High impact running improves learning

https://doi.org/10.1016/j.nlm.2006.11.003Get rights and content

Abstract

Regular physical exercise improves cognitive functions and lowers the risk for age-related cognitive decline. Since little is known about the nature and the timing of the underlying mechanisms, we probed whether exercise also has immediate beneficial effects on cognition. Learning performance was assessed directly after high impact anaerobic sprints, low impact aerobic running, or a period of rest in 27 healthy subjects in a randomized cross-over design. Dependent variables comprised learning speed as well as immediate (1 week) and long-term (>8 months) overall success in acquiring a novel vocabulary. Peripheral levels of brain-derived neurotrophic factor (BDNF) and catecholamines (dopamine, epinephrine, norepinephrine) were assessed prior to and after the interventions as well as after learning. We found that vocabulary learning was 20 percent faster after intense physical exercise as compared to the other two conditions. This condition also elicited the strongest increases in BDNF and catecholamine levels. More sustained BDNF levels during learning after intense exercise were related to better short-term learning success, whereas absolute dopamine and epinephrine levels were related to better intermediate (dopamine) and long-term (epinephrine) retentions of the novel vocabulary. Thus, BDNF and two of the catecholamines seem to be mediators by which physical exercise improves learning.

Introduction

Physical exercise seems to be beneficial to cognition. Epidemiological studies show that more frequent (self-reported) regular physical activity is associated with a reduced risk for age-related neurodegenerative diseases, like dementia or Parkinson’s disease (Abbott et al., 2004, Colcombe et al., 2004, Larson et al., 2006, Laurin et al., 2001, van Gelder et al., 2004, Weuve et al., 2004). Beneficial effects of exercise on cognition may, however, be due to an overall healthier life style (non-smoking, better nutrition) in already cognitively high functioning subjects (Abbott et al., 2004, Kalmijn et al., 2000). Another confounder is that a preexisting, yet undiagnosed cognitive disorder may have led to a concomitant reduction in physical activity (Weuve et al., 2004). Thus, longitudinal intervention studies are better suited to determine the link between physical exercise and cognition. These studies show that several months of regular physical exercise led to improved mental functions or a slower cognitive decline in elderly subjects (Colcombe & Kramer, 2003 for a meta-analysis), with varying effect sizes for different cognitive functions (Fig. 1).

Several studies probed the effect of acute bouts of exercise on cognitive functions (Etnier et al., 1997, Tomporowski, 2003, Tomporowski and Ellis, 1986 for a review). Most of these studies, however, did not directly assess effects on learning or memory, but rather investigated the effect of exercise on various neuropsychological measures, like simple reaction time tasks (e.g., Hogervorst, Riedel, Jeukendrup, & Jolles, 1996), or on exercise-related tasks like decision making in soccer (e.g., McMorris & Graydon, 1997). Studies probing the effect of exercise on memory led to divergent results, depending on the length and intensity of the exercise intervention. After short-duration anaerobic exercise (up to 2 min), short-term memory was facilitated (Davey, 1973). During or immediately after long anaerobic exercise (5–40 min), no effects on memory were found (Sjoberg, 1980, Tomporowski et al., 1987). When the exercise condition led to dehydration, either no effects or even negative effects on memory were noted (Cian et al., 2001, Cian et al., 2000).

Similar results were obtained for healthy children: Sibley and Etnier reported positive effects of regular physical exercise for various cognitive tasks, but not for “pure” memory performance in their recent meta-analysis (Sibley & Etnier, 2003). Findings in children with attention deficit disorder are less conclusive: positive effects of exercise on disturbing behaviors have been found (Allison et al., 1995, Tantillo et al., 2002), but effects on cognition have not been reported so far (Craft, 1983).

In contrast to the preliminary evidence regarding the relation of physical exercise and cognition in humans, animals consistently showed improved learning after daily physical exercise for up to 7 months (Anderson et al., 2000, Baruch et al., 2004, Fordyce and Farrar, 1991, van Praag et al., 1999). Negative reports can be explained by an interaction of task complexity and heterogeneous task performance of the animals (Braszko, Kaminski, Hryszko, Jedynak, & Brzosko, 2001) or may be due to the use of a non-voluntary exercise condition (forced treadmill running; Burghardt, Fulk, Hand, & Wilson, 2004).

In animal studies, upregulations of various neurotransmitters in the brain, especially dopamine and norepinephrine, were found (Hattori et al., 1994, Meeusen and De Meirleir, 1995, Sutoo and Akiyama, 2003). In addition to catecholamines, the release of neurotrophic factors, like brain-derived neurotrophic factor (BDNF), nerve growth factor (NGF), or insulin-like growth factor (IGF-1), is increased in the brain after a regimen of daily physical exercise in animals (Carro et al., 2000, Gobbo and O’Mara, 2005, Neeper et al., 1995, Neeper et al., 1996). The amount of neurotrophic factor release correlated with faster learning and better retention over a period of 1 week (Vaynman, Ying, & Gomez-Pinilla, 2004). Exercise also enhances neurogenesis (van Praag et al., 1999, van Praag et al., 1999), which could also contribute to better learning.

In humans, the association between learning improvement and exercise-induced humoral changes has not yet been investigated. It has only been shown that the P300 component of the event-related brain potential (ERP) has a larger amplitude and a shortened latency in attentional challenging tasks, consistent with an overall arousing effect, after a short bout of anaerobic exercise compared to rest (Hillman et al., 2003, Magnie et al., 2000, Nakamura et al., 1999). Furthermore, peripheral catecholamine levels may increase after physical exercise (Hyyppa et al., 1986, Koch et al., 1980, Kraemer et al., 1999, Musso et al., 1990), but several other studies found no changes (Bracken et al., 2005, Hartling et al., 1989, Sothmann et al., 1987). The only study probing central dopamine level changes after a single bout of exercise by positron emission tomography yielded negative results (Wang et al., 2000).

Outside the realm of exercise research, increased peripheral epinephrine levels were correlated with enhanced memory performance in both animals (Costa-Miserachs, Portell-Cortes, Aldavert-Vera, Torras-Garcia, & Morgado-Bernal, 1994) and humans (Cahill & Alkire, 2003). Together, these findings suggest that an exercise-induced increase of catecholamines and neurotrophic factors might improve learning.

We here examined the effects of single bouts of controlled intense anaerobic or moderate aerobic physical exercises (lactate levels above 10 mmol/l or below 2 mmol/l, respectively; Spurway, 1992) on learning and memory. We chose a language learning model because lexical learning is an important aspect of every day life. In search of the mediating mechanisms, we additionally assessed exercise-induced changes in mood, peripheral catecholamine plasma levels and BDNF serum levels and correlated these parameters with subjects’ cognitive performance.

Section snippets

Subjects

A total of 30 healthy male sport students (mean age: 22.2 ± 1.7 years; range: 19–27) participated as subjects in this prospective randomized controlled trial. Two subjects failed to complete the study due to exercise injuries unrelated to the study. Another subject failed to learn, presumably due to inattentive responding (reactions times on average <300 ms). Therefore, data analysis was conducted with a total of 27 subjects

Learning performance

Using a cross-over study design, learning performance was assessed directly after high impact anaerobic sprints (intense condition), low impact aerobic running (moderate condition), or a period of rest (relaxed condition).

Discussion

The main finding of the present study was that intense exercise directly improves learning: After two sprints of less than 3 min each, subjects learned 20 percent faster compared to moderate exercise or being sedentary. To our knowledge, this is the first study of immediate exercise-induced effects on a complex learning task with a parallel analysis of neurophysiological correlates (changes in peripheral catecholamine or BDNF levels) in humans. Our results suggests that short bouts of exercise

Acknowledgments

This work was supported by the Cusanuswerk, the NRW-Nachwuchsgruppe Kn2000 of the Nordrhein-Westfalen Ministry of Education and Research (Foe.1KS9604/0), the Interdisciplinary Center of Clinical Research Muenster (IZKF Projects FG2 and Kne3/074/04), the Volkswagen Stiftung (Az.: I/80 708), as well as the German Ministry of Education and Research (BMBF: 01GW0520).

References (91)

  • D.M. Feeney et al.

    Reinstatement of binocular depth perception by amphetamine and visual experience after visual cortex ablation

    Brain Research

    (1985)
  • D.E. Fordyce et al.

    Enhancement of spatial learning in F344 rats by physical activity and related learning-associated alterations in hippocampal and cortical cholinergic functioning

    Behavioural Brain Research

    (1991)
  • O.L. Gobbo et al.

    Exercise, but not environmental enrichment, improves learning after kainic acid-induced hippocampal neurodegeneration in association with an increase in brain-derived neurotrophic factor

    Behavioural Brain Research

    (2005)
  • S.M. Gold 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

    Journal of Neuroimmunology

    (2003)
  • S. Hattori et al.

    Striatal dopamine turnover during treadmill running in the rat: relation to the speed of running

    Brain Research Bulletin

    (1994)
  • C.H. Hillman et al.

    Acute cardiovascular exercise and executive control function

    International Journal of Psychophysiology

    (2003)
  • W. Hollmann et al.

    Brain function, mind, mood, nutrition, and physical exercise

    Nutrition

    (2000)
  • T.M. Jay

    Dopamine: a potential substrate for synaptic plasticity and memory mechanisms

    Progress in Neurobiology

    (2003)
  • T. Miyashita et al.

    Peripheral arousal-related hormones modulate norepinephrine release in the hippocampus via influences on brainstem nuclei

    Behavioural Brain Research

    (2004)
  • T. Miyashita et al.

    Epinephrine administration increases neural impulses propagated along the vagus nerve: role of peripheral beta-adrenergic receptors

    Neurobiology of Learning and Memory

    (2006)
  • N.R. Musso et al.

    Plasma dopamine response to sympathetic activation in man: a biphasic pattern

    Life Science

    (1990)
  • S.A. Neeper et al.

    Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain

    Brain Research

    (1996)
  • R.C. Oldfield

    The assessment and analysis of handedness: the Edinburgh inventory

    Neuropsychologia

    (1971)
  • W. Pan et al.

    Transport of brain-derived neurotrophic factor across the blood–brain barrier

    Neuropharmacology

    (1998)
  • A.F. Schinder et al.

    The neurotrophin hypothesis for synaptic plasticity

    Trends in Neuroscience

    (2000)
  • W. Schultz

    Getting formal with dopamine and reward

    Neuron

    (2002)
  • D. Sutoo et al.

    Regulation of brain function by exercise

    Neurobiology of Disease

    (2003)
  • P.D. Tomporowski

    Effects of acute bouts of exercise on cognition

    Acta Psychologica

    (2003)
  • D. Wu

    Neuroprotection in experimental stroke with targeted neurotrophins

    NeuroRx

    (2005)
  • R.D. Abbott et al.

    Walking and dementia in physically capable elderly men

    JAMA: The Journal of the American Medical Association

    (2004)
  • D.B. Allison et al.

    Antecedent exercise in the treatment of disruptive behavior: a meta-analytic review

    Clinical Psychology: Science & Practice

    (1995)
  • S.A. Baker et al.

    Dopaminergic nigrostriatal projections regulate neural precursor proliferation in the adult mouse subventricular zone

    European Journal of Neuroscience

    (2004)
  • D.E. Baruch et al.

    Effects of exercise on Pavlovian fear conditioning

    Behavioral Neuroscience

    (2004)
  • R.M. Bracken et al.

    Alkalosis and the plasma catecholamine response to high-intensity exercise in man

    Medicine and Science in Sports and Exercise

    (2005)
  • M.W. Bradbury

    The blood–brain barrier

    Experimental Physiology

    (1993)
  • C. Breitenstein et al.

    Tonic dopaminergic stimulation impairs associative learning in healthy subjects

    Neuropsychopharmacology

    (2006)
  • C. Breitenstein et al.

    Word learning can be achieved without feedback: implications for aphasia therapy

    Restorative Neurology and Neuroscience

    (2004)
  • E. Carro et al.

    Circulating insulin-like growth factor I mediates effects of exercise on the brain

    Journal of Neuroscience

    (2000)
  • S.A. Castner et al.

    Enhancement of working memory in aged monkeys by a sensitizing regimen of dopamine D1 receptor stimulation

    Journal of Neuroscience

    (2004)
  • C. Cian et al.

    Influences of variations in body hydration on cognitive function: effect of hyperhydration, heat stress, and exercise-induced dehydration

    Journal of Psychophysiology

    (2000)
  • S. Colcombe et al.

    Fitness effects on the cognitive function of older adults: a meta-analytic study

    Psychological Science

    (2003)
  • S.J. Colcombe et al.

    Cardiovascular fitness, cortical plasticity, and aging

    Proceedings of the National Academy of Sciences of the United States of America

    (2004)
  • D. Costa-Miserachs et al.

    Long-term memory facilitation in rats by posttraining epinephrine

    Behavioral Neuroscience

    (1994)
  • D.H. Craft

    Effect of prior exercise on cognitive performance tasks by hyperactive and normal young boys

    Perceptual and Motor Skills

    (1983)
  • C.P. Davey

    Physical exertion and mental performance

    Ergonomics

    (1973)
  • Cited by (581)

    View all citing articles on Scopus
    1

    These authors contributed equally.

    View full text