Joshua Hendrikse, Emily Brooks, Sarah Wallis, Dylan Curtin, Nigel C Rogasch, Murat Yücel, Mana Biabani, Charlotte J Stagg, Mark Bellgrove, Richard McIntyre, Chao Suo, James Coxon
{"title":"Default mode and motor networks facilitate early learning of implicit motor sequences: a multimodal MR spectroscopy and fMRI study.","authors":"Joshua Hendrikse, Emily Brooks, Sarah Wallis, Dylan Curtin, Nigel C Rogasch, Murat Yücel, Mana Biabani, Charlotte J Stagg, Mark Bellgrove, Richard McIntyre, Chao Suo, James Coxon","doi":"10.1113/JP288361","DOIUrl":null,"url":null,"abstract":"<p><p>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 an implicit process 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 interval training (HIIT) exercise group (n = 16) or to a very low-intensity control group (n = 17). After exercise participants performed a serial reaction time task, magnetic resonance (MR) spectroscopy estimates of sensorimotor GABA were acquired before and after exercise and during task performance, and resting-state functional magnetic resonance imaging (fMRI) was acquired at the end of the protocol. We show that early stages of learning are linked to default mode network connectivity, whereas 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 through the integration of multiple neuroimaging modalities we demonstrate that interactions between hippocampal and motor networks underlie implicit motor sequence learning. KEY POINTS: Motor learning occurs across different temporal scales and can arise implicitly in the absence of conscious awareness. Explicit motor 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 in implicit learning is unclear. Similarly the capacity to influence implicit 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, whereas total learning following sustained practice is linked to motor network connectivity. We also found that high-intensity interval training (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.</p>","PeriodicalId":50088,"journal":{"name":"Journal of Physiology-London","volume":" ","pages":""},"PeriodicalIF":4.4000,"publicationDate":"2025-09-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Physiology-London","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1113/JP288361","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"NEUROSCIENCES","Score":null,"Total":0}
引用次数: 0
Abstract
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 an implicit process 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 interval training (HIIT) exercise group (n = 16) or to a very low-intensity control group (n = 17). After exercise participants performed a serial reaction time task, magnetic resonance (MR) spectroscopy estimates of sensorimotor GABA were acquired before and after exercise and during task performance, and resting-state functional magnetic resonance imaging (fMRI) was acquired at the end of the protocol. We show that early stages of learning are linked to default mode network connectivity, whereas 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 through the integration of multiple neuroimaging modalities we demonstrate that interactions between hippocampal and motor networks underlie implicit motor sequence learning. KEY POINTS: Motor learning occurs across different temporal scales and can arise implicitly in the absence of conscious awareness. Explicit motor 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 in implicit learning is unclear. Similarly the capacity to influence implicit 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, whereas total learning following sustained practice is linked to motor network connectivity. We also found that high-intensity interval training (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.
期刊介绍:
The Journal of Physiology publishes full-length original Research Papers and Techniques for Physiology, which are short papers aimed at disseminating new techniques for physiological research. Articles solicited by the Editorial Board include Perspectives, Symposium Reports and Topical Reviews, which highlight areas of special physiological interest. CrossTalk articles are short editorial-style invited articles framing a debate between experts in the field on controversial topics. Letters to the Editor and Journal Club articles are also published. All categories of papers are subjected to peer reivew.
The Journal of Physiology welcomes submitted research papers in all areas of physiology. Authors should present original work that illustrates new physiological principles or mechanisms. Papers on work at the molecular level, at the level of the cell membrane, single cells, tissues or organs and on systems physiology are all acceptable. Theoretical papers and papers that use computational models to further our understanding of physiological processes will be considered if based on experimentally derived data and if the hypothesis advanced is directly amenable to experimental testing. While emphasis is on human and mammalian physiology, work on lower vertebrate or invertebrate preparations may be suitable if it furthers the understanding of the functioning of other organisms including mammals.