Elsevier

Brain and Cognition

Volume 147, February 2021, 105653
Brain and Cognition

Lack of interlimb transfer following visuomotor adaptation in a person with congenital mirror movements despite the awareness of the visuomotor perturbation

https://doi.org/10.1016/j.bandc.2020.105653Get rights and content

Highlights

  • Interlimb transfer of visuomotor adaptation does not occur in a person with CMMs.

  • No transfer in a person with CMMs even when perturbation information is provided.

  • Providing perturbation information had detrimental, rather than beneficial effects.

  • Interlimb transfer of visuomotor adaptation does not depend on one’s awareness.

Abstract

There is a controversy regarding whether visuomotor adaptation heavily involves both implicit and explicit learning processes or not. Likewise, another controversy exists regarding whether interlimb transfer of visuomotor adaptation is related to explicit processes or not. To address the latter issue, we examined interlimb transfer of visuomotor adaptation in an individual with congenital mirror movements, ‘DB’. DB has been tested previously using an experimental paradigm in which neurologically intact individuals demonstrated substantial transfer. DB, however, showed no transfer due to impaired interhemispheric communications. In that study, DB was unaware of the visuomotor perturbation. Here, we informed him of the perturbation prior to the experiment to determine whether providing the information would increase interlimb transfer. DB first adapted to a visuomotor rotation with the left arm, then with the right arm during reaching movements. Data from the present study were compared against those from our previous study. Results indicate no transfer across the arms despite the fact that he was aware of the perturbation. Considering overall findings in the literature, we suggest that interlimb transfer does not depend on one’s awareness, although its extent can increase when individuals rely on cognitive strategies to deal with perturbations (c.f., Werner et al., 2019).

Introduction

Transfer of a motor skill from one limb to the other has long been used as a tool to examine the role of each brain hemisphere in controlling different aspects of motor control and learning (Laszlo et al., 1970, Sainburg and Wang, 2002). Numerous studies were conducted to investigate the pattern of interlimb transfer and demonstrated that the pattern varied across different motor skills. For example, investigators have uncovered skills that transfer from the dominant to the nondominant arm (Wang and Sainburg, 2004, Criscimagna-Hemminger et al., 2003, Ammons, 1958, Gordon et al., 1994, Halsband, 1992) and from the nondominant to the dominant arm (Sainburg and Wang, 2002, Wang and Sainburg, 2006a, Hicks, 1974, Parlow and Kinsbourne, 1990, Taylor and Heilman, 1980), as well as skills that transfer in both directions (Morton et al. 2001) and skills that do not transfer in either direction at all (Baizer et al., 1999, Kitazawa et al., 1997, Rand et al., 1998, Teixeira, 1993).

Some studies also showed that the pattern of interlimb transfer following the performance or adaptation of a motor skill under a novel visuomotor environment can also vary depending on certain factors, such as workspace locations for each arm and movement features in question. Sainburg and Wang demonstrated that the direction of interlimb transfer following visuomotor adaptation depended on the features of reaching movements (i.e., directional vs. positional) (Sainburg and Wang, 2002, Wang and Sainburg, 2006a). They also demonstrated that the directional information transferred only in one direction (i.e., from the nondominant to the dominant arm) when both arms adapted to the visuomotor perturbation in a shared midline workspace, while it transferred in both directions when each arm adapted to the perturbation at an ipsilateral workspace (Wang and Sainburg, 2006b). The direction, or pattern, of interlimb transfer following visuomotor adaptation has also been shown to vary depending on whether the visual and motor workspaces overlapped with each other or not (Wang, 2008, Lei et al., 2013). These findings collectively suggest that the neural mechanisms underlying interlimb transfer of visuomotor adaptation is quite complex.

There is a controversy regarding whether visuomotor adaptation primarily involves implicit learning processes, or both implicit and explicit processes. Some studies argued for the former idea (e.g., Mazzoni and Krakauer, 2006, Benson et al., 2011, Wang et al., 2019), while others argued for the latter (e.g., Taylor et al., 2014, McDougle et al., 2015, Bond and Taylor, 2015). Similarly, a controversy also exists as to whether interlimb transfer of visuomotor adaptation depends on one’s cognitive awareness of the perturbation (i.e., explicit processes) or not (Wang et al., 2011, Taylor et al., 2011, Werner et al., 2019). Wang et al. (2011) conducted a study in which subjects were assigned to three different conditions: one in which they adapted to a 32-deg. visuomotor rotation during targeted reaching movements (abrupt condition), another in which they adapted to a visuomotor rotation whose size gradually increased from zero up to 32 degrees (gradual condition), and another which was the same as the abrupt condition, except that the subjects were informed of the visuomotor perturbation prior to the experiment (informed abrupt condition). Regardless of the conditions they were in, all subjects showed substantial transfer from the left to the right arm in terms of direction errors; and the extent of transfer did not differ across the conditions. Post-experiment interviews revealed that most subjects in the gradual and abrupt conditions were not aware of the nature of the perturbation. Based on these findings, Wang et al. concluded that interlimb transfer does not occur as a result of one’s cognitive awareness of the perturbation. Taylor et al. (2011) also conducted a study that included a similar experimental paradigm, which provided support to the argument made by Wang et al. (2011). More recently, however, Werner et al. (2019) examined interlimb transfer in four conditions in which the rotation size was 30 or 75 degrees and the rotation was provided gradually or abruptly. The authors measured indexes of awareness and unawareness separately, and the results indicated that both awareness and transfer were larger in the abrupt 75-deg. condition, while unawareness was smaller in that condition than in other conditions. Thus, they argued that the amount of interlimb transfer is directly related to the extent of awareness of the perturbation.

In the present study, we examined the effect of the cognitive awareness of a visuomotor perturbation on interlimb transfer of visuomotor adaptation in a person with congenital mirror movements (CMMs), which refer to involuntary movements of one arm observed during voluntary movements of the other (e.g., Cincotta et al., 1994, Ueki et al., 2005, Verstynen et al., 2007, Welniarz et al., 2015). We recently published a study (Bao et al., 2020) in which a person with CMMs adapted to a 30-deg. visuomotor rotation with the left arm first, then with the right arm. Unlike neurologically intact individuals who showed substantial transfer, our subject with CMMs showed no transfer at all. In that study, the subject was not aware of the visuomotor perturbation. In the present study, we informed the same subject of the visuomotor perturbation prior to his participation in the experiment and examined whether the extent of interlimb transfer would increase. We hypothesized that if interlimb transfer of visuomotor adaptation occurred based on one’s cognitive awareness of the visuomotor perturbation, informing the subject of the perturbation would result in an increased extent of interlimb transfer of visuomotor adaptation. Data from the present study were compared against those reported in our previous study (Bao et al., 2020).

Section snippets

Subjects

A person with CMMs (27-year old male, who considered himself right-handed), “DB,” participated in this study. He had no history of neurological issues other than CMMS, that is, involuntary mirror movements in one hand/arm seen when he intended to contract the opposite hand/arm. The subject signed a consent form approved by the Institutional Review Board of the University of Wisconsin-Milwaukee. (For additional information on the characteristics of DB’s CMMs, refer to Bao et al. (2020)).

Apparatus

A

Results

Fig. 2 illustrates DB’s hand-paths during reaching movements from our current study (solid lines). In the baseline session, the hand-paths observed during reaching movements with the left and right arms appear relatively straight and similar to each other, as expected. In the adaptation session, noticeable deviations from imaginary straight target lines were observed in the early phase of adaptation with the left arm (upper middle panel); similar deviations were also observed for the right arm

Discussion

The objective of the present study was to examine the effect of the cognitive awareness of a visuomotor perturbation on interlimb transfer of visuomotor adaptation in a person with congenital mirror movements (CMMs). We compared the pattern of interlimb transfer observed in this study (explicit condition) with that observed in our previous study (Bao et al., (2020); implicit condition). DB, a person with CMMs, showed no transfer between the arms in our previous study, although neurologically

Conclusion

In conclusion, our current and previous (Bao et al., 2020) studies demonstrate that a person with CMMs tested in these studies, DB, can adapt to a novel visuomotor rotation condition during targeted reaching movements with either arm, although interlimb transfer does not occur because of the impaired interhemispheric communications in him. Our studies further demonstrate that in DB, interlimb transfer of visuomotor adaptation does not occur regardless of whether he is aware of the manipulation

CRediT authorship contribution statement

Mousa Javidialsaadi: Conceptualization, Data curation, Formal analysis, Writing - original draft. Jinsung Wang: Conceptualization, Formal analysis, Methodology, Writing - review & editing.

Acknowledgements

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

References (40)

  • Bryan L. Benson et al.

    A spatial explicit strategy reduces error but interferes with sensorimotor adaptation

    Journal of Neurophysiology

    (2011)
  • Krista M. Bond et al.

    Flexible explicit but rigid implicit learning in a visuomotor adaptation task

    Journal of Neurophysiology

    (2015)
  • Krista M. Bond et al.

    Structural Learning in a Visuomotor Adaptation Task Is Explicitly Accessible

    eNeuro

    (2017)
  • Sarah E. Criscimagna-Hemminger et al.

    Learned Dynamics of Reaching Movements Generalize From Dominant to Nondominant Arm

    Journal of Neurophysiology

    (2003)
  • Ulrike Halsband

    Left hemisphere preponderance in trajectorial learning

    NeuroReport

    (1992)
  • Robert E. Hicks

    Asymmetry of Bilateral Transfer

    The American Journal of Psychology

    (1974)
  • S. Kitazawa et al.

    Prism adaptation of reaching movements: Specificity for the velocity of reaching

    Journal of Neuroscience

    (1997)
  • Judith I. Laszlo et al.

    Bilateral Transfer in Tapping Skill in the Absence of Peripheral Information

    Journal of Motor Behavior

    (1970)
  • Li-Ann Leow et al.

    Estimating the implicit component of visuomotor rotation learning by constraining movement preparation time

    Journal of Neurophysiology

    (2017)
  • P. Mazzoni et al.

    An implicit plan overrides an explicit strategy during visuomotor adaptation

    Journal of neuroscience

    (2006)
  • Cited by (2)

    • Generalization of visuomotor adaptation associated with use-dependent learning across different movement workspaces and limb postures

      2022, Human Movement Science
      Citation Excerpt :

      We did not include a control condition that can be used to answer this question, which is a limitation of the present study. However, we recently demonstrated that a person with congenital mirror movements (CMMs), who had previously showed no transfer of visuomotor adaptation from the left to the right arm (Bao et al., 2020; Javidialsaadi & Wang, 2021), was able to show over 90% transfer from the left to the right arm when use-dependent learning (though in the form of active training) with the right arm was included intermittently during visuomotor adaptation with the left arm (Jo, Javidialsaadi, & Wang, 2022). In fact, the subject's initial performance in the transfer session was significantly better than that of the control subjects who only received the same active training with the right arm (i.e., no visuomotor adaptation with the left arm) prior to the transfer session with the right arm.

    • Facilitative effects of use-dependent learning on interlimb transfer of visuomotor adaptation in a person with congenital mirror movements

      2022, Human Movement Science
      Citation Excerpt :

      Given that the person with CMMs tested in our previous studies (Bao et al., 2020; Javidialsaadi & Wang, 2021) showed no interlimb transfer of visuomotor adaptation, we assumed that any transfer observed in the current study would be attributed to use-dependent learning. A right-handed, 29-year-old male with CMMs, DB, who was tested in our previous studies (Bao et al., 2020; Javidialsaadi & Wang, 2021), participated in this study. ( DB was 27 years old when tested in our previous studies.)

    View full text