Inter-task transfer of prism adaptation depends on exposed task mastery.
Acclimatization
/ physiology
Adaptation, Physiological
/ physiology
Adult
Feedback, Sensory
/ physiology
Female
Hand
/ physiology
Humans
Male
Motor Activity
/ physiology
Photic Stimulation
/ methods
Psychomotor Performance
/ physiology
Sensorimotor Cortex
/ physiology
Space Perception
/ physiology
Visual Fields
/ physiology
Visual Perception
/ physiology
Young Adult
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
30 03 2020
30 03 2020
Historique:
received:
10
07
2019
accepted:
05
03
2020
entrez:
2
4
2020
pubmed:
2
4
2020
medline:
2
12
2020
Statut:
epublish
Résumé
The sensorimotor system sets up plastic alterations to face new demands. Terms such as adaptation and learning are broadly used to describe a variety of processes underlying this aptitude. The mechanisms whereby transformations acquired to face a perturbation generalize to other situations or stay context-dependent remain weakly understood. Here, we compared the performance of hand pointing vs throwing to visual targets while facing an optical shift of the visual field (prismatic deviation). We found that the transfer of compensations was conditioned by the task performed during exposure to the perturbation: compensations transferred from pointing to throwing but not at all from throwing to pointing. Additionally, expertise on the task performed during exposure had a marked influence on the amount of transfer to the non-exposed task: throwing experts (dart players) remarkably transferred compensations to the pointing task. Our results reveal that different processes underlying these distinct transfer properties may be at work to face a given perturbation. Their solicitation depends on mastery for the exposed task, which is responsible for different patterns of inter-task transfer. An important implication is that transfer properties, and not only after-effects, should be included as a criterion for adaptation. At the theoretical level, we suggest that tasks may need to be mastered before they can be subjected to adaptation, which has new implications for the distinction between learning and adaptation.
Identifiants
pubmed: 32231235
doi: 10.1038/s41598-020-62519-5
pii: 10.1038/s41598-020-62519-5
pmc: PMC7105469
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
5687Références
Poggio, T. & Bizzi, E. Generalization in vision and motor control. Nature 431, 768–774 (2004).
doi: 10.1038/nature03014
Bastian, A. J. Understanding sensorimotor adaptation and learning for rehabilitation. Curr. Opin. Neurol. 21, 628–633 (2008).
doi: 10.1097/WCO.0b013e328315a293
Fleury, L., Prablanc, C. & Priot, A.-E. Do prism and other adaptation paradigms really measure the same processes? Cortex J. Devoted Study Nerv. Syst. Behav. 119, 480–496 (2019).
doi: 10.1016/j.cortex.2019.07.012
Redding, G. M., Rossetti, Y. & Wallace, B. Applications of prism adaptation: a tutorial in theory and method. Neurosci. Biobehav. Rev. 29, 431–444 (2005).
doi: 10.1016/j.neubiorev.2004.12.004
Telgen, S., Parvin, D. & Diedrichsen, J. Mirror reversal and visual rotation are learned and consolidated via separate mechanisms: recalibrating or learning de novo? J. Neurosci. Off. J. Soc. Neurosci. 34, 13768–13779 (2014).
doi: 10.1523/JNEUROSCI.5306-13.2014
Prablanc, C. et al. Adapting terminology: clarifying prism adaptation vocabulary, concepts, and methods. Neurosci. Res., https://doi.org/10.1016/j.neures.2019.03.003 (2019).
Welch, R. B. Speculations on a Model of Prism Adaptation. Perception 3, 451–460 (1974).
doi: 10.1068/p030451
O’Shea, J. et al. Kinematic markers dissociate error correction from sensorimotor realignment during prism adaptation. Neuropsychologia 55, 15–24 (2014).
doi: 10.1016/j.neuropsychologia.2013.09.021
Taylor, J. A. & Ivry, R. B. Context-dependent generalization. Front. Hum. Neurosci. 7 (2013).
Rossetti, Y., Koga, K. & Mano, T. Prismatic displacement of vision induces transient changes in the timing of eye-hand coordination. Percept. Psychophys. 54, 355–364 (1993).
doi: 10.3758/BF03205270
Held, R. & Gottlieb, N. Technique for Studying Adaptation to Disarranged Hand-Eye Coordination. Percept. Mot. Skills 8, 83–86 (1958).
doi: 10.2466/pms.1958.8.3.83
Weiner, M. J., Hallett, M. & Funkenstein, H. H. Adaptation to lateral displacement of vision in patients with lesions of the central nervous system. Neurology 33, 766–772 (1983).
doi: 10.1212/WNL.33.6.766
Rossetti, Y. et al. Prism adaptation to a rightward optical deviation rehabilitates left hemispatial neglect. Nature 395, 166–169 (1998).
doi: 10.1038/25988
Inoue, M. et al. Three timescales in prism adaptation. J. Neurophysiol. 113, 328–338 (2015).
doi: 10.1152/jn.00803.2013
Redding, G. M. & Wallace, B. Adaptive spatial alignment and strategic perceptual-motor control. J. Exp. Psychol. Hum. Percept. Perform. 22, 379–394 (1996).
doi: 10.1037/0096-1523.22.2.379
Kitazawa, S., Kimura, T. & Uka, T. Prism adaptation of reaching movements: specificity for the velocity of reaching. J. Neurosci. Off. J. Soc. Neurosci. 17, 1481–1492 (1997).
doi: 10.1523/JNEUROSCI.17-04-01481.1997
Baraduc, P. & Wolpert, D. M. Adaptation to a Visuomotor Shift Depends on the Starting Posture. J. Neurophysiol. 88, 973–981 (2002).
doi: 10.1152/jn.2002.88.2.973
Fernandez-Ruiz, J. et al. Normal prism adaptation but reduced after-effect in basal ganglia disorders using a throwing task. Eur. J. Neurosci. 18, 689–694 (2003).
doi: 10.1046/j.1460-9568.2003.02785.x
Martin, T. A., Keating, J. G., Goodkin, H. P., Bastian, A. J. & Thach, W. T. Throwing while looking through prisms. I. Focal olivocerebellar lesions impair adaptation. Brain J. Neurol. 119(Pt 4), 1183–1198 (1996).
doi: 10.1093/brain/119.4.1183
Bedford, F. Perceptual and cognitive spatial learning. J. Exp. Psychol. Hum. Percept. Perform. 19, 517–530 (1993).
doi: 10.1037/0096-1523.19.3.517
Redding, G. M. & Wallace, B. Generalization of prism adaptation. J. Exp. Psychol. Hum. Percept. Perform. 32, 1006–1022 (2006).
doi: 10.1037/0096-1523.32.4.1006
Michel, C., Rossetti, Y., Rode, G. & Tilikete, C. After-effects of visuo-manual adaptation to prisms on body posture in normal subjects. Exp. Brain Res. 148, 219–226 (2003).
doi: 10.1007/s00221-002-1294-3
Michel, C., Vernet, P., Courtine, G., Ballay, Y. & Pozzo, T. Asymmetrical after-effects of prism adaptation during goal oriented locomotion. Exp. Brain Res. 185, 259–268 (2008).
doi: 10.1007/s00221-007-1152-4
Girardi, M., McIntosh, R. D., Michel, C., Vallar, G. & Rossetti, Y. Sensorimotor effects on central space representation: prism adaptation influences haptic and visual representations in normal subjects. Neuropsychologia 42, 1477–1487 (2004).
doi: 10.1016/j.neuropsychologia.2004.03.008
Savin, D. N. & Morton, S. M. Asymmetric generalization between the arm and leg following prism-induced visuomotor adaptation. Exp. Brain Res. 186, 175–182 (2008).
doi: 10.1007/s00221-007-1220-9
Morton, S. M. Prism Adaptation During Walking Generalizes to Reaching and Requires the Cerebellum. J. Neurophysiol. 92, 2497–2509 (2004).
doi: 10.1152/jn.00129.2004
Spang, K., Wischhusen, S. & Fahle, M. Limited Plasticity of Prismatic Visuomotor Adaptation. -Percept. 8, 2041669517701458 (2017).
Wagner, H., Pfusterschmied, J., Klous, M., von Duvillard, S. P. & Müller, E. Movement variability and skill level of various throwing techniques. Hum. Mov. Sci. 31, 78–90 (2012).
doi: 10.1016/j.humov.2011.05.005
Redding, G. M. & Wallace, B. Strategic calibration and spatial alignment: a model from prism adaptation. J. Mot. Behav. 34, 126–138 (2002).
doi: 10.1080/00222890209601935
Jeannerod, M. & Rossetti, Y. Visuomotor coordination as a dissociable visual function: experimental and clinical evidence. Baillieres Clin. Neurol. 2, 439–460 (1993).
Bedford, F. L. Constraints on perceptual learning: objects and dimensions. Cognition 54, 253–297 (1995).
doi: 10.1016/0010-0277(94)00637-Z
Cothros, N., Wong, J. D. & Gribble, P. L. Are there distinct neural representations of object and limb dynamics? Exp. Brain Res. 173, 689–697 (2006).
doi: 10.1007/s00221-006-0411-0
Harris, C. S. Adaptation to Displaced Vision: Visual, Motor, or Proprioceptive Change? Science 140, 812–813 (1963).
doi: 10.1126/science.140.3568.812
Herzfeld, D. J. & Shadmehr, R. Motor variability is not noise, but grist for the learning mill. Nat. Neurosci. 17, 149–150 (2014).
doi: 10.1038/nn.3633
Wu, H. G., Miyamoto, Y. R., Castro, L. N. G., Ölveczky, B. P. & Smith, M. A. Temporal structure of motor variability is dynamically regulated and predicts motor learning ability. Nat. Neurosci. 17, 312–321 (2014).
doi: 10.1038/nn.3616
Lefumat, H. Z. et al. To transfer or not to transfer? Kinematics and laterality quotient predict interlimb transfer of motor learning. J. Neurophysiol. jn.00749.2015, https://doi.org/10.1152/jn.00749.2015 (2015).
Kast, V. & Leukel, C. Motor Experts Care about Consistency and Are Reluctant to Change Motor Outcome. PloS One 11, e0161798 (2016).
doi: 10.1371/journal.pone.0161798
Fitts, P. M. & Posner, M. I. Human Performance. (Brooks/Cole Publishing Company, 1967).
Leukel, C., Gollhofer, A. & Taube, W. In Experts, underlying processes that drive visuomotor adaptation are different than in Novices. Front. Hum. Neurosci. 9 (2015).
Taylor, J. A. & Ivry, R. B. The role of strategies in motor learning. Ann. N. Y. Acad. Sci. 1251, 1–12 (2012).
doi: 10.1111/j.1749-6632.2011.06430.x
Lin, C.-H., Lien, Y.-H., Wang, S.-F. & Tsauo, J.-Y. Hip and knee proprioception in elite, amateur, and novice tennis players. Am. J. Phys. Med. Rehabil. 85, 216–221 (2006).
doi: 10.1097/01.phm.0000200376.12974.41
Wei, K. & Körding, K. Relevance of error: what drives motor adaptation? J. Neurophysiol. 101, 655–664 (2009).
doi: 10.1152/jn.90545.2008