to declare.

Ethical approval was obtained from the Vancouver Coastal Health Research Institute and the University of British, Columbia's Clinical Research Ethics Board. All participants provided written informed consent.

Acknowledgements

The authors thank the Vancouver South Slope YMCA management and members who enthusiastically supported the study by allowing access to participants for the training intervention. The authors are indebted to Ms. Lindsay Katarynych for coordinating this study. We thank the instructors for their commitment to the participants' health and safety.

The Vancouver Foundation (BCMSF, Operating Grant to TLA), Natural Sciences and Engineering Research Council of Canada (NSERC, Operating Grant to TCH), and

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