High-intensity acute exercise impacts motor learning in healthy older adults

Taylor, Eleanor M.; Cadwallader, Claire J.; Curtin, Dylan; Chong, Trevor T.-J.; Hendrikse, Joshua J.; Coxon, James P.

doi:10.1038/s41539-024-00220-2

Cited by 3 publications

References 95 publications

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Default mode and motor networks facilitate early learning of implicit motor sequences: a multimodal MR spectroscopy and fMRI study

Hendrikse,

Brooks,

Wallis

et al. 2024

Preprint

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Learning new motor skills is a fundamental process that involves the sequencing of actions. Skill develops with practice and time, and manifests as performance that is fast and accurate. Although we know that learning can occur through animplicitprocess in the absence of conscious awareness, and across multiple temporal scales, the precise neural mechanisms mediating implicit motor sequence learning remain poorly understood. Similarly, the capacity for interventions with known influence on learning and memory, such as cardiovascular exercise, to facilitate implicit learning is yet to be clearly established. Here, we investigated the neuroplasticity of implicit motor sequence learning and the effect of acute exercise priming. Healthy adults (39.5% female) aged 22.55 ± 2.69 years were allocated to either a high-intensity exercise (HIIT) group (n = 16) or to a very low-intensity control group (n = 17). Following exercise, participants performed a serial reaction time task. MR spectroscopy estimates of sensorimotor gamma-aminobutyric acid (GABA) were acquired before and after exercise, and during task performance, and resting-state fMRI was acquired at the end of the protocol. We show that early stages of learning are linked to default mode network connectivity, while the overall degree of learning following sustained practice is associated with motor network connectivity. Sensorimotor GABA concentration was linked to the early stages of learning, and GABA concentration was modulated following HIIT, although the two were not related. Overall, via integration of multiple neuroimaging modalities we demonstrate that interactions between hippocampal and motor networks underlieimplicitmotor sequence learning.Key points summary-Motor learning occurs across different temporal scales and can arise implicitly in the absence of conscious awareness.-Explicitmotor learning is linked to the brain’s primary inhibitory neurotransmitter, GABA, and interactions across motor and hippocampal networks.-Whether these same neural mechanisms are implicated inimplicitlearning is unclear. Similarly, the capacity to influence learning via priming with cardiovascular exercise is yet to be clearly established.-We show that early implicit learning is underpinned by default mode network connectivity and sensorimotor GABA concentration, while total learning following sustained practice is linked to motor network connectivity. We also found that HIIT exercise elevated sensorimotor GABA concentration, but not the magnitude of implicit learning.-Overall, our results highlight shared involvement of default mode and motor networks in implicit motor sequence learning.

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Default mode and motor networks facilitate early learning of implicit motor sequences: a multimodal MR spectroscopy and fMRI study

Hendrikse,

Brooks,

Wallis

et al. 2024

Preprint

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Association Between Physical Activity and Performance in Skill Learning Among Older Adults Based on Cognitive Function

Kasahara,

Chiba,

Jiang

et al. 2024

Journal of Aging and Physical Activity

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Background/Objectives: Most older adults experience cognitive and physical functioning problems; however, they require the ability to learn skills in response to age-related or social environmental changes for independent living. This study aimed to clarify the associations between age-related physical activity and performance in skill learning tasks based on cognitive function. Methods: Fifty-eight adults participated in this study and were divided into two groups: the control group (aged under 65 years) and older adult group (aged over 65). All the participants performed two-skill learning exercises based on cognitive function. Habitual exercise was measured using an accelerometer and a self-reported questionnaire. Results: At baseline, the scores on skill tasks were lower in the older adult group than in the control group and were associated with habitual exercise and motor performance. Skill acquisition, observed in both groups, was associated with age and self-reported physical activity. Retention of the acquired skill was not associated with habitual exercise, and it declined significantly in the older group. Conclusions: Skill acquisition was maintained regardless of age; however, the ability to retain the acquired skills decreased among the older adults. Habitual physical activity was associated with skill acquisition but not the retention of the acquired skill. Significance/Implications: The study findings highlight the association between habitual exercise and motor skill learning in older adults, providing insight for practitioners in the rehabilitation and health care fields.

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Dopamine D2 Receptor Modulates Exercise Related Effect on Cortical Excitation/Inhibition and Motor Skill Acquisition

Curtin,

Taylor,

Bellgrove

et al. 2024

J. Neurosci.

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Exercise is known to benefit motor skill learning in health and neurological disease. Evidence from brain stimulation, genotyping, and Parkinson's disease studies converge to suggest that the dopamine D2 receptor, and shifts in the cortical excitation and inhibition (E:I) balance, are prime candidates for the drivers of exercise-enhanced motor learning. However, causal evidence using experimental pharmacological challenge is lacking. We hypothesised that the modulatory effect of the dopamine D2 receptor on exercise-induced changes in the E:I balance would determine the magnitude of motor skill acquisition. To test this, we measured exercise-induced changes in excitation and inhibition using paired-pulse transcranial magnetic stimulation (TMS) in 22 healthy female and male humans, and then had participants learn a novel motor skill — the sequential visual isometric pinch task (SVIPT). We examined the effect of D2 receptor blockade (800 mg sulpiride) on these measures within a randomised, double-blind, placebo-controlled design. Our key result was that motor skill acquisition was driven by an interaction between the D2 receptor and E:I balance. Specifically, poorer skill learning was related to an attenuated shift in the E:I balance in the sulpiride condition, whereas this interaction was not evident in placebo. Our results demonstrate that exercise-primed motor skill acquisition is causally influenced by D2 receptor activity on motor cortical circuits.Significance statementExercise is known to benefit the ability to acquire new motor skills, but the neural mechanisms driving this phenomenon are not well understood. We tested whether the effects of exercise on cortical neurophysiology and motor skill learning was due to dopaminergic neuromodulation. We obtained measures of cortical excitation and inhibition before and after high-intensity cardiorespiratory exercise, and then had participants learn a novel motor skill. We provide causal evidence that motor skill acquisition is driven by an interaction between the dopamine D2 receptor and exercise-induced shifts in the cortical excitation:inhibition balance. Such findings have implications for prescribing exercise to improve motor learning in disorders of dopamine dysfunction, such as Parkinson's disease.

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High-intensity acute exercise impacts motor learning in healthy older adults

Cited by 3 publications

References 95 publications

Default mode and motor networks facilitate early learning of implicit motor sequences: a multimodal MR spectroscopy and fMRI study

Default mode and motor networks facilitate early learning of implicit motor sequences: a multimodal MR spectroscopy and fMRI study

Association Between Physical Activity and Performance in Skill Learning Among Older Adults Based on Cognitive Function

Dopamine D2 Receptor Modulates Exercise Related Effect on Cortical Excitation/Inhibition and Motor Skill Acquisition

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