The dissociable effects of punishment and reward on motor learning

被引:230
作者
Galea, Joseph M. [1 ]
Mallia, Elizabeth [2 ]
Rothwell, John [2 ]
Diedrichsen, Joern [3 ]
机构
[1] Univ Birmingham, Sch Psychol, Birmingham B15 2TT, W Midlands, England
[2] UCL, Inst Neurol, Sobell Dept Motor Neurosci & Movement Disorders, London, England
[3] UCL, Insititute Cognit Neurosci, London, England
关键词
VISUOMOTOR ROTATION; SKILL ACQUISITION; PROSPECT-THEORY; BASAL GANGLIA; CORTEX; ADAPTATION; CEREBELLUM; DOPAMINE; REINFORCEMENT; SEROTONIN;
D O I
10.1038/nn.3956
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
A common assumption regarding error-based motor learning (motor adaptation) in humans is that its underlying mechanism is automatic and insensitive to reward- or punishment-based feedback. Contrary to this hypothesis, we show in a double dissociation that the two have independent effects on the learning and retention components of motor adaptation. Negative feedback, whether graded or binary, accelerated learning. While it was not necessary for the negative feedback to be coupled to monetary loss, it had to be clearly related to the actual performance on the preceding movement. Positive feedback did not speed up learning, but it increased retention of the motor memory when performance feedback was withdrawn. These findings reinforce the view that independent mechanisms underpin learning and retention in motor adaptation, reject the assumption that motor adaptation is independent of motivational feedback, and raise new questions regarding the neural basis of negative and positive motivational feedback in motor learning.
引用
收藏
页码:597 / +
页数:8
相关论文
共 53 条
  • [1] Reward Improves Long-Term Retention of a Motor Memory through Induction of Offline Memory Gains
    Abe, Mitsunari
    Schambra, Heidi
    Wassermann, Eric M.
    Luckenbaugh, Dave
    Schweighofer, Nicolas
    Cohen, Leonardo G.
    [J]. CURRENT BIOLOGY, 2011, 21 (07) : 557 - 562
  • [2] Local application of dopamine inhibits pyramidal tract neuron activity in the rodent motor cortex
    Awenowicz, PW
    Porter, LL
    [J]. JOURNAL OF NEUROPHYSIOLOGY, 2002, 88 (06) : 3439 - 3451
  • [3] Dopamine Modulates Reward-Related Vigor
    Beierholm, Ulrik
    Guitart-Masip, Marc
    Economides, Marcos
    Chowdhury, Rumana
    Duezel, Emrah
    Dolan, Ray
    Dayan, Peter
    [J]. NEUROPSYCHOPHARMACOLOGY, 2013, 38 (08) : 1495 - 1503
  • [4] Opponent interactions between serotonin and dopamine
    Daw, ND
    Kakade, S
    Dayan, P
    [J]. NEURAL NETWORKS, 2002, 15 (4-6) : 603 - 616
  • [5] Stochastic reinforcement benefits skill acquisition
    Dayan, Eran
    Averbeck, Bruno B.
    Richmond, Barry J.
    Cohen, Leonardo G.
    [J]. LEARNING & MEMORY, 2014, 21 (03) : 140 - 142
  • [6] Decision theory, reinforcement learning, and the brain
    Dayan, Peter
    Daw, Nathaniel D.
    [J]. COGNITIVE AFFECTIVE & BEHAVIORAL NEUROSCIENCE, 2008, 8 (04) : 429 - 453
  • [7] Amygdala damage eliminates monetary loss aversion
    De Martino, Benedetto
    Camerer, Colin F.
    Adolphs, Ralph
    [J]. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2010, 107 (08) : 3788 - 3792
  • [8] Contributions of the Motor Cortex to Adaptive Control of Reaching Depend on the Perturbation Schedule
    de Xivry, Jean-Jacques Orban
    Criscimagna-Hemminger, Sarah E.
    Shadmehr, Reza
    [J]. CEREBRAL CORTEX, 2011, 21 (07) : 1475 - 1484
  • [9] Dissociable Effects of Dopamine and Serotonin on Reversal Learning
    den Ouden, Hanneke E. M.
    Daw, Nathaniel D.
    Fernandez, Guillen
    Elshout, Joris A.
    Rijpkema, Mark
    Hoogman, Martine
    Franke, Barbara
    Cools, Roshan
    [J]. NEURON, 2013, 80 (04) : 1090 - 1100
  • [10] Neural correlates of reach errors
    Diedrichsen, J
    Hashambhoy, Y
    Rane, T
    Shadmehr, R
    [J]. JOURNAL OF NEUROSCIENCE, 2005, 25 (43) : 9919 - 9931