The association between aerobic fitness and cognitive function in older men mediated by frontal lateralization

Previous studies have shown that higher aerobic fitness is related to higher cognitive function and higher task-related prefrontal activation in older adults. However, a holistic picture of these factors has yet to be presented. As a typical age-related change of brain activation, less lateralized activity in the prefrontal cortex during cognitive tasks has been observed in various neuroimaging studies. Thus, this study aimed to reveal the relationship between aerobic fitness, cognitive function, and frontal lateralization. Sixty male older adults each performed a submaximal incremental exercise test to determine their oxygen intake (V·O2) at ventilatory threshold (VT) in order to index their aerobic fitness. They performed a color-word Stroop task while prefrontal activation was monitored using functional near infrared spectroscopy. As an index of cognitive function, Stroop interference time was analyzed. Partial correlation analyses revealed significant correlations among higher VT, shorter Stroop interference time and greater left-lateralized dorsolateral prefrontal cortex (DLPFC) activation when adjusting for education. Moreover, mediation analyses showed that left-lateralized DLPFC activation significantly mediated the association between VT and Stroop interference time. These results suggest that higher aerobic fitness is associated with cognitive function via lateralized frontal activation in older adults.

[1]  Masako Okamoto,et al.  Three-dimensional probabilistic anatomical cranio-cerebral correlation via the international 10–20 system oriented for transcranial functional brain mapping , 2004, NeuroImage.

[2]  Paige E. Scalf,et al.  Cardiovascular fitness, cortical plasticity, and aging. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[3]  W L Beaver,et al.  Anaerobic threshold and respiratory gas exchange during exercise. , 1973, Journal of applied physiology.

[4]  Joep C. Teeken,et al.  Aerobic capacity and cognitive performance in a cross-sectional aging study. , 1997, Medicine and science in sports and exercise.

[5]  S. Green.  How Many Subjects Does It Take To Do A Regression Analysis. , 1991, Multivariate behavioral research.

[6]  R. Cabeza.  Hemispheric asymmetry reduction in older adults: the HAROLD model. , 2002, Psychology and aging.

[7]  Kathryn M. McMillan,et al.  A comparison of label‐based review and ALE meta‐analysis in the Stroop task , 2005, Human brain mapping.

[8]  D. Boas,et al.  Non-invasive neuroimaging using near-infrared light , 2002, Biological Psychiatry.

[9]  J. Ridley.  Studies of Interference in Serial Verbal Reactions , 2001 .

[10]  B. Whipp,et al.  A new method for detecting anaerobic threshold by gas exchange. , 1986, Journal of applied physiology.

[11]  D. V. Cramon,et al.  Stroop interference, hemodynamic response and aging: An event-related fMRI study , 2007, Neurobiology of Aging.

[12]  G. Sorrentino,et al.  Biological Mechanisms of Physical Activity in Preventing Cognitive Decline , 2010, Cellular and Molecular Neurobiology.

[13]  A. Kramer,et al.  Be smart, exercise your heart: exercise effects on brain and cognition , 2008, Nature Reviews Neuroscience.

[14]  L. White,et al.  Role of Aerobic Fitness and Aging on Cerebral White Matter Integrity , 2007, Annals of the New York Academy of Sciences.

[15]  D. Roth,et al.  Association between aerobic fitness and visuospatial performance in healthy older adults. , 1992, Psychology and aging.

[16]  Ben Godde,et al.  Physical and motor fitness are both related to cognition in old age , 2010, The European journal of neuroscience.

[17]  Jurgen A. H. R. Claassen,et al.  Effects of Aging on Cerebral Oxygenation during Working-Memory Performance: A Functional Near-Infrared Spectroscopy Study , 2012, PloS one.

[18]  R. Casaburi,et al.  Metabolic acidosis during exercise in patients with chronic obstructive pulmonary disease. Use of the V-slope method for anaerobic threshold determination. , 1988, Chest.

[19]  Ben Godde,et al.  Human Neuroscience , 2009 .

[20]  D. Cunningham,et al.  Exercise training and "ventilation threshold" in elderly. , 1986, Journal of applied physiology.

[21]  M. Tamura,et al.  Interpretation of near-infrared spectroscopy signals: a study with a newly developed perfused rat brain model. , 2001, Journal of applied physiology.

[22]  J. Cohen,et al.  Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. , 2000, Science.

[23]  Scott A Langenecker,et al.  fMRI of healthy older adults during Stroop interference , 2004, NeuroImage.

[24]  Angel Nuñez,et al.  Neuronal Activity Drives Localized Blood-Brain-Barrier Transport of Serum Insulin-like Growth Factor-I into the CNS , 2010, Neuron.

[25]  E B Ryan,et al.  Cognitive mediation of adult age differences in language performance. , 1995, Psychology and aging.

[26]  Hellmuth Obrig,et al.  Separability and cross talk: optimizing dual wavelength combinations for near-infrared spectroscopy of the adult head , 2004, NeuroImage.

[27]  Cheryl L. Dahle,et al.  Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. , 2005, Cerebral cortex.

[28]  Masako Okamoto,et al.  Acute moderate exercise elicits increased dorsolateral prefrontal activation and improves cognitive performance with Stroop test , 2010, NeuroImage.

[29]  A. Iwanami,et al.  Effect of Parietal Transcranial Magnetic Stimulation on Spatial Working Memory in Healthy Elderly Persons - Comparison of Near Infrared Spectroscopy for Young and Elderly , 2014, PloS one.

[30]  Jacob Cohen,et al.  A power primer. , 1992, Psychological bulletin.

[31]  Colin M. Macleod.  Half a century of research on the Stroop effect: an integrative review. , 1991, Psychological bulletin.

[32]  N. Cohen,et al.  Attentional Control in the Aging Brain: Insights from an fMRI Study of the Stroop Task , 2002, Brain and Cognition.

[33]  Katja Hagen,et al.  Aging-related cortical reorganization of verbal fluency processing: a functional near-infrared spectroscopy study , 2013, Neurobiology of Aging.

[34]  E. McAuley,et al.  Aerobic fitness is associated with hippocampal volume in elderly humans , 2009, Hippocampus.

[35]  W. Kohrt,et al.  Effect of aging. , 2000, Nutrition reviews.

[36]  K. Sykes,et al.  Aerobic capacity. , 1992, Occupational health; a journal for occupational health nurses.

[37]  Edward E. Smith,et al.  Age Differences in the Frontal Lateralization of Verbal and Spatial Working Memory Revealed by PET , 2000, Journal of Cognitive Neuroscience.

[38]  J. Raaijmakers,et al.  Neuroanatomical correlates of episodic encoding and retrieval in young and elderly subjects. , 2003, Brain : a journal of neurology.

[39]  Arthur F. Kramer,et al.  Human Neuroscience , 2022 .

[40]  Jonas Persson,et al.  Structure-function correlates of cognitive decline in aging. , 2006, Cerebral cortex.

[41]  D. Delpy,et al.  Methods of quantitating cerebral near infrared spectroscopy data. , 1988, Advances in experimental medicine and biology.

[42]  E. Watanabe,et al.  Spatial and temporal analysis of human motor activity using noninvasive NIR topography. , 1995, Medical physics.

[43]  A. Maki,et al.  Optical topography: practical problems and new applications. , 2003, Applied optics.

[44]  T J Sejnowski,et al.  Running enhances neurogenesis, learning, and long-term potentiation in mice. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[45]  J. Dempsey,et al.  Effects of respiratory muscle work on cardiac output and its distribution during maximal exercise. , 1998, Journal of applied physiology.

[46]  D. A. Kenny,et al.  The moderator-mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. , 1986, Journal of personality and social psychology.

[47]  I. Johnsrude,et al.  The problem of functional localization in the human brain , 2002, Nature Reviews Neuroscience.

[48]  Arthur W. Toga,et al.  Construction of a 3D probabilistic atlas of human cortical structures , 2008, NeuroImage.

[49]  J. Logan,et al.  Under-Recruitment and Nonselective Recruitment Dissociable Neural Mechanisms Associated with Aging , 2002, Neuron.

[50]  Haruka Dan,et al.  Individual classification of ADHD children by right prefrontal hemodynamic responses during a go/no-go task as assessed by fNIRS , 2015, NeuroImage: Clinical.

[51]  Masato Fukuda,et al.  Reduced frontopolar activation during verbal fluency task in schizophrenia: A multi-channel near-infrared spectroscopy study , 2008, Schizophrenia Research.

[52]  Eiju Watanabe,et al.  Neuropharmacological effect of methylphenidate on attention network in children with attention deficit hyperactivity disorder during oddball paradigms as assessed using functional near-infrared spectroscopy , 2014, Neurophotonics.

[53]  A. Villringer,et al.  Beyond the Visible—Imaging the Human Brain with Light , 2003, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[54]  Roberto Cabeza,et al.  Aging Gracefully: Compensatory Brain Activity in High-Performing Older Adults , 2002, NeuroImage.

[55]  J. Stroop.  Studies of interference in serial verbal reactions. , 1992 .

[56]  B. Yankner,et al.  Neural mechanisms of ageing and cognitive decline , 2010, Nature.

[57]  Kae Itoh,et al.  Relationship between exercise intolerance and levels of neurohormonal factors and proinflammatory cytokines in patients with stable chronic heart failure. , 2005, International heart journal.

[58]  K. Nakagome,et al.  Association between social functioning and prefrontal hemodynamic responses in elderly adults , 2014, Behavioural Brain Research.

[59]  Eiju Watanabe,et al.  Neuropharmacological effect of atomoxetine on attention network in children with attention deficit hyperactivity disorder during oddball paradigms as assessed using functional near-infrared spectroscopy , 2014, Neurophotonics.

[60]  G. Borg.  Perceived exertion as an indicator of somatic stress. , 2019, Scandinavian journal of rehabilitation medicine.

[61]  Ippeita Dan,et al.  Positive effect of acute mild exercise on executive function via arousal-related prefrontal activations: An fNIRS study , 2014, NeuroImage.

[62]  J. Jonides,et al.  Interference resolution: Insights from a meta-analysis of neuroimaging tasks , 2007, Cognitive, affective & behavioral neuroscience.

[63]  Cathy J. Price,et al.  Explaining Left Lateralization for Words in the Ventral Occipitotemporal Cortex , 2011, The Journal of Neuroscience.

[64]  Archana K. Singh,et al.  Spatial registration of multichannel multi-subject fNIRS data to MNI space without MRI , 2005, NeuroImage.

[65]  E. McAuley,et al.  The association between aerobic fitness and executive function is mediated by prefrontal cortex volume , 2012, Brain, Behavior, and Immunity.

[66]  Masako Okamoto,et al.  Automated cortical projection of head-surface locations for transcranial functional brain mapping , 2005, NeuroImage.

[67]  M. Miyashita,et al.  Effects of daily activity recorded by pedometer on peak oxygen consumption ($$ \dot V{\rm{O}}_2 {\rm{peak}} $$), ventilatory threshold and leg extension power in 30- to 69-year-old Japanese without exercise habit , 2003, European Journal of Applied Physiology.

[68]  Haruka Dan,et al.  Right prefrontal activation as a neuro-functional biomarker for monitoring acute effects of methylphenidate in ADHD children: An fNIRS study☆ , 2012, NeuroImage: Clinical.

[69]  S. Holm.  A Simple Sequentially Rejective Multiple Test Procedure , 1979 .

[70]  Paige E. Scalf,et al.  The implications of cortical recruitment and brain morphology for individual differences in inhibitory function in aging humans. , 2005, Psychology and aging.

[71]  Arthur F. Kramer,et al.  Age-related differences in the involvement of the prefrontal cortex in attentional control , 2009, Brain and Cognition.

[72]  I. Tabata,et al.  Evaluation of ventilatory threshold and its relation to exercise habits among Japanese , 2010, Environmental health and preventive medicine.

[73]  Kristopher J Preacher,et al.  Asymptotic and resampling strategies for assessing and comparing indirect effects in multiple mediator models , 2008, Behavior research methods.

[74]  Hasan Ayaz,et al.  Optical brain monitoring for operator training and mental workload assessment , 2012, NeuroImage.

[75]  Hiroki Sato,et al.  Practicality of Wavelength Selection to Improve Signal-to-noise Ratio in Near-infrared Spectroscopy , 2003 .

[76]  Reiko Kawagoe,et al.  Influence of skin blood flow on near-infrared spectroscopy signals measured on the forehead during a verbal fluency task , 2011, NeuroImage.

[77]  Mitsuhiro Okada,et al.  Effects of aging on hemispheric asymmetry in inferior frontal cortex activity during belief–bias syllogistic reasoning: A near-infrared spectroscopy study , 2010, Behavioural Brain Research.

[78]  Chobok Kim,et al.  Cardiorespiratory fitness is positively correlated with cerebral white matter integrity in healthy seniors , 2012, NeuroImage.

[79]  Masako Okamoto,et al.  Virtual spatial registration of stand-alone fNIRS data to MNI space , 2007, NeuroImage.

[80]  I. Dan,et al.  Acute moderate exercise enhances compensatory brain activation in older adults , 2012, Neurobiology of Aging.

[81]  R. Luthringer,et al.  The effect of aging on the inhibitory function in middle‐aged subjects: a functional MRI study coupled with a color‐matched Stroop task , 2009, International journal of geriatric psychiatry.

[82]  Anthony R. McIntosh,et al.  Age-Related Differences in Neural Activity during Memory Encoding and Retrieval: A Positron Emission Tomography Study , 1997, The Journal of Neuroscience.

[83]  Heidrun Wabnitz,et al.  The physiological origin of task-evoked systemic artefacts in functional near infrared spectroscopy , 2012, NeuroImage.

[84]  E. Perret.  The left frontal lobe of man and the suppression of habitual responses in verbal categorical behaviour. , 1974, Neuropsychologia.

[85]  Mohamed L. Seghier,et al.  Laterality index in functional MRI: methodological issues☆ , 2008, Magnetic resonance imaging.

[86]  D. Stuss,et al.  Principles of frontal lobe function , 2002 .

[87]  Haruka Dan,et al.  Acute neuropharmacological effects of atomoxetine on inhibitory control in ADHD children: A fNIRS study , 2014, NeuroImage: Clinical.

[88]  Masako Okamoto,et al.  Mapping of optical pathlength of human adult head at multi-wavelengths in near infrared spectroscopy. , 2010, Advances in experimental medicine and biology.

[89]  B. McEwen,et al.  Mild exercise increases dihydrotestosterone in hippocampus providing evidence for androgenic mediation of neurogenesis , 2012, Proceedings of the National Academy of Sciences.

[90]  C. Prefaut,et al.  Effectiveness of individualized aerobic training at the ventilatory threshold in the elderly. , 1997, The journals of gerontology. Series A, Biological sciences and medical sciences.

[91]  S. Langenecker,et al.  Differences in the functional neuroanatomy of inhibitory control across the adult life span. , 2002, Psychology and aging.

[92]  G. Lohmann,et al.  Color-Word Matching Stroop Task: Separating Interference and Response Conflict , 2001, NeuroImage.