Force field generalization and the internal representation of motor learning
Autoři:
Alireza Rezazadeh aff001; Max Berniker aff001
Působiště autorů:
Department of Mechanical and Industrial Engineering, University of Illinois at Chicago, Chicago, IL, United States of America
aff001
Vyšlo v časopise:
PLoS ONE 14(11)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0225002
Souhrn
When learning a new motor behavior, e.g. reaching in a force field, the nervous system builds an internal representation. Examining how subsequent reaches in unpracticed directions generalize reveals this representation. Although often studied, it is not known how this representation changes across training directions, or how changes in reach direction and the corresponding changes in limb impedance, influence these measurements. We ran a force field adaptation experiment using eight groups of subjects each trained on one of eight standard directions and then tested for generalization in the remaining seven directions. Generalization in all directions was local and asymmetric, providing limited and unequal transfer to the left and right side of the trained target. These asymmetries were not consistent in either magnitude or direction, even after correcting for changes in limb impedance. Relying on a standard model for generalization the inferred representations inconsistently shifted to one side or the other of their respective training direction. A second model that accounted for limb impedance and variations in baseline trajectories explained more data and the inferred representations were centered on their respective training directions. Our results highlight the influence of limb mechanics and impedance on psychophysical measurements and their interpretations for motor learning.
Klíčová slova:
Learning – Body limbs – Learning curves – Stiffness – Engines – Robots – Perceptual learning
Zdroje
1. Wolpert DM, Ghahramani Z, Jordan MI. An internal model for sensorimotor integration. Science. 1995;269(5232):1880–2. doi: 10.1126/science.7569931 7569931
2. Conditt MA, Gandolfo F, Mussa-Ivaldi FA. The motor system does not learn the dynamics of the arm by rote memorization of past experience. Journal of Neurophysiology. 1997;78(1):554–60. doi: 10.1152/jn.1997.78.1.554 9242306
3. Shadmehr R, Mussa-Ivaldi FA. Adaptive representation of dynamics during learning of a motor task. Journal of Neuroscience. 1994;14(5):3208–24.
4. Thoroughman KA, Shadmehr R. Learning of action through adaptive combination of motor primitives. Nature. 2000;407(6805):742. doi: 10.1038/35037588 11048720
5. Donchin O, Francis JT, Shadmehr R. Quantifying generalization from trial-by-trial behavior of adaptive systems that learn with basis functions: theory and experiments in human motor control. Journal of Neuroscience. 2003;23(27):9032–45. doi: 10.1523/JNEUROSCI.23-27-09032.2003 14534237
6. Mattar AA, Ostry DJ. Modifiability of generalization in dynamics learning. J Neurophysiol. 2007;98(6):3321–9. Epub 2007/10/12. doi: 10.1152/jn.00576.2007 17928561.
7. Darainy M, Mattar AA, Ostry DJ. Effects of human arm impedance on dynamics learning and generalization. J Neurophysiol. 2009;101(6):3158–68. Epub 2009/04/10. doi: 10.1152/jn.91336.2008 19357340; PubMed Central PMCID: PMCPMC2694125.
8. Castro LNG, Wu HG, Smith MA, editors. Adaptation to dynamic environments displays local generalization for voluntary reaching movements. 2011 Annual International Conference of the IEEE Engineering in Medicine and Biology Society; 2011 30 Aug.-3 Sept. 2011.
9. Hwang EJ, Smith MA, Shadmehr R. Adaptation and generalization in acceleration-dependent force fields. Experimental brain research. 2006;169(4):496. doi: 10.1007/s00221-005-0163-2 16292640
10. Gonzalez Castro LN, Monsen CB, Smith MA. The binding of learning to action in motor adaptation. PLoS Comput Biol. 2011;7(6):e1002052. Epub 2011/07/07. doi: 10.1371/journal.pcbi.1002052 21731476; PubMed Central PMCID: PMCPMC3121685.
11. Krakauer JW, Pine ZM, Ghilardi M-F, Ghez C. Learning of visuomotor transformations for vectorial planning of reaching trajectories. Journal of Neuroscience. 2000;20(23):8916–24. doi: 10.1523/JNEUROSCI.20-23-08916.2000 11102502
12. Taylor JA, Krakauer JW, Ivry RB. Explicit and implicit contributions to learning in a sensorimotor adaptation task. Journal of Neuroscience. 2014;34(8):3023–32. doi: 10.1523/JNEUROSCI.3619-13.2014 24553942
13. Gandolfo F, Mussa-Ivaldi F, Bizzi E. Motor learning by field approximation. Proceedings of the National Academy of Sciences. 1996;93(9):3843–6.
14. Huang VS, Shadmehr R. Evolution of motor memory during the seconds after observation of motor error. Journal of neurophysiology. 2007;97(6):3976–85. doi: 10.1152/jn.01281.2006 17428900
15. Thoroughman KA, Taylor JA. Rapid reshaping of human motor generalization. Journal of Neuroscience. 2005;25(39):8948–53. doi: 10.1523/JNEUROSCI.1771-05.2005 16192385
16. Burdet E, Osu R, Franklin DW, Milner TE, Kawato M. The central nervous system stabilizes unstable dynamics by learning optimal impedance. Nature. 2001;414(6862):446. doi: 10.1038/35106566 11719805
17. Franklin DW, Osu R, Burdet E, Kawato M, Milner TE. Adaptation to stable and unstable dynamics achieved by combined impedance control and inverse dynamics model. Journal of neurophysiology. 2003;90(5):3270–82. doi: 10.1152/jn.01112.2002 14615432
18. Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971;9(1):97–113. doi: 10.1016/0028-3932(71)90067-4 5146491
19. Scheidt RA, Reinkensmeyer DJ, Conditt MA, Rymer WZ, Mussa-Ivaldi FA. Persistence of motor adaptation during constrained, multi-joint, arm movements. Journal of Neurophysiology. 2000;84(2):853–62. doi: 10.1152/jn.2000.84.2.853 10938312
20. Berniker M, Kording K. Estimating the sources of motor errors for adaptation and generalization. Nature neuroscience. 2008;11(12):1454. doi: 10.1038/nn.2229 19011624
21. Shadmehr R. Generalization as a behavioral window to the neural mechanisms of learning internal models. Human movement science. 2004;23(5):543–68. doi: 10.1016/j.humov.2004.04.003 15589621
22. Flash T. The control of hand equilibrium trajectories in multi-joint arm movements. Biological cybernetics. 1987;57(4–5):257–74. doi: 10.1007/bf00338819 3689835
23. Wolpert DM, Ghahramani Z. Computational principles of movement neuroscience. Nature neuroscience. 2000;3(11s):1212.
24. Shadmehr R, Smith MA, Krakauer JW. Error correction, sensory prediction, and adaptation in motor control. Annual review of neuroscience. 2010;33:89–108. doi: 10.1146/annurev-neuro-060909-153135 20367317
25. Smith MA, Ghazizadeh A, Shadmehr R. Interacting adaptive processes with different timescales underlie short-term motor learning. PLoS biology. 2006;4(6):e179. doi: 10.1371/journal.pbio.0040179 16700627
26. Zwislocki J, Maire F, Feldman A, Rubin H. On the effect of practice and motivation on the threshold of audibility. The Journal of the Acoustical Society of America. 1958;30(4):254–62.
27. Fitzgerald MB, Wright BA. Perceptual learning and generalization resulting from training on an auditory amplitude-modulation detection task. The Journal of the Acoustical Society of America. 2011;129(2):898–906. doi: 10.1121/1.3531841 21361447
28. Demany L, Semal C. Learning to perceive pitch differences. The Journal of the Acoustical Society of America. 2002;111(3):1377–88. doi: 10.1121/1.1445791 11931315
29. Wright BA, Buonomano DV, Mahncke HW, Merzenich MM. Learning and generalization of auditory temporal–interval discrimination in humans. Journal of Neuroscience. 1997;17(10):3956–63. doi: 10.1523/JNEUROSCI.17-10-03956.1997 9133413
30. Karmarkar UR, Buonomano DV. Temporal specificity of perceptual learning in an auditory discrimination task. Learning & Memory. 2003;10(2):141–7.
31. Linster C, Smith BH. Generalization between binary odor mixtures and their components in the rat. Physiology & behavior. 1999;66(4):701–7.
32. Linster C, Garcia PA, Hasselmo ME, Baxter MG. Selective loss of cholinergic neurons projecting to the olfactory system increases perceptual generalization between similar, but not dissimilar, odorants. Behavioral neuroscience. 2001;115(4):826. doi: 10.1037//0735-7044.115.4.826 11508721
33. Nagarajan SS, Blake DT, Wright BA, Byl N, Merzenich MM. Practice-related improvements in somatosensory interval discrimination are temporally specific but generalize across skin location, hemisphere, and modality. Journal of Neuroscience. 1998;18(4):1559–70. doi: 10.1523/JNEUROSCI.18-04-01559.1998 9454861
34. Sathian K, Zangaladze A, Green J, Vitek J, DeLong M. Tactile spatial acuity and roughness discrimination: impairments due to aging and Parkinson's disease. Neurology. 1997;49(1):168–77. doi: 10.1212/wnl.49.1.168 9222186
35. Sathian K, Zangaladze A. Tactile learning is task specific but transfers between fingers. Perception & Psychophysics. 1997;59(1):119–28.
36. Harrar V, Spence C, Makin TR. Topographic generalization of tactile perceptual learning. Journal of Experimental Psychology: Human Perception and Performance. 2014;40(1):15. doi: 10.1037/a0033200 23855526
37. Karni A, Sagi D. Where practice makes perfect in texture discrimination: evidence for primary visual cortex plasticity. Proceedings of the National Academy of Sciences. 1991;88(11):4966–70.
38. Schoups AA, Vogels R, Orban GA. Human perceptual learning in identifying the oblique orientation: retinotopy, orientation specificity and monocularity. The Journal of physiology. 1995;483(3):797–810.
39. Poggio T, Fahle M, Edelman S. Fast perceptual learning in visual hyperacuity. Science. 1992;256(5059):1018–21. doi: 10.1126/science.1589770 1589770
40. Fiorentini A, Berardi N. Learning in grating waveform discrimination: Specificity for orientation and spatial frequency. Vision research. 1981;21(7):1149–58. doi: 10.1016/0042-6989(81)90017-1 7314493
41. Sowden PT, Rose D, Davies IR. Perceptual learning of luminance contrast detection: Specific for spatial frequency and retinal location but not orientation. Vision research. 2002;42(10):1249–58. doi: 10.1016/s0042-6989(02)00019-6 12044757
Článok vyšiel v časopise
PLOS One
2019 Číslo 11
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Je Fuchsova endotelová dystrofie rohovky neurodegenerativní onemocnění?
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- A daily diary study on maladaptive daydreaming, mind wandering, and sleep disturbances: Examining within-person and between-persons relations
- A 3’ UTR SNP rs885863, a cis-eQTL for the circadian gene VIPR2 and lincRNA 689, is associated with opioid addiction
- A substitution mutation in a conserved domain of mammalian acetate-dependent acetyl CoA synthetase 2 results in destabilized protein and impaired HIF-2 signaling
- Molecular validation of clinical Pantoea isolates identified by MALDI-TOF