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01-02-2025 | Research

Reliability of online visual and proprioceptive feedback: impact on learning and sensorimotor coding

Auteurs: Cécile R. Scotto, Marie Bernardo, Romain Tisserand, Géry Casiez, Yannick Blandin

Gepubliceerd in: Psychological Research | Uitgave 1/2025

Abstract

Multisensory integration is essential for learning and sensorimotor coding, facilitating learners’ adaptation to environmental changes. Recent findings confirm that introducing unreliability into visual feedback enhances the use of motor coding, probably because proprioceptive cues are given greater weight. The present study was designed to test this hypothesis and, more generally, to explore the impact of visual versus proprioceptive cue reliability on learning processes. Participants performed a 12-target pointing sequence 100 times with different combinations of visual and proprioceptive feedback: reliable versus unreliable. Retention tests and intermanual transfer tests were administered 24 h later. Results showed that learning and sensorimotor coding were both affected by the different combinations of visual and proprioceptive cue reliability. Fully reliable feedback allowed for the best retention, while fully unreliable feedback resulted in the worst retention. Visual reliability alone mediated the level of visuospatial coding performance in visuospatial transfer, regardless of the level of proprioceptive reliability, and conversely, reliable proprioception combined with unreliable vision provided the optimum sensory environment for motor coding in the motor transfer test. Overall, our study highlighted the essential role of both visual cue reliability and proprioceptive cue reliability -and their interactions- in motor learning and its generalization.

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Abrahamse, E. L., Jiménez, L., Verwey, W. B., & Clegg, B. A. (2010). Representing serial action and perception. Psychonomic Bulletin & Review, 17, 603–623. https://doi.org/10.3758/PBR.17.5.603

Adams, J. A. (1977). Feedback theory of how joint receptors regulate the timing and positioning of a limb. Psychological Review, 84(6), 504–523. https://doi.org/10.1037/0033-295X.84.6.504CrossRefPubMed

Bernardo, M., Blandin, Y., Casiez, G., & Scotto, C. R. (2023a). Reliability of on-line visual feedback influences learning of continuous motor task of healthy young adults. Frontiers in Psychology, 14. https://www.frontiersin.org/articles/https://doi.org/10.3389/fpsyg.2023.1234010

Bernardo, M., Blandin, Y., Casiez, G., & Scotto, C. R. (2023b). Use of variable online visual feedback to optimize sensorimotor coding and learning of a motor sequence. PloS One, 18(11), e0294138. https://doi.org/10.1371/journal.pone.0294138CrossRefPubMedPubMedCentral

Blandin, Y., Toussaint, L., & Shea, C. H. (2008). Specificity of practice: Interaction between concurrent sensory information and terminal feedback. Journal of Experimental Psychology: Learning Memory and Cognition, 34(4), 994–1000. https://doi.org/10.1037/0278-7393.34.4.994CrossRefPubMed

Block, H. J., & Sexton, B. M. (2020). Visuo-Proprioceptive Control of the Hand in older adults. Multisensory Research, 34(1), 93–111. https://doi.org/10.1163/22134808-bja10032CrossRefPubMed

Bock, O., Vercher, J. L., & Gauthier, G. M. (2005). Wrist vibration affects the production of finely graded forces. Aviation Space and Environmental Medicine, 76(5), 435–440.

Bock, O., Pipereit, K., & Mierau, A. (2007). A method to reversibly degrade proprioceptive feedback in research on human motor control. Journal of Neuroscience Methods, 160(2), 246–250. https://doi.org/10.1016/j.jneumeth.2006.09.010CrossRefPubMed

Boutin, A., Fries, U., Panzer, S., Shea, C. H., & Blandin, Y. (2010). Role of action observation and action in sequence learning and coding. Acta Psychologica, 135(2). https://doi.org/10.1016/j.actpsy.2010.07.005

Boutin, A., Badets, A., Salesse, R. N., Fries, U., Panzer, S., & Blandin, Y. (2012). Practice makes transfer of motor skills imperfect. Psychological Research Psychologische Forschung, 76, 611–625. https://doi.org/10.1007/s00426-011-0355-2CrossRefPubMed

Boutin, A., Blandin, Y., Massen, C., Heuer, H., & Badets, A. (2014). Conscious awareness of action potentiates sensorimotor learning. Cognition, 133, 1–9. https://doi.org/10.1016/j.cognition.2014.05.012CrossRefPubMed

Capaday, C., & Cooke, J. D. (1981). The effects of muscle vibration on the attainment of intended final position during voluntary human arm movements. Experimental Brain Research, 42(2), 228–230. https://doi.org/10.1007/BF00236912CrossRefPubMed

Casadei, K., & Kiel, J. (2023). Anthropometric Measurement. In StatPearls. StatPearls Publishing. http://www.ncbi.nlm.nih.gov/books/NBK537315/

Coello, Y., Orliaguet, J. P., & Prablanc, C. (1996). Pointing movement in an artificial perturbing inertial field: A prospective paradigm for motor control study. Neuropsychologia, 34(9). https://doi.org/10.1016/0028-3932(96)00003-6. Article 9.

Cole, J. D., & Katifi, H. A. (1991). Evoked potentials in a man with a complete large myelinated fibre sensory neuropathy below the neck. Electroencephalography and Clinical Neurophysiology, 80(2). https://doi.org/10.1016/0168-5597(91)90147-p

Cole, J., & Paillard, J. (1995). Living Without Touch and Peripheral Information About Body Position and Movement: Studies with Deafferented Subjects. In J. L. Bermudez, A. J. Marcel, & N. M. Eilan (Éds.), The Body and the Self (pp. 245–266). MIT Press.

Cordo, P., Gurfinkel, V. S., Bevan, L., & Kerr, G. K. (1995). Proprioceptive consequences of tendon vibration during movement. Journal of Neurophysiology, 74(4), 1675–1688. https://doi.org/10.1152/jn.1995.74.4.1675CrossRefPubMed

Criscimagna-Hemminger, S. E., Donchin, O., Gazzaniga, M. S., & Shadmehr, R. (2003). Learned dynamics of reaching movements generalize from dominant to nondominant arm. Journal of Neurophysiology, 89(1). https://doi.org/10.1152/jn.00622.2002

Cuppone, A. V., Semprini, M., & Konczak, J. (2018). Consolidation of human somatosensory memory during motor learning. Behavioural Brain Research, 347, 184–192. https://doi.org/10.1016/j.bbr.2018.03.013CrossRefPubMed

de Leva, P. (1996). Adjustments to Zatsiorsky-Seluyanov’s segment inertia parameters. Journal of Biomechanics, 29(9). https://doi.org/10.1016/0021-9290(95)00178-6. Article 9.

Dean, N. J., Kovacs, A. J., & Shea, C. H. (2008). Transfer of movement sequences: Bigger is better. Acta Psychologica, 127(2), 355–368. https://doi.org/10.1016/j.actpsy.2007.07.004CrossRefPubMed

Doyon, J., Penhune, V., & Ungerleider, L. G. (2003). Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning. Neuropsychologia, 41(3), 252–262. https://doi.org/10.1016/S0028-3932(02)00158-6CrossRefPubMed

Ernst, M. O., & Banks, M. S. (2002). Humans integrate visual and haptic information in a statistically optimal fashion. Nature, 415(6870). https://doi.org/10.1038/415429a. Article 6870.

Ernst, M. O., & Bülthoff, H. H. (2004). Merging the senses into a robust percept. Trends in Cognitive Sciences, 8(4). https://doi.org/10.1016/j.tics.2004.02.002

Faul, F., Erdfelder, E., Lang, A. G., & Buchner, A. (2007). G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Research Methods, 39(2), 175–191. https://doi.org/10.3758/bf03193146CrossRefPubMed

Ghafouri, M., Archambault, P. S., Adamovich, S. V., & Feldman, A. G. (2002). Pointing movements may be produced in different frames of reference depending on the task demand. Brain Research, 929(1). https://doi.org/10.1016/s0006-8993(01)03332-7

Goodman, R., & Tremblay, L. (2018). Using proprioception to control ongoing actions: Dominance of vision or altered proprioceptive weighing? Experimental Brain Research, 236(7). https://doi.org/10.1007/s00221-018-5258-7. Article 7.

Goodman, R., Crainic, V. A., Bested, S. R., Wijeyaratnam, D. O., de Grosbois, J., & Tremblay, L. (2018). Amending Ongoing Upper-Limb reaches: Visual and proprioceptive contributions? Multisensory Research, 31(5), 455–480. https://doi.org/10.1163/22134808-00002615CrossRefPubMed

Goodwin, G. M., McCloskey, D. I., & Matthews, P. B. (1972). Proprioceptive illusions induced by muscle vibration: Contribution by muscle spindles to perception? Science (New York N Y), 175(4028), 1382–1384. https://doi.org/10.1126/science.175.4028.1382CrossRefPubMed

Hagbarth, K. E., & Eklund, G. (1966). Motor effects of vibratory muscle stimuli in man. In Muscular Afferents and Motor Control, pp. 177–186. Proceedings of the 1st Nobel Symposium, 1965, Sodergarn. Edited by R. Granit. Almqvist and Wiksell: Stockholm.

Hay, J. C., & Pick, H. L. (1966). Visual and proprioceptive adaptation to optical displacement of the visual stimulus. Journal of Experimental Psychology, 71(1), 150–158. https://doi.org/10.1037/h0022611CrossRefPubMed

Heus, R., Daanen, H. A., & Havenith, G. (1995). Physiological criteria for functioning of hands in the cold: A review. Applied Ergonomics, 26(1), 5–13. https://doi.org/10.1016/0003-6870(94)00004-iCrossRefPubMed

Hewitson, C. L., Sowman, P. F., & Kaplan, D. M. (2018). Interlimb generalization of learned bayesian Visuomotor Prior occurs in extrinsic coordinates. Eneuro, 5(4). https://doi.org/10.1523/ENEURO.0183-18.2018. Article 4.

Hikosaka, O., Nakahara, H., Rand, M. K., Sakai, K., Lu, X., Nakamura, K., Miyachi, S., & Doya, K. (1999). Parallel neural networks for learning sequential procedures. Trends in Neurosciences, 22(10). https://doi.org/10.1016/s0166-2236(99)01439-3

Hikosaka, O., Nakamura, K., Sakai, K., & Nakahara, H. (2002). Central mechanisms of motor skill learning. Current Opinion in Neurobiology, 12(2). https://doi.org/10.1016/S0959-4388(02)00307-0

Jordan, M. I., & Wolpert, D. M. (1999). Computational motor control. The Cognitive Neurosciences. M. Gazzaniga, (Ed.). Cambridge, MA: MIT Press.

Kazak, A. E. (2018). Editorial: Journal article reporting standards. 1–2.

Körding, K. P., & Wolpert, D. M. (2004). Bayesian integration in sensorimotor learning. Nature, 427(6971). https://doi.org/10.1038/nature02169. Article 6971.

Kovacs, A. J., Mühlbauer, T., & Shea, C. H. (2009). The coding and effector transfer of movement sequences. Journal of Experimental Psychology Human Perception and Performance, 35(2). https://doi.org/10.1037/a0012733

Krakauer, J. W., & Mazzoni, P. (2011). Human sensorimotor learning: Adaptation, skill, and beyond. Current Opinion in Neurobiology, 21(4). https://doi.org/10.1016/j.conb.2011.06.012

Krakauer, J. W., Hadjiosif, A. M., Xu, J., Wong, A. L., & Haith, A. M. (2019). Motor Learning. Comprehensive Physiology (pp. 613–663). Wiley. https://doi.org/10.1002/cphy.c170043

Lai, Q., & Shea, C. H. (1998). Generalized Motor Program (GMP) Learning: Effects of reduced frequency of knowledge of results and practice variability. Journal of Motor Behavior, 30(1), 51–59. https://doi.org/10.1080/00222899809601322CrossRefPubMed

Lange, R. K., Godde, B., & Braun, C. (2004). EEG correlates of coordinate processing during intermanual transfer. Experimental Brain Research, 159(2). https://doi.org/10.1007/s00221-004-1942-x

Leys, C., Ley, C., Klein, O., Bernard, P., & Licata, L. (2013). Detecting outliers: Do not use standard deviation around the mean, use absolute deviation around the median. Journal of Experimental Social Psychology, 49(4), 764–766. https://doi.org/10.1016/j.jesp.2013.03.013CrossRef

Liu, Y., Sexton, B. M., & Block, H. J. (2018). Spatial bias in estimating the position of visual and proprioceptive targets. Journal of Neurophysiology, 119(5), 1879–1888. https://doi.org/10.1152/jn.00633.2017CrossRefPubMed

Meugnot, A., & Toussaint, L. (2015). Functional plasticity of sensorimotor representations following short-term immobilization of the dominant versus non-dominant hands. Acta Psychologica, 155, 51–56. https://doi.org/10.1016/j.actpsy.2014.11.013CrossRefPubMed

Miall, R. C., Kitchen, N. M., Nam, S. H., Lefumat, H., Renault, A. G., Ørstavik, K., Cole, J. D., & Sarlegna, F. R. (2018). Proprioceptive loss and the perception, control and learning of arm movements in humans: Evidence from sensory neuronopathy. Experimental Brain Research, 236(8), 2137–2155. https://doi.org/10.1007/s00221-018-5289-0CrossRefPubMedPubMedCentral

Mizelle, J. C., Oparah, A., & Wheaton, L. A. (2016). Reliability of visual and somatosensory feedback in Skilled Movement: The role of the Cerebellum. Brain Topography, 29(1), 27–41. https://doi.org/10.1007/s10548-015-0446-2CrossRefPubMed

Mon-Williams, M., Wann, J., Jenkinson, M., & Rushton, K. (1997). Synaesthesia in the normal limb. Proceedings Biological Sciences, 264(1384), 1007–1010. https://doi.org/10.1098/rspb.1997.0139CrossRefPubMedPubMedCentral

Panzer, S., Krueger, M., Muehlbauer, T., Kovacs, A. J., & Shea, C. H. (2009). Inter-manual transfer and practice: Coding of simple motor sequences. Acta Psychologica, 131(2), 99–109. https://doi.org/10.1016/j.actpsy.2009.03.004CrossRefPubMed

Paqueron, X., Leguen, M., Gentili, M. E., Riou, B., Coriat, P., & Willer, J. C. (2004). Influence of sensory and proprioceptive impairment on the development of phantom limb syndrome during regional anesthesia. Anesthesiology, 100(4), 979–986. https://doi.org/10.1097/00000542-200404000-00032CrossRefPubMed

Park, J. H., & Shea, C. H. (2002). Effector independence. Journal of Motor Behavior, 34(3). https://doi.org/10.1080/00222890209601944

Park, J. H., & Shea, C. H. (2005). Sequence learning: Response structure and effector transfer. The Quarterly Journal of Experimental Psychology Section A, 58(3). https://doi.org/10.1080/02724980343000918

Pipereit, K., Bock, O., & Vercher, J. L. (2006). The contribution of proprioceptive feedback to sensorimotor adaptation. Experimental Brain Research, 174(1), 45–52. https://doi.org/10.1007/s00221-006-0417-7CrossRefPubMed

Proske, U., & Gandevia, S. C. (2012). The proprioceptive senses: Their roles in signaling body shape, body position and movement, and muscle force. Physiological Reviews, 92(4), 1651–1697. https://doi.org/10.1152/physrev.00048.2011CrossRefPubMed

Redding, G. M., Rossetti, Y., & Wallace, B. (2005). Applications of prism adaptation: A tutorial in theory and method. Neuroscience and Biobehavioral Reviews, 29(3), 431–444. https://doi.org/10.1016/j.neubiorev.2004.12.004CrossRefPubMed

Redon, C., Hay, L., & Velay, J. L. (1991). Proprioceptive control of goal-directed movements in man, studied by means of vibratory muscle tendon stimulation. Journal of Motor Behavior, 23(2), 101–108. https://doi.org/10.1080/00222895.1991.9942027CrossRefPubMed

Robin, C., Toussaint, L., Blandin, Y., & Vinter, A. (2004). Sensory integration in the learning of aiming toward « self-defined » targets. Research Quarterly for Exercise and Sport, 75(4), 381–387. https://doi.org/10.1080/02701367.2004.10609171CrossRefPubMed

Roll, J. P., & Vedel, J. P. (1982). Kinaesthetic role of muscle afferents in man, studied by tendon vibration and microneurography. Experimental Brain Research, 47(2). https://doi.org/10.1007/BF00239377

Sainburg, R. L., Ghilardi, M. F., Poizner, H., & Ghez, C. (1995). Control of limb dynamics in normal subjects and patients without proprioception. Journal of Neurophysiology, 73(2). https://doi.org/10.1152/jn.1995.73.2.820

Sarlegna, F. R., & Sainburg, R. L. (2009). The roles of vision and proprioception in the planning of reaching movements. Advances in Experimental Medicine and Biology, 629, 317–335. https://doi.org/10.1007/978-0-387-77064-2_16CrossRefPubMedPubMedCentral

Sarlegna, F. R., Malfait, N., Bringoux, L., Bourdin, C., & Vercher, J. L. (2010). Force-field adaptation without proprioception: Can vision be used to model limb dynamics? Neuropsychologia, 48(1). https://doi.org/10.1016/j.neuropsychologia.2009.08.011

Scotto, C. R., Meugnot, A., Casiez, G., & Toussaint, L. (2020). Short-Term Sensorimotor Deprivation Impacts Feedforward and Feedback Processes of Motor Control. Frontiers in Neuroscience, 14. https://www.frontiersin.org/articles/https://doi.org/10.3389/fnins.2020.00696

Scotto, C. R., Petitcollin, F., Dupuy, O., Casiez, G., Dugué, B., & Toussaint, L. (2024). Arm cooling selectively impacts sensorimotor control. Journal of Neurophysiology, 131(4), 607–618. https://doi.org/10.1152/jn.00196.2023CrossRefPubMed

Shea, C. H., Kovacs, A. J., & Panzer, S. (2011). The coding and inter-manual transfer of movement sequences. Frontiers in Psychology, 2. https://doi.org/10.3389/fpsyg.2011.00052

Sigrist, R., Rauter, G., Riener, R., & Wolf, P. (2013). Augmented visual, auditory, haptic, and multimodal feedback in motor learning: A review. Psychonomic Bulletin & Review, 20(1), 21–53. https://doi.org/10.3758/s13423-012-0333-8CrossRef

Soderstrom, N. C., & Bjork, R. A. (2015). Learning Versus performance: An integrative review. Perspectives on Psychological Science, 10(2), 176–199. https://doi.org/10.1177/1745691615569000CrossRefPubMed

Toussaint, L., Meugnot, A., Badets, A., Chesnet, D., & Proteau, L. (2017). The specificity of practice hypothesis in goal-directed movements: Visual dominance or proprioception neglect? Psychological Research Psychologische Forschung, 81(2), 407–414. https://doi.org/10.1007/s00426-016-0748-3CrossRefPubMed

Touzalin-Chretien, P., Ehrler, S., & Dufour, A. (2010). Dominance of vision over proprioception on motor programming: Evidence from ERP. Cerebral Cortex (New York N Y : 1991), 20(8), Article8. https://doi.org/10.1093/cercor/bhp271CrossRef

Tremblay, L., & Proteau, L. (1998). Specificity of practice: The case of Powerlifting. Research Quarterly for Exercise and Sport, 69(3). https://doi.org/10.1080/02701367.1998.10607695

van Beers, R. J., Sittig, A. C., & van der Denier, J. J. (1996). How humans combine simultaneous proprioceptive and visual position information. Experimental Brain Research, 111(2), 253–261. https://doi.org/10.1007/BF00227302CrossRefPubMed

van Beers, R. J., Sittig, A. C., & Gon, J. J. (1999). Integration of proprioceptive and visual position-information: An experimentally supported model. Journal of Neurophysiology, 81(3), 1355–1364. https://doi.org/10.1152/jn.1999.81.3.1355CrossRefPubMed

van Beers, R. J., Wolpert, D. M., & Haggard, P. (2002). When feeling is more important than seeing in sensorimotor adaptation. Current Biology: CB, 12(10), 834–837. https://doi.org/10.1016/s0960-9822(02)00836-9CrossRefPubMed

Vidoni, E., & Boyd, L. (2008). Motor sequence learning occurs despite disrupted visual and proprioceptive feedback. Behavioral and Brain Functions: BBF, 4, 32. https://doi.org/10.1186/1744-9081-4-32CrossRefPubMedPubMedCentral

Vuillerme, N., Danion, F., Forestier, N., & Nougier, V. (2002). Postural sway under muscle vibration and muscle fatigue in humans. Neuroscience Letters, 333(2), 131–135. https://doi.org/10.1016/S0304-3940(02)00999-0CrossRefPubMed

Wali, M., Lee-Miller, T., Babu, R., & Block, H. J. (2023). Retention of visuo-proprioceptive recalibration in estimating hand position. Scientific Reports, 13(1), 6097. https://doi.org/10.1038/s41598-023-33290-0CrossRefPubMedPubMedCentral

Titel: Reliability of online visual and proprioceptive feedback: impact on learning and sensorimotor coding
Auteurs: Cécile R. Scotto
Marie Bernardo
Romain Tisserand
Géry Casiez
Yannick Blandin
Publicatiedatum: 01-02-2025
Uitgeverij: Springer Berlin Heidelberg
Gepubliceerd in: Psychological Research / Uitgave 1/2025
Print ISSN: 0340-0727
Elektronisch ISSN: 1430-2772
DOI: https://doi.org/10.1007/s00426-024-02041-9

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