Multiple Bouts of High-intensity Interval Exercise Reverse Age-related Functional Connectivity Disruptions Without Affecting Motor Learning in Older Adults

Overview

Journal Sci Rep

Specialty Science

Date 2021 Aug 25

PMID 34429472

Citations 8

Authors

Brian Greeley

Briana Chau

Christina B Jones

Jason L Neva

Sarah N Kraeutner

Kristin L Campbell

Lara A Boyd

Affiliations

Soon will be listed here.

Abstract

Exercise has emerged as an intervention that may mitigate age-related resting state functional connectivity and sensorimotor decline. Here, 42 healthy older adults rested or completed 3 sets of high-intensity interval exercise for a total of 23 min, then immediately practiced an implicit motor task with their non-dominant hand across five separate sessions. Participants completed resting state functional MRI before the first and after the fifth day of practice; they also returned 24-h and 35-days later to assess short- and long-term retention. Independent component analysis of resting state functional MRI revealed increased connectivity in the frontoparietal, the dorsal attentional, and cerebellar networks in the exercise group relative to the rest group. Seed-based analysis showed strengthened connectivity between the limbic system and right cerebellum, and between the right cerebellum and bilateral middle temporal gyri in the exercise group. There was no motor learning advantage for the exercise group. Our data suggest that exercise paired with an implicit motor learning task in older adults can augment resting state functional connectivity without enhancing behaviour beyond that stimulated by skilled motor practice.

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References

Mang C, Snow N, Wadden K, Campbell K, Boyd L . High-Intensity Aerobic Exercise Enhances Motor Memory Retrieval. Med Sci Sports Exerc. 2016; 48(12):2477-2486. DOI: 10.1249/MSS.0000000000001040. View

Wang Y, Li T . Dimensionality of ICA in resting-state fMRI investigated by feature optimized classification of independent components with SVM. Front Hum Neurosci. 2015; 9:259. PMC: 4424860. DOI: 10.3389/fnhum.2015.00259. View

Wang L, LaViolette P, OKeefe K, Putcha D, Bakkour A, Van Dijk K . Intrinsic connectivity between the hippocampus and posteromedial cortex predicts memory performance in cognitively intact older individuals. Neuroimage. 2010; 51(2):910-7. PMC: 2856812. DOI: 10.1016/j.neuroimage.2010.02.046. View

Birn R, Molloy E, Patriat R, Parker T, Meier T, Kirk G . The effect of scan length on the reliability of resting-state fMRI connectivity estimates. Neuroimage. 2013; 83:550-8. PMC: 4104183. DOI: 10.1016/j.neuroimage.2013.05.099. View

Vidoni E, Boyd L . Achieving enlightenment: what do we know about the implicit learning system and its interaction with explicit knowledge?. J Neurol Phys Ther. 2007; 31(3):145-54. DOI: 10.1097/NPT.0b013e31814b148e. View

Dayan E, Cohen L . Neuroplasticity subserving motor skill learning. Neuron. 2011; 72(3):443-54. PMC: 3217208. DOI: 10.1016/j.neuron.2011.10.008. View

Doyon J, Benali H . Reorganization and plasticity in the adult brain during learning of motor skills. Curr Opin Neurobiol. 2005; 15(2):161-7. DOI: 10.1016/j.conb.2005.03.004. View

Debas K, Carrier J, Orban P, Barakat M, Lungu O, Vandewalle G . Brain plasticity related to the consolidation of motor sequence learning and motor adaptation. Proc Natl Acad Sci U S A. 2010; 107(41):17839-44. PMC: 2955095. DOI: 10.1073/pnas.1013176107. View

Botvinik-Nezer R, Holzmeister F, Camerer C, Dreber A, Huber J, Johannesson M . Variability in the analysis of a single neuroimaging dataset by many teams. Nature. 2020; 582(7810):84-88. PMC: 7771346. DOI: 10.1038/s41586-020-2314-9. View

10.

Ahlfeld J, Filser S, Schmidt F, Wefers A, Merk D, Glass R . Neurogenesis from Sox2 expressing cells in the adult cerebellar cortex. Sci Rep. 2017; 7(1):6137. PMC: 5522437. DOI: 10.1038/s41598-017-06150-x. View

11.

Herszage J, Dayan E, Sharon H, Censor N . Explaining Individual Differences in Motor Behavior by Intrinsic Functional Connectivity and Corticospinal Excitability. Front Neurosci. 2020; 14:76. PMC: 7025558. DOI: 10.3389/fnins.2020.00076. View

12.

Lin T, Shih Y, Chen S, Lien C, Chang C, Huang T . Running exercise delays neurodegeneration in amygdala and hippocampus of Alzheimer's disease (APP/PS1) transgenic mice. Neurobiol Learn Mem. 2014; 118:189-97. DOI: 10.1016/j.nlm.2014.12.005. View

13.

Damoiseaux J, Beckmann C, Arigita E, Barkhof F, Scheltens P, Stam C . Reduced resting-state brain activity in the "default network" in normal aging. Cereb Cortex. 2007; 18(8):1856-64. DOI: 10.1093/cercor/bhm207. View

14.

Weng T, Pierce G, Darling W, Falk D, Magnotta V, Voss M . The Acute Effects of Aerobic Exercise on the Functional Connectivity of Human Brain Networks. Brain Plast. 2018; 2(2):171-190. PMC: 5928541. DOI: 10.3233/BPL-160039. View

15.

Meehan S, Randhawa B, Wessel B, Boyd L . Implicit sequence-specific motor learning after subcortical stroke is associated with increased prefrontal brain activations: an fMRI study. Hum Brain Mapp. 2010; 32(2):290-303. PMC: 3010500. DOI: 10.1002/hbm.21019. View

16.

Neva J, Ma J, Orsholits D, Boisgontier M, Boyd L . The effects of acute exercise on visuomotor adaptation, learning, and inter-limb transfer. Exp Brain Res. 2019; 237(4):1109-1127. DOI: 10.1007/s00221-019-05491-5. View

17.

Mang C, Snow N, Campbell K, Ross C, Boyd L . A single bout of high-intensity aerobic exercise facilitates response to paired associative stimulation and promotes sequence-specific implicit motor learning. J Appl Physiol (1985). 2014; 117(11):1325-36. PMC: 4254838. DOI: 10.1152/japplphysiol.00498.2014. View

18.

Newbold D, Laumann T, Hoyt C, Hampton J, Montez D, Raut R . Plasticity and Spontaneous Activity Pulses in Disused Human Brain Circuits. Neuron. 2020; 107(3):580-589.e6. PMC: 7419711. DOI: 10.1016/j.neuron.2020.05.007. View

19.

Behzadi Y, Restom K, Liau J, Liu T . A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. Neuroimage. 2007; 37(1):90-101. PMC: 2214855. DOI: 10.1016/j.neuroimage.2007.04.042. View

20.

Ahlskog J, Geda Y, Graff-Radford N, Petersen R . Physical exercise as a preventive or disease-modifying treatment of dementia and brain aging. Mayo Clin Proc. 2011; 86(9):876-84. PMC: 3258000. DOI: 10.4065/mcp.2011.0252. View