Temporal structure of motor variability is dynamically regulated and predicts motor learning ability

被引:463
作者
Wu, Howard G. [1 ]
Miyamoto, Yohsuke R. [1 ]
Castro, Luis Nicolas Gonzalez [1 ]
Oelveczky, Bence P. [2 ,3 ]
Smith, Maurice A. [1 ,3 ]
机构
[1] Harvard Univ, Sch Engn & Appl Sci, Cambridge, MA 02138 USA
[2] Harvard Univ, Dept Organism & Evolutionary Biol, Cambridge, MA 02138 USA
[3] Harvard Univ, Ctr Brain Sci, Cambridge, MA 02138 USA
关键词
GANGLIA-FOREBRAIN CIRCUIT; SIGNAL-DEPENDENT NOISE; BASAL GANGLIA; INDIVIDUAL-DIFFERENCES; ADAPTATION; MODULATION; MODEL; TIME; UNCERTAINTY; PRIMITIVES;
D O I
10.1038/nn.3616
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
Individual differences in motor learning ability are widely acknowledged, yet little is known about the factors that underlie them. Here we explore whether movement-to-movement variability in motor output, a ubiquitous if often unwanted characteristic of motor performance, predicts motor learning ability. Surprisingly, we found that higher levels of task-relevant motor variability predicted faster learning both across individuals and across tasks in two different paradigms, one relying on reward-based learning to shape specific arm movement trajectories and the other relying on error-based learning to adapt movements in novel physical environments. We proceeded to show that training can reshape the temporal structure of motor variability, aligning it with the trained task to improve learning. These results provide experimental support for the importance of action exploration, a key idea from reinforcement learning theory, showing that motor variability facilitates motor learning in humans and that our nervous systems actively regulate it to improve learning.
引用
收藏
页码:312 / 321
页数:10
相关论文
共 50 条
[1]   The Basal Ganglia Is Necessary for Learning Spectral, but Not Temporal, Features of Birdsong [J].
Ali, Farhan ;
Otchy, Timothy M. ;
Pehlevan, Cengiz ;
Fantana, Antoniu L. ;
Burak, Yoram ;
Oelveczky, Bence P. .
NEURON, 2013, 80 (02) :494-506
[2]   A basal ganglia-forebrain circuit in the songbird biases motor output to avoid vocal errors [J].
Andalman, Aaron S. ;
Fee, Michale S. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2009, 106 (30) :12518-12523
[3]  
[Anonymous], 2020, Reinforcement Learning, An Introduction
[4]   Interference between velocity-dependent and position-dependent force-fields indicates that tasks depending on different kinematic parameters compete for motor working memory [J].
Bays, PM ;
Flanagan, JR ;
Wolpert, DM .
EXPERIMENTAL BRAIN RESEARCH, 2005, 163 (03) :400-405
[5]   PREDICTION OF LEARNING RATE FROM HIPPOCAMPAL ELECTROENCEPHALOGRAM [J].
BERRY, SD ;
THOMPSON, RF .
SCIENCE, 1978, 200 (4347) :1298-1300
[6]   Covert skill learning in a cortical-basal ganglia circuit [J].
Charlesworth, Jonathan D. ;
Warren, Timothy L. ;
Brainard, Michael S. .
NATURE, 2012, 486 (7402) :251-+
[7]   A central source of movement variability [J].
Churchland, Mark M. ;
Afshar, Afsheen ;
Shenoy, Krishna V. .
NEURON, 2006, 52 (06) :1085-1096
[8]   Central representation of time during motor learning [J].
Conditt, MA ;
Mussa-Ivaldi, FA .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 1999, 96 (20) :11625-11630
[9]   Uncertainty-based competition between prefrontal and dorsolateral striatal systems for behavioral control [J].
Daw, ND ;
Niv, Y ;
Dayan, P .
NATURE NEUROSCIENCE, 2005, 8 (12) :1704-1711
[10]   The Rate of Visuomotor Adaptation Correlates with Cerebellar White-Matter Microstructure [J].
Della-Maggiore, Valeria ;
Scholz, Jan ;
Johansen-Berg, Heidi ;
Paus, Tomas .
HUMAN BRAIN MAPPING, 2009, 30 (12) :4048-4053