Physical activity and memory functions: An interventional study
Introduction
During the aging process, a deterioration in a broad array of cognitive processes (Hedden and Gabrieli, 2004) has been documented. The structural integrity of the brain likewise declines, particularly in the frontal, parietal, and temporal lobes (Jernigan et al., 2001, Raz et al., 2004), and decreases are found in neurochemical systems, most notably in dopaminergic, noradrenergic, and cholinergic pathways (Eriksdotter-Nilsson et al., 1989, Jouvenceau et al., 1998, Wise, 2004, Floel et al., 2006). Thus, the rapidly increasing proportion of elderly individuals in our society will be paralleled by an increase of individuals with cognitive impairment and dementia (Pressley et al., 2003). Given the staggering medical and nursing home expenses associated with cognitive deterioration (Infeld and Whitelaw, 2002, Sadik and Wilkock, 2003), it is becoming an imperative public health goal to identify effective mechanisms for warding off structural and functional decline of the central nervous system. Epidemiological and interventional studies for the larger part support the role of exercise in late life as a means to prevent or delay the onset of mild cognitive impairment or dementia (Laurin et al., 2001, Barnes et al., 2003, Colcombe et al., 2003, Colcombe et al., 2004a), but several important questions remain unanswered.
First, it is not clear whether physical activity may enhance episodic memory functions, since previous interventional studies in elderly individuals examined only performance in frontal-executive, or attentional, tasks (Colcombe et al., 2003, Colcombe et al., 2004a). Since the cardinal feature of dementia of the Alzheimer type and its precursor, “mild cognitive impairment”, is an impairment of episodic memory functions (Blacker et al., 2007), the most important cognitive domain to be targeted is the domain of episodic memory. Previous animal studies that examined the effects of exercise on behaviour and brain structure focused on episodic memory, and found increases in spatial memory tasks, as well as increases in neurogenesis and neurotrophic factors in task-related brain regions (most importantly hippocampus and parahippocampus (Gomez-Pinilla et al., 1997, van Praag et al., 1999a, van Praag et al., 1999b, Vaynman and Gomez-Pinilla, 2006)).
Second, the mechanisms underlying the beneficial effect of physical activity in the human brain are incompletely understood. Animal studies, as well as a short-term interventional human study, suggest that physical activity leads to increases in catecholamines and neurotrophins, possibly mediating changes in cognition and episodic memory (van Praag et al., 1999a, van Praag et al., 1999b, Vaynman et al., 2006a, Winter et al., 2007), but this issue has not been examined in an interventional long-term approach in humans. Local gray matter volume and cerebral blood volume have been studied previously in longitudinal studies, but results have been mixed, with some reports suggesting changes primarily in prefrontal and supplementary motor, and cingulate cortex (Colcombe et al., 2005, Colcombe et al., 2006), and others changes in medial temporal cortex (Pereira et al., 2007).
Third, it is not clear if memory functions are differentially affected in low-intensity physical activity vs. medium-intensity physical activity. Recent studies have suggested that any energy expenditure through activity in older adults can help lower mortality risks (Manini et al., 2006), and contradicts the previously held belief that exercise needs to be performed at a specific intensity to confer a significant health benefit (Pate et al., 1995, Stiggelbout et al., 2004). A recent cross-sectional study of our own group showed that level of overall physical activity may be more important for memory functions than cardiovascular-effective sport regimes or aerobic fitness per se (Floel et al., 2007). So far, the impact of different intensity levels of physical activity on episodic memory in healthy elderly individuals has not been examined in an interventional approach.
To address these questions, we assessed the influence of different physical activity regimes, as well as increase in total energy expenditure by physical activity, on the performance in an episodic memory task, in a 6 months interventional approach. In parallel, we examined neurotrophin and catecholamine levels, and local gray matter volume, to test the hypothesis that these parameters may be mediators between physical activity and episodic memory. Based on our assumption that physical activity would primarily benefit episodic memory encoding and retrieval, we expected changes in frontal cortex (Fletcher and Henson, 2001), and medial temporal lobe structures (Squire et al., 1992).
Section snippets
Subjects
Participants were 62 community-dwelling older adults (aged 50–72 years; mean 60.2 ± 6.6; 43 female). They were pre-screened for history of stroke, psychiatric illness, previous level of exercise, or dementia (defined on scores below 26 on the Mini-Mental State Examination (MMSE) (Folstein et al., 1975, Lezak, 2004)). To avoid ceiling effects, only sedentary individuals (less than two exercise sessions per week) were invited for further testing. Participants’ written informed consent was obtained
Baseline
Factorial ANOVA revealed no significant differences at baseline between the three groups for episodic memory score, walking speed at 2 mmol/l lactate, level of physical activity, depression scores (BDI), neurotrophin levels, and catecholamine levels (see Table 1 and Supplementary Table 1).
Intervention check
Participants in the nordic walking and gymnastic groups were required to sign up for at least three 50 min sessions per week and were allowed to miss up to 20% of the sessions over the entire 6 months. Analysis
Discussion
In this longitudinal study, we were able to demonstrate that an increase in physical activity led to improved episodic memory performance in elderly individuals. To achieve this aim, no high-intensity exercise was required. Rather, gymnastics, nordic walking, and activities embedded into the routines of daily life, sufficed. Moreover, no difference in increase of episodic memory was detected between the two intervention groups that participated either in low-level sport activity (gymnastics) or
Disclosure statement
None of the authors reports any conflict of interest or a financial interest.
Acknowledgements
This work was supported by grants from the Deutsche Forschungsgemeinschaft to A.F. (Fl 379-4/1), the IZKF to A.F. (Floe/3/004/08), the Bundesministerium für Forschung und Bildung to A.F and S.K. (01GW0520), and the Volkswagen Stiftung to S. K. (Az.: I/80 708).
References (131)
- et al.
Voxel-based morphometry—the methods
Neuroimage
(2000) - et al.
Unified segmentation
Neuroimage
(2005) - et al.
Cognitive and emotional influences in anterior cingulate cortex
Trends Cogn. Sci.
(2000) - et al.
Exercise: a behavioral intervention to enhance brain health and plasticity
Trends Neurosci.
(2002) - et al.
Training effects of long versus short bouts of exercise in healthy subjects
Am. J. Cardiol.
(1990) - et al.
Interactive effects of fitness and hormone treatment on brain health in postmenopausal women
Neurobiol. Aging
(2007) - et al.
Multiple changes in noradrenergic mechanisms in the coeruleo-hippocampal pathway during aging. Structural and functional correlates in intraocular double grafts
Neurobiol. Aging
(1989) - et al.
“Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician
J. Psychiatr. Res.
(1975) - et al.
Basal serum levels and reactivity of nerve growth factor and brain-derived neurotrophic factor to standardized acute exercise in multiple sclerosis and controls
J. Neuroimmunol.
(2003) - et al.
Physical exercise induces FGF-2 and its mRNA in the hippocampus
Brain Res.
(1997)
Striatal dopamine turnover during treadmill running in the rat: relation to the speed of running
Brain Res. Bull.
Nonstationary cluster-size inference with random field and permutation methods
Neuroimage
Influence of demographic, physiologic, and psychosocial variables on adherence to a yearlong moderate-intensity exercise trial in postmenopausal women
Prev. Med.
Dopamine: a potential substrate for synaptic plasticity and memory mechanisms
Prog. Neurobiol.
Effects of age on tissues and regions of the cerebrum and cerebellum
Neurobiol. Aging
Insulin-like growth factor-1 ameliorates age-related behavioral deficits
Neuroscience
Neuroprotective signaling and the aging brain: take away my food and let me run
Brain Res.
A test of the catecholamines hypothesis for an acute exercise-cognition interaction
Pharmacol. Biochem. Behav.
Structural brain alterations in subjects at high-risk of psychosis: a voxel-based morphometric study
Schizophr. Res.
Activation of the posterior cingulate by semantic priming: a co-registered ERP/fMRI study
Brain Res.
The assessment and analysis of handedness: the Edinburgh inventory
Neuropsychologia
Transport of brain-derived neurotrophic factor across the blood-brain barrier
Neuropharmacology
Permeability at the blood-brain and blood-nerve barriers of the neurotrophic factors: NGF, CNTF, NT-3, BDNF
Brain Res. Mol. Brain Res.
Combining spatial extent and peak intensity to test for activations in functional imaging
Neuroimage
Dementia in community-dwelling elderly patients: a comparison of survey data, medicare claims, cognitive screening, reported symptoms, and activity limitations
J. Clin. Epidemiol.
The myth of the visual word form area
Neuroimage
Aging, sexual dimorphism, and hemispheric asymmetry of the cerebral cortex: replicability of regional differences in volume
Neurobiol. Aging
Walking and dementia in physically capable elderly men
JAMA
Compendium of physical activities: an update of activity codes and MET intensities
Med. Sci. Sports Exerc.
The anterior cingulate cortex. The evolution of an interface between emotion and cognition
Ann. N Y Acad. Sci.
Potential therapeutic effects of exercise to the brain
Curr. Med. Chem.
Exercise treatment for major depression: maintenance of therapeutic benefit at 10 months
Psychosom. Med.
A longitudinal study of cardiorespiratory fitness and cognitive function in healthy older adults
J. Am. Geriatr. Soc.
Neuropsychological measures in normal individuals that predict subsequent cognitive decline
Arch. Neurol.
Tonic dopaminergic stimulation impairs associative learning in healthy subjects
Neuropsychopharmacology
D-amphetamine boosts language learning independent of its cardiovascular and motor arousing effects
Neuropsychopharmacology
Circulating insulin-like growth factor I mediates effects of exercise on the brain
J. Neurosci.
The precuneus: a review of its functional anatomy and behavioural correlates
Brain
Physical activity and the risk of Parkinson disease
Neurology
The primary motor and premotor areas of the human cerebral cortex
Neuroscientist
The frontopolar cortex and human cognition: evidence for a rostrocaudal hierarchical organisation within the human prefrontal cortex
Psychobiology
Field testing of physiological responses associated with Nordic Walking
Res. Q Exerc. Sport
Fitness effects on the cognitive function of older adults: a meta-analytic study
Psychol. Sci.
The implications of cortical recruitment and brain morphology for individual differences in inhibitory function in aging humans
Psychol. Aging
Aerobic fitness reduces brain tissue loss in aging humans
J. Gerontol. A Biol. Sci. Med. Sci.
Aerobic exercise training increases brain volume in aging humans
J. Gerontol. A Biol. Sci. Med. Sci.
Cardiovascular fitness, cortical plasticity, and aging
Proc. Natl. Acad. Sci. U.S.A.
Neurocognitive aging and cardiovascular fitness: recent findings and future directions
J. Mol. Neurosci.
Contributions of anterior cingulate cortex to behaviour
Brain
Cited by (361)
Long-term protective effects of physical activity and self-control on problematic smartphone use in adolescents: A longitudinal mediation analysis
2024, Mental Health and Physical ActivityAge-varying association between depression symptoms and executive function among older adults: Moderation by physical activity
2023, Journal of Psychiatric Research