Seeing the Errors You Feel Enhances Locomotor Performance but Not Learning.
In human motor learning, it is thought that the more information we have about our errors, the faster we learn. Here, we show that additional error information can lead to improved motor performance without any concomitant improvement in learning. We studied split-belt treadmill walking that drives people to learn a new gait pattern using sensory prediction errors detected by proprioceptive feedback. When we also provided visual error feedback, participants acquired the new walking pattern far more rapidly and showed accelerated restoration of the normal walking pattern during washout. However, when the visual error feedback was removed during either learning or washout, errors reappeared with performance immediately returning to the level expected based on proprioceptive learning alone. These findings support a model with two mechanisms: a dual-rate adaptation process that learns invariantly from sensory prediction error detected by proprioception and a visual-feedback-dependent process that monitors learning and corrects residual errors but shows no learning itself. We show that our voluntary correction model accurately predicted behavior in multiple situations where visual feedback was used to change acquisition of new walking patterns while the underlying learning was unaffected. The computational and behavioral framework proposed here suggests that parallel learning and error correction systems allow us to rapidly satisfy task demands without necessarily committing to learning, as the relative permanence of learning may be inappropriate or inefficient when facing environments that are liable to change.
Department of Neuroscience, The Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Center for Movement Studies, The Kennedy Krieger Institute, Baltimore, MD 21205, USA. Electronic address: rroemmi1@jhmi.edu.
Ryan T
RT
Roemmich
Center for Movement Studies, The Kennedy Krieger Institute, Baltimore, MD 21205, USA; Department of Biomedical Engineering, The Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Andrew W
AW
Long
Department of Neuroscience, The Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Center for Movement Studies, The Kennedy Krieger Institute, Baltimore, MD 21205, USA.
Amy J
AJ
Bastian
D000328:Adult; D056228:Feedback, Sensory; D005260:Female; D005684:Gait; D006801:Humans; D007858:Learning; D008297:Male; D009043:Motor Activity; D014785:Vision, Ocular; D014796:Visual Perception; D016138:Walking; D055815:Young Adult
adaptation; feedback; gait; locomotion; motor learning; split-belt treadmill; walking
J Neurophysiol. 2015 Jun 1;113(10):3905-14
25867742
J Neurosci. 2006 Sep 6;26(36):9107-16
16957067
J Neurosci. 2002 Feb 1;22(3):1108-13
11826139
J Neurophysiol. 2009 Aug;102(2):931-40
19494195
J Neurophysiol. 2005 Jun;93(6):3200-13
15659526
J Neurosci. 2006 Apr 5;26(14):3642-5
16597717
J Neurophysiol. 2014 Apr;111(7):1444-54
24431403
J Neurophysiol. 2016 Apr;115(4):2014-20
26864768
J Neurophysiol. 2007 Jul;98(1):54-62
17507504
PLoS Biol. 2006 Jun;4(6):e179
16700627
J Physiol. 2013 Feb 15;591(4):1081-95
23247109
Curr Biol. 2015 Sep 21;25(18):2452-6
26365256
J Neurophysiol. 2005 Oct;94(4):2403-15
15958603
Exp Brain Res. 1998 Jan;118(1):126-30
9547070
J Biomech. 2012 Nov 15;45(16):2817-21
22985473
J Neurophysiol. 2015 Dec;114(6):3255-67
26424576
Brain. 2009 Mar;132(Pt 3):722-33
19074191
J Neurophysiol. 2016 May 1;115(5):2341-8
26912598
J Neurosci. 2015 Jul 1;35(26):9568-79
26134640
J Neurosci. 2010 Dec 15;30(50):17015-22
21159971
J Neurophysiol. 2000 Oct;84(4):2175-80
11024106
J Appl Physiol (1985). 2011 Jun;110(6):1682-90
21393467
J Neurophysiol. 2015 Jun 1;113(10):3519-30
25855699
Curr Biol. 2014 May 19;24(10):1050-61
24794296
J Neurosci. 2011 Oct 19;31(42):15136-43
22016547
Brain. 1996 Aug;119 ( Pt 4):1199-211
8813283
Curr Opin Neurobiol. 2015 Aug;33:71-7
25827272
J Neurophysiol. 2010 Apr;103(4):1954-62
20147417
J Neurosci. 2014 Feb 19;34(8):3023-32
24553942
J Neurophysiol. 2016 May 1;115(5):2692-700
26961100
Phys Ther. 1991 Feb;71(2):140-9
1989009
J Neurophysiol. 2012 Jun;107(11):2950-7
22378177