Neural correlates of transfer of learning in motor coordination tasks: role of inhibitory and excitatory neurometabolites.

Bimanual coordination GABA Glx Magnetic resonance spectroscopy Transfer of learning

Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
08 Feb 2024
Historique:
received: 04 12 2023
accepted: 06 02 2024
medline: 9 2 2024
pubmed: 9 2 2024
entrez: 8 2 2024
Statut: epublish

Résumé

We aimed to investigate transfer of learning, whereby previously acquired skills impact new task learning. While it has been debated whether such transfer may yield positive, negative, or no effects on performance, very little is known about the underlying neural mechanisms, especially concerning the role of inhibitory (GABA) and excitatory (Glu) (measured as Glu + glutamine (Glx)) neurometabolites, as measured by magnetic resonance spectroscopy (MRS). Participants practiced a bimanual coordination task across four days. The Experimental group trained a task variant with the right hand moving faster than the left (Task A) for three days and then switched to the opposite variant (Task B) on Day4. The control group trained Task B across four days. MRS data were collected before, during, and after task performance on Day4 in the somatosensory (S1) and visual (MT/V5) cortex. Results showed that both groups improved performance consistently across three days. On Day4, the Experimental group experienced performance decline due to negative task transfer while the control group continuously improved. GABA and Glx concentrations obtained during task performance showed no significant group-level changes. However, individual Glx levels during task performance correlated with better (less negative) transfer performance. These findings provide a first window into the neurochemical mechanisms underlying task transfer.

Identifiants

DOI: 10.1038/s41598-024-53901-8 PMID: 38331950
pubmed: 38331950
doi: 10.1038/s41598-024-53901-8
pii: 10.1038/s41598-024-53901-8
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

3251

Informations de copyright

© 2024. The Author(s).

Références

Schmidt, R. A. et al. Motor Control and Learning: A Behavioral Emphasis (Human Kinetics, 2018).
Steiner, G. Transfer of learning. Int. Encycl. Soc. Behav. Sci. 11, 15845–15851 (2001).
Yadav, G. & Mutha, P. K. Symmetric interlimb transfer of newly acquired skilled movements. J. Neurophysiol. 124(5), 1364–1376 (2020).
pubmed: 32902352 doi: 10.1152/jn.00777.2019
Denis, H. H. An approximate transfer surface. J. Motor Behav. 8(1), 1–9 (1976).
doi: 10.1080/00222895.1976.10735049
Snapp-Childs, W., Wilson, A. D. & Bingham, G. P. Transfer of learning between unimanual and bimanual rhythmic movement coordination: Transfer is a function of the task dynamic. Exp. Brain Res. 233, 2225–2238 (2015).
pubmed: 25929551 doi: 10.1007/s00221-015-4292-y
Kirsch, W. & Hoffmann, J. Asymmetrical intermanual transfer of learning in a sensorimotor task. Exp. Brain Res. 202, 927–934 (2010).
pubmed: 20157699 doi: 10.1007/s00221-010-2184-8
Chase, C. & Seidler, R. Degree of handedness affects intermanual transfer of skill learning. Exp. Brain Res. 190, 317–328 (2008).
pubmed: 18592225 pmcid: 2570758 doi: 10.1007/s00221-008-1472-z
Van Mier, H. I. & Petersen, S. E. Intermanual transfer effects in sequential tactuomotor learning: Evidence for effector independent coding. Neuropsychologia 44(6), 939–949 (2006).
pubmed: 16198379 doi: 10.1016/j.neuropsychologia.2005.08.010
Vangheluwe, S. et al. Learning and transfer of bimanual multifrequency patterns: Effector-independent and effector-specific levels of movement representation. Exp. Brain Res. 170(4), 543–554 (2006).
pubmed: 16307261 doi: 10.1007/s00221-005-0238-0
Wigmore, V., Tong, C. & Flanagan, J. R. Visuomotor rotations of varying size and direction compete for a single internal model in a motor working memory. J. Exp. Psychol. Hum. Percept. Perform. 28(2), 447 (2002).
pubmed: 11999865 doi: 10.1037/0096-1523.28.2.447
Thut, G. et al. Intermanual transfer of proximal and distal motor engrams in humans. Exp. Brain Res. 108, 321–327 (1996).
pubmed: 8815040 doi: 10.1007/BF00228105
Perez, M. A. et al. Neural substrates of intermanual transfer of a newly acquired motor skill. Curr. Biol. 17(21), 1896–1902 (2007).
pubmed: 17964167 doi: 10.1016/j.cub.2007.09.058
Dirren, E. et al. The neural correlates of intermanual transfer. NeuroImage 245, 118657 (2021).
pubmed: 34687859 doi: 10.1016/j.neuroimage.2021.118657
Gabitov, E., Manor, D. & Karni, A. Learning from the other limb’s experience: Sharing the ‘trained’M1 representation of the motor sequence knowledge. J. Physiol. 594(1), 169–188 (2016).
pubmed: 26442464 doi: 10.1113/JP270184
Wiestler, T., Waters-Metenier, S. & Diedrichsen, J. Effector-independent motor sequence representations exist in extrinsic and intrinsic reference frames. J. Neurosci. 34(14), 5054–5064 (2014).
pubmed: 24695723 pmcid: 3972728 doi: 10.1523/JNEUROSCI.5363-13.2014
Andrushko, J. W. et al. Repeated unilateral handgrip contractions alter functional connectivity and improve contralateral limb response times. Sci. Rep. 13(1), 6437 (2023).
pubmed: 37081073 pmcid: 10119116 doi: 10.1038/s41598-023-33106-1
Bell, T. K. et al. Functional changes in GABA and glutamate during motor learning. Eneuro 10(2), 0356 (2023).
doi: 10.1523/ENEURO.0356-20.2023
King, B. R. et al. Baseline sensorimotor GABA levels shape neuroplastic processes induced by motor learning in older adults. Hum. Brain Map. 41(13), 3680–3695 (2020).
doi: 10.1002/hbm.25041
Kolasinski, J. et al. The dynamics of cortical GABA in human motor learning. J. Physiol. 597(1), 271–282 (2019).
pubmed: 30300446 doi: 10.1113/JP276626
Chalavi, S. et al. The neurochemical basis of the contextual interference effect. Neurobiol. Aging 66, 85–96 (2018).
pubmed: 29549874 doi: 10.1016/j.neurobiolaging.2018.02.014
Floyer-Lea, A. et al. Rapid modulation of GABA concentration in human sensorimotor cortex during motor learning. J. Neurophysiol. 95(3), 1639–1644 (2006).
pubmed: 16221751 doi: 10.1152/jn.00346.2005
Maes, C. et al. Task-related modulation of sensorimotor GABA+ levels in association with brain activity and motor performance: A multimodal MRS–fMRI study in young and older adults. J. Neurosci. 42(6), 1119–1130 (2022).
pubmed: 34876470 pmcid: 8824510 doi: 10.1523/JNEUROSCI.1154-21.2021
Li, H. et al. The role of MRS-assessed GABA in human behavioral performance. Progr. Neurobiol. 212, 102247 (2022).
doi: 10.1016/j.pneurobio.2022.102247
Pasanta, D. et al. Functional MRS studies of GABA and glutamate/Glx: A systematic review and meta-analysis. Neurosci. Biobehav. Rev. 144, 104940 (2022).
pubmed: 36332780 pmcid: 9846867 doi: 10.1016/j.neubiorev.2022.104940
Purves, D. et al. Neuroscience 15–16 (De Boeck, Sinauer, 2014).
Heuninckx, S., Wenderoth, N. & Swinnen, S. P. Age-related reduction in the differential pathways involved in internal and external movement generation. Neurobiol. Aging 31(2), 301–314 (2010).
pubmed: 18472185 doi: 10.1016/j.neurobiolaging.2008.03.021
Sunaert, S. et al. Motion-responsive regions of the human brain. Exp. Brain Res. 127, 355–370 (1999).
pubmed: 10480271 doi: 10.1007/s002210050804
Debaere, F. et al. Internal vs external generation of movements: Differential neural pathways involved in bimanual coordination performed in the presence or absence of augmented visual feedback. Neuroimage 19(3), 764–776 (2003).
pubmed: 12880805 doi: 10.1016/S1053-8119(03)00148-4
Ronsse, R. et al. Motor learning with augmented feedback: Modality-dependent behavioral and neural consequences. Cerebr. Cortex 21(6), 1283–1294 (2011).
doi: 10.1093/cercor/bhq209
Oldfield, R. C. The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia 9(1), 97–113 (1971).
pubmed: 5146491 doi: 10.1016/0028-3932(71)90067-4
Beck, A. T. et al. An inventory for measuring depression. Arch. Gen. Psychiatry 4(6), 561–571 (1961).
pubmed: 13688369 doi: 10.1001/archpsyc.1961.01710120031004
Maclean, A. W. et al. Psychometric evaluation of the Stanford sleepiness scale. J. Sleep Res. 1(1), 35–39 (1992).
pubmed: 10607023 doi: 10.1111/j.1365-2869.1992.tb00006.x
Sisti, H. M. et al. Testing multiple coordination constraints with a novel bimanual visuomotor task. PLoS ONE 6(8), e23619 (2011).
pubmed: 21858185 pmcid: 3157395 doi: 10.1371/journal.pone.0023619
Monteiro, T. S. et al. Relative cortico-subcortical shift in brain activity but preserved training-induced neural modulation in older adults during bimanual motor learning. Neurobiol. Aging 58, 54–67 (2017).
doi: 10.1016/j.neurobiolaging.2017.06.004
Edden, R. A. & Barker, P. B. Spatial effects in the detection of γ-aminobutyric acid: Improved sensitivity at high fields using inner volume saturation. Magn. Reason. Med. 58(6), 1276–1282 (2007).
doi: 10.1002/mrm.21383
Mescher, M. et al. Simultaneous in vivo spectral editing and water suppression. NMR Biomed. 11(6), 266–272 (1998).
pubmed: 9802468 doi: 10.1002/(SICI)1099-1492(199810)11:6<266::AID-NBM530>3.0.CO;2-J
Mullins, P. G. et al. Current practice in the use of MEGA-PRESS spectroscopy for the detection of GABA. Neuroimage 86, 43–52 (2014).
pubmed: 23246994 doi: 10.1016/j.neuroimage.2012.12.004
Greenhouse, I. et al. Individual differences in GABA content are reliable but are not uniform across the human cortex. Neuroimage 139, 1–7 (2016).
pubmed: 27288552 doi: 10.1016/j.neuroimage.2016.06.007
Edden, R. A. et al. Gannet: A batch-processing tool for the quantitative analysis of gamma-aminobutyric acid–edited MR spectroscopy spectra. J. Magn. Reason. Imaging 40(6), 1445–1452 (2014).
doi: 10.1002/jmri.24478
Mikkelsen, M. et al. Correcting frequency and phase offsets in MRS data using robust spectral registration. NMR Biomed. 33(10), e4368 (2020).
pubmed: 32656879 pmcid: 9652614 doi: 10.1002/nbm.4368
Petroff, O., Yu, R. & Ogino, T. High-resolution proton magnetic resonance analysis of human cerebrospinal fluid. J. Neurochem. 47(4), 1270–1276 (1986).
pubmed: 3746301 doi: 10.1111/j.1471-4159.1986.tb00750.x
Mikkelsen, M. et al. Quantification of γ-aminobutyric acid (GABA) in 1H MRS volumes composed heterogeneously of grey and white matter. NMR Biomed. 29(11), 1644–1655 (2016).
pubmed: 27687518 doi: 10.1002/nbm.3622
Harris, A. D., Puts, N. A. & Edden, R. A. Tissue correction for GABA-edited MRS: Considerations of voxel composition, tissue segmentation, and tissue relaxations. J. Magn. Reason. Imaging 42(5), 1431–1440 (2015).
doi: 10.1002/jmri.24903
Noguchi, K. et al. nparLD: An R software Package for the Nonparametric Analysis of Longitudinal Data in Factorial Experiments (2012).
Bonferroni, C. Teoria statistica delle classi e calcolo delle probabilita. Pubbl. R Istit. Superiore Sci. Econ. Commeric. Firenze 8, 3–62 (1936).
Sink, C. A. & Stroh, H. R. Practical Significance: The Use of Effect Sizes in School Counseling Research 401–411 (Professional School Counseling, 2016).
Boisgontier, H. M. et al. Complexity of central processing in simple and choice multilimb reaction-time tasks. PLoS ONE 9(2), e90457 (2014).
pubmed: 24587371 pmcid: 3938735 doi: 10.1371/journal.pone.0090457
Rasooli, A. et al. Prefronto-striatal structural connectivity mediates adult age differences in action selection. J. Neurosci. 41(2), 331–341 (2021).
pubmed: 33214318 pmcid: 7810660 doi: 10.1523/JNEUROSCI.1709-20.2020
Boisgontier, M. P. et al. Nucleus accumbens and caudate atrophy predicts longer action selection times in young and old adults. Hum. Brain Map. 37(12), 4629–4639 (2016).
doi: 10.1002/hbm.23333
Weigelt, C. et al. Transfer and motor skill learning in association football. Ergonomics 43(10), 1698–1707 (2000).
pubmed: 11083148 doi: 10.1080/001401300750004104
Ausenda, C. & Carnovali, M. Transfer of motor skill learning from the healthy hand to the paretic hand in stroke patients: A randomized controlled trial. Eur. J. Phys. Rehabil. Med. 47(3), 417–425 (2011).
pubmed: 21555982
Raibert, M. H. Motor Control and Learning by the State Space Model (Massachusetts Institute of Technology, 1977).
Imamizu, H. & Shimojo, S. The locus of visual-motor learning at the task or manipulator level: Implications from intermanual transfer. J. Exp. Psychol. 21(4), 719 (1995).
Sathian, K. & Zangaladze, A. Perceptual learning in tactile hyperacuity: Complete intermanual transfer but limited retention. Exp. Brain Res. 118, 131–134 (1998).
pubmed: 9547071 doi: 10.1007/s002210050263
Thorndike, E. L. Educational Psychology Vol. 2 (Columbia university, 1913).
Bapi, R. S., Doya, K. & Harner, A. M. Evidence for effector independent and dependent representations and their differential time course of acquisition during motor sequence learning. Exp. Brain Res. 132, 149–162 (2000).
pubmed: 10853941 doi: 10.1007/s002219900332
Heba, S. et al. Local GABA concentration predicts perceptual improvements after repetitive sensory stimulation in humans. Cerebr. Cortex 26(3), 1295–1301 (2016).
doi: 10.1093/cercor/bhv296
Lea-Carnall, C. A. et al. GABA modulates frequency-dependent plasticity in humans. Iscience 23(11), 101657 (2020).
pubmed: 33163932 pmcid: 7599432 doi: 10.1016/j.isci.2020.101657
Chen, C. et al. Activation induced changes in GABA: Functional MRS at 7 T with MEGA-sLASER. Neuroimage 156, 207–213 (2017).
pubmed: 28533117 doi: 10.1016/j.neuroimage.2017.05.044
Maruyama, S. et al. Cognitive control affects motor learning through local variations in GABA within the primary motor cortex. Sci. Rep. 11(1), 18566 (2021).
pubmed: 34535725 pmcid: 8448760 doi: 10.1038/s41598-021-97974-1
Mikkelsen, M. et al. Designing GABA-edited magnetic resonance spectroscopy studies: Considerations of scan duration, signal-to-noise ratio and sample size. J. Neurosci. Methods 303, 86–94 (2018).
pubmed: 29476871 pmcid: 5940501 doi: 10.1016/j.jneumeth.2018.02.012

Auteurs

Amirhossein Rasooli (A)

Movement Control and Neuroplasticity Research Group, Department of Movement Sciences, Group Biomedical Sciences, KU Leuven, Leuven, Belgium.
Leuven Brain Institute (LBI), KU Leuven, Leuven, Belgium.

Sima Chalavi (S)

Movement Control and Neuroplasticity Research Group, Department of Movement Sciences, Group Biomedical Sciences, KU Leuven, Leuven, Belgium.
Leuven Brain Institute (LBI), KU Leuven, Leuven, Belgium.
ORCID: 0000-0002-2339-8168

Hong Li (H)

Movement Control and Neuroplasticity Research Group, Department of Movement Sciences, Group Biomedical Sciences, KU Leuven, Leuven, Belgium.
Leuven Brain Institute (LBI), KU Leuven, Leuven, Belgium.

Caroline Seer (C)

Movement Control and Neuroplasticity Research Group, Department of Movement Sciences, Group Biomedical Sciences, KU Leuven, Leuven, Belgium.
Leuven Brain Institute (LBI), KU Leuven, Leuven, Belgium.

Hamed Zivari Adab (HZ)

Movement Control and Neuroplasticity Research Group, Department of Movement Sciences, Group Biomedical Sciences, KU Leuven, Leuven, Belgium.
Leuven Brain Institute (LBI), KU Leuven, Leuven, Belgium.

Dante Mantini (D)

Movement Control and Neuroplasticity Research Group, Department of Movement Sciences, Group Biomedical Sciences, KU Leuven, Leuven, Belgium.
Leuven Brain Institute (LBI), KU Leuven, Leuven, Belgium.
ORCID: 0000-0001-6485-5559

Stefan Sunaert (S)

Department of Imaging and Pathology, Group Biomedical Sciences, KU Leuven, Leuven, Belgium.

Mark Mikkelsen (M)

Department of Radiology, Weill Cornell Medicine, New York, NY, USA.

Richard A E Edden (RAE)

Russell H. Morgan Department of Radiology and Radiological Science, The Johns Hopkins University School of Medicine, Baltimore, MD, USA.
F. M. Kirby Research Center for Functional Brain Imaging, Kennedy Krieger Institute, Baltimore, MD, USA.

Stephan P Swinnen (SP)

Movement Control and Neuroplasticity Research Group, Department of Movement Sciences, Group Biomedical Sciences, KU Leuven, Leuven, Belgium. Stephan.Swinnen@kuleuven.be.
Leuven Brain Institute (LBI), KU Leuven, Leuven, Belgium. Stephan.Swinnen@kuleuven.be.
Motor Control Laboratory, Movement Control and Neuroplasticity Research Group, KU Leuven, Tervuurse Vest 101, Building De Nayer, Room 02.11, 3001, Leuven, Belgium. Stephan.Swinnen@kuleuven.be.

Classifications MeSH