Two Processes in Early Bimanual Motor Skill Learning

Maral Yeganeh Doost, Jean-Jacques Orban de Xivry, Benoît Bihin, Yves Vandermeeren, Maral Yeganeh Doost, Jean-Jacques Orban de Xivry, Benoît Bihin, Yves Vandermeeren

Abstract

Most daily activities are bimanual and their efficient performance requires learning and retention of bimanual coordination. Despite in-depth knowledge of the various stages of motor skill learning in general, how new bimanual coordination control policies are established is still unclear. We designed a new cooperative bimanual task in which subjects had to move a cursor across a complex path (a circuit) as fast and as accurately as possible through coordinated bimanual movements. By looking at the transfer of the skill between different circuits and by looking at training with varying circuits, we identified two processes in early bimanual motor learning. Loss of performance due to the switch in circuit after 15 min of training amounted to 20%, which suggests that a significant portion of improvements in bimanual performance is specific to the used circuit (circuit-specific skill). In contrast, the loss of performance due to the switch in circuit was 5% after 4 min of training. This suggests that learning the new bimanual coordination control policy dominates early in the training and is independent of the used circuit. Finally, switching between two circuits throughout training did not affect the early stage of learning (i.e., the first few minutes), but did affect the later stage. Together, these results suggest that early bimanual motor skill learning includes two different processes. Learning the new bimanual coordination control policy predominates in the first minutes whereas circuit-specific skill improvements unfold later in parallel with further improvements in the bimanual coordination control policy.

Keywords: bimanual coordination; bimanual motor skill learning; inter-limb coordination; motor coordination; motor learning; motor skill learning; robotics.

Figures

FIGURE 1
FIGURE 1
Experimental setup. (A) The three forms of the circuit experienced by the subjects: circuit 2 (C2) was the rotated form of circuit 1 (C1); circuit 3 (C3) had the same segments with a different order. (B) Order of presentation of the circuits for the five groups. The color of the bars indicates which circuit is used. (C) In this bimanual task, the right hand was restricted to move in horizontal axis and the left hand to vertical axis in the XY plane. Based on the orientation and angle (±45°) of each segment of the circuits, there are four possibilities for achieving successful coordinated bimanual movements: For the segments with 45° from the X-axis, (1) to ascend, subjects need to go right with the right hand and up with the left hand; (2) to descend, they need to go left with the right hand and down with the left hand, and for the segments with –45° from the X-axis, (3) to ascend, they need to go left with the right hand and up with the left hand; (4) to descend, they need to go right with the right hand and go down with the left hand. (D) The error was computed as the surface between the cursor trajectory and the ideal trajectory (light blue area), defined as the midline of the track. The orange line represents the real trajectory of the cursor.
FIGURE 2
FIGURE 2
Behavior during the first and 30th minute of training. (Top) Cursor trajectory during the 1st minute of the training (left, green trace) and during the 30th minute of training (right, red trace). (Bottom) Velocities of the left (red) and right (blue) hands (sample of 5 s between 10 and 15 s after the go signal), bottom left: on the 1st minute of training; bottom right: on the 30th minute of training.
FIGURE 3
FIGURE 3
Evolution of the outcome measures for Long_C1 and Long_C2. The plots demonstrate the evolution of the mean of the 3 outcome measures for Long_C1 (in green) during the 2 days of training and Long_C2 (in blue) during 1 day of training. The top plot shows the mean values of Bi-SAT; Bi-Co is in the middle plot and the lowest plot indicates the Bi-F. Error bars represent standard error of the mean (SEM).
FIGURE 4
FIGURE 4
Change in the outcomes with different training regimens. Individual data points (in gray) are shown for the percentage of change between the 1st and last block of training in Bi-SAT (top), Bi-Co (middle) and Bi-F (bottom). The red dots represent medians and the black dots represent means with the black bars showing SEM. For Bi-SAT and Bi-Co, a change greater than 1 corresponds to improvement; for Bi-F, the percentage of change should be smaller than 1 as a decrease in the non-desired force reflects performance improvement.
FIGURE 5
FIGURE 5
Evolution of the mean in Bi-SAT and Bi-Co for the Switch groups. Data from the Switch_C1/C2 is represented by the orange curve and that of the Switch_C2/C1 by the black curve. The angle of the diamond illustrates the circuit used on a particular block. Error bars represent SEM.
FIGURE 6
FIGURE 6
Performance drop after the circuit-switch in early vs. later phases of bimanual motor skill learning. Individual data points (in gray) are shown for the loss of performance (in %) between the last block of training and the transfer block (the blocks 15 and 16 for the Long_C2 group and the blocks 4 and 5 for the Short_C2 group). The red dots represent medians and the black dots represent means with the black bars showing standard error of the mean. Note that the scale is different for Bi-SAT and Bi-Co.

References

    1. Clark D., Ivry R. B. (2010). Multiple systems for motor skill learning. Wiley Interdiscip. Rev. Cogn. Sci. 1 461–467. 10.1002/wcs.56
    1. Dayan E., Cohen L. G. (2011). Neuroplasticity subserving motor skill learning. Neuron 72 443–454. 10.1016/j.neuron.2011.10.008
    1. Diedrichsen J., Shadmehr R., Ivry R. B. (2010). The coordination of movement: optimal feedback control and beyond. Trends Cogn. Sci. 14 31–39. 10.1016/j.tics.2009.11.004
    1. Doyon J., Penhune V., Ungerleider L. G. (2003). Distinct contribution of the cortico-striatal and cortico- cerebellar systems to motor skill learning. Neuropsychologia 41 252–262. 10.1016/j.conb.2003.10.014
    1. Fitts P. M., Posner M. I. (1967). Human Performance. Eugene, OR: University of Oregon.
    1. Haken H., Kelso J. A., Bunz H. (1985). A theoretical model of phase transitions in human hand movements. Biol. Cybern. 51 347–356. 10.1007/BF00336922
    1. Johnson M. J., Wang S., Bai P., Strachota E., Tchekanov G., Melbye J., et al. (2011). Bilateral assessment of functional tasks for robot-assisted therapy applications. Med. Biol. Eng. Comput. 49 1157–1171. 10.1007/s11517-011-0817-0
    1. Karni A., Meyer G., Rey-Hipolito C., Jezzard P., Adams M. M., Turner R., et al. (1998). The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex. Proc. Natl. Acad. Sci. U.S.A. 95 861–868. 10.1073/pnas.95.3.861
    1. Kelso J. A. (1984). Phase transitions and critical behavior in human bimanual coordination. Am. J. Physiol. 246(6 Pt 2) R1000–R1004.
    1. Krakauer J. W., Mazzoni P. (2011). Human sensorimotor learning: adaptation, skill, and beyond. Curr. Opin. Neurobiol. 21 636–644. 10.1016/j.conb.2011.06.012
    1. Lafe C. W., Pacheco M. M., Newell K. M. (2016). Adapting relative phase of bimanual isometric force coordination through scaling visual information intermittency. Hum. Mov. Sci. 47 186–196. 10.1016/j.humov.2016.03.011
    1. Lefebvre S., Dricot L., Gradkowski W., Laloux P., Vandermeeren Y. (2012a). Brain activations underlying different patterns of performance improvement during early motor skill learning. Neuroimage 62 290–299. 10.1016/j.neuroimage.2012.04.052
    1. Lefebvre S., Dricot L., Laloux P., Gradkowski W., Desfontaines P., Evrard F., et al. (2015). Neural substrates underlying stimulation-enhanced motor skill learning after stroke. Brain 138 149–163. 10.1093/brain/awu336
    1. Lefebvre S., Laloux P., Peeters A., Desfontaines P., Jamart J., Vandermeeren Y. (2012b). Dual-tDCS enhances online motor skill learning and long-term retention in chronic stroke patients. Front. Hum. Neurosci. 6:343. 10.3389/fnhum.2012.00343
    1. Luft A. R., Buitrago M. M. (2005). Stages of motor skill learning. Mol. Neurobiol. 32 205–216. 10.1385/MN:32:3:205
    1. Maes C., Gooijers J., Orban de Xivry J. J., Swinnen S. P., Boisgontier M. P. (2017). Two hands, one brain, and aging. Neurosci. Biobehav. Rev. 75 234–256. 10.1016/j.neubiorev.2017.01.052
    1. Magill R. A., Hall K. G. (1990). A review of the contextual interference effect in motor skill acquisition. Hum. Mov. Sci. 9 241–289. 10.1016/0167-9457(90)90005-X
    1. McCombe Waller S., Harris-Love M., Liu W., Whitall J. (2006). Temporal coordination of the arms during bilateral simultaneous and sequential movements in patients with chronic hemiparesis. Exp. Brain Res. 168 450–454. 10.1007/s00221-005-0235-3
    1. Pauwels L., Swinnen S. P., Beets I. A. M. (2014). Contextual interference in complex bimanual skill learning leads to better skill persistence. PLOS ONE 9:e100906. 10.1371/journal.pone.0100906
    1. Platz T., Roschka S., Christel M. I., Duecker F., Rothwell J. C., Sack A. T. (2012). Early stages of motor skill learning and the specific relevance of the cortical motor system - a combined behavioural training and theta burst tms study. Restor. Neurol. Neurosci. 30 199–211. 10.3233/RNN-2012-110204
    1. Puttemans V., Wenderoth N., Swinnen S. P. (2005). Changes in brain activation during the acquisition of a multifrequency bimanual coordination task: from the cognitive stage to advanced levels of automaticity. J. Neurosci. 25 4270–4278. 10.1523/JNEUROSCI.3866-04.2005
    1. Reis J., Schambra H. M., Cohen L. G., Buch E. R., Fritsch B., Zarahn E., et al. (2017). Noninvasive Cortical Stimulation Enhances Motor Skill Acquisition Over Multiple Days Through an Effect on Consolidation. Available at: [accessed April 25 2017].
    1. Rosenblum M., Kurths J. (1998). “Analysing synchronization phenomena from bivariate data by means of the hilbert transform,” in Nonlinear Analysis of Physiological Data eds Kantz H., Kurths J., Mayer-Kress G. (Berlin: Springer; ) 91–99.
    1. Sailer U., Flanagan J. R., Johansson R. S. (2005). Eye–Hand coordination during learning of a novel visuomotor task. J. Neurosci. 25 8833–8842. 10.1523/JNEUROSCI.2658-05.2005
    1. Salimpour Y., Shadmehr R. (2014). Motor costs and the coordination of the two arms. J. Neurosci. 34 1806–1818. 10.1523/JNEUROSCI.3095-13.2014
    1. Sallagoïty I., Athènes S., Zanone P. G., Albaret J. M. (2004). Stability of coordination patterns in handwriting: effects of speed and hand. Mot. Control 8 405–421.
    1. Schmidt R. A. (1975). A schema theory of discrete motor skill learning. Psychol. Rev. 82 225–260. 10.1037/h0076770
    1. Shea C. H., Wulf G. (2005). Schema theory: a critical appraisal and reevaluation. J. Mot. Behav. 37 85–101. 10.3200/JMBR.37.2.85-102
    1. Shmuelof L., Krakauer J. W. (2011). Are we ready for a natural history of motor learning? Neuron 72 469–476. 10.1016/j.neuron.2011.10.017
    1. Shmuelof L., Krakauer J. W., Mazzoni P. (2012). How is a motor skill learned? change and invariance at the levels of task success and trajectory control. J. Neurophysiol. 108 578–94. 10.1152/jn.00856.2011
    1. Sisti H. M., Geurts M., Clerckx R., Gooijers J., Coxon J. P., Heitger M. H., et al. (2011). Testing multiple coordination constraints with a novel bimanual visuomotor task. PLOS ONE 6:e23619. 10.1371/journal.pone.0023619
    1. Sleimen-Malkoun R., Temprado J. J., Thefenne L., Berton E. (2011). Bimanual training in stroke: how do coupling and symmetry-breaking matter? BMC Neurol. 11:11. 10.1186/1471-2377-11-11
    1. Swinnen S. P. (2002). Intermanual coordination: from behavioural principles to neural-network interactions. Nat. Rev. Neurosci. 3 348–359. 10.1038/Nrn807
    1. Swinnen S. P., Gooijers J. (2015). “Bimanual coordination,” in Brain Mapping: An Encyclopedic Reference Vol. 2 ed. Toga W. (Cambridge, MA: Academic Press; ) 475–482.
    1. Willingham D. B. (1998). A neuropsychological theory of motor skill learning. Psychol. Rev. 105 558–584. 10.1037/0033-295X.105.3.558
    1. Wu C. Y., Chou S. H., Chen C. L., Kuo M. Y., Lu T. W., Fu Y. C. (2009). Kinematic analysis of a functional and sequential bimanual task in patients with left hemiparesis: intra-limb and interlimb coordination. Disabil. Rehabil. 31 958–966. 10.1080/09638280802358357

Source: PubMed

Patrocinadores y Colaboradores

Condiciones médicas

Intervenciones de drogas

3
Suscribir