Parallel specification of competing sensorimotor control policies for alternative action options

Nature Neuroscience

Volumn 19, Issue 2, 2016, Pages 320-326

  Gallivan, Jason P ^a,b   Logan, Lindsey ^a   Wolpert, Daniel M ^c   Flanagan, J Randall ^a,b  

^a QUEEN S UNIVERSITY   (Canada)

^b QUEEN S UNIVERSITY   (Canada)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; ELECTRIC POTENTIAL; ERROR; FEEDBACK SYSTEM; HUMAN; MOTOR SYSTEM; MOVEMENT (PHYSIOLOGY); NOISE; OBJECT RELATION; PRIORITY JOURNAL; SENSORIMOTOR CORTEX; SENSORIMOTOR FUNCTION; ADOLESCENT; ADVERSE EFFECTS; BRAIN; FEMALE; MALE; PHOTOSTIMULATION; PHYSIOLOGY; PSYCHOLOGICAL FEEDBACK; PSYCHOMOTOR PERFORMANCE; SENSATION; YOUNG ADULT;

ADOLESCENT; BRAIN; FEEDBACK, PSYCHOLOGICAL; FEMALE; HUMANS; MALE; MOVEMENT; NOISE; PHOTIC STIMULATION; PSYCHOMOTOR PERFORMANCE; SENSATION; YOUNG ADULT;

EID: 84956616996     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.4214     Document Type: Article

References (57)

1. Cisek, P. & Kalaska, J.F. Neural correlates of reaching decisions in dorsal premotor cortex: specification of multiple direction choices and final selection of action. Neuron 45, 801-814 (2005).
2. Thura, D. & Cisek, P. Deliberation and commitment in the premotor and primary motor cortex during dynamic decision making. Neuron 81, 1401-1416 (2014).
3. Cisek, P. Cortical mechanisms of action selection: the affordance competition hypothesis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 362, 1585-1599 (2007).
4. Baumann, M.A., Fluet, M.C. & Scherberger, H. Context-specific grasp movement representation in the macaque anterior intraparietal area. J. Neurosci. 29, 6436-6448 (2009).
5. McPeek, R.M., Han, J.H. & Keller, E.L. Competition between saccade goals in the superior colliculus produces saccade curvature. J. Neurophysiol. 89, 2577-2590 (2003).
6. Chapman, C.S. et al. Reaching for the unknown: multiple target encoding and real-time decision-making in a rapid reach task. Cognition 116, 168-176 (2010).
7. Ghez, C. et al. Discrete and continuous planning of hand movements and isometric force trajectories. Exp. Brain Res. 115, 217-233 (1997).
8. Van der Stigchel, S., Meeter, M. & Theeuwes, J. Eye movement trajectories and what they tell us. Neurosci. Biobehav. Rev. 30, 666-679 (2006).
9. Stewart, B.M., Gallivan, J.P., Baugh, L.A. & Flanagan, J.R. Motor, not visual, encoding of potential reach targets. Curr. Biol. 24, R953-R954 (2014).
10. Stewart, B.M., Baugh, L.A., Gallivan, J.P. & Flanagan, J.R. Simultaneous encoding of the direction and orientation of potential targets during reach planning: evidence of multiple competing reach plans. J. Neurophysiol. 110, 807-816 (2013).
11. Shadmehr, R., Smith, M.A. & Krakauer, J.W. Error correction, sensory prediction, and adaptation in motor control. Annu. Rev. Neurosci. 33, 89-108 (2010).
12. Wolpert, D.M., Diedrichsen, J. & Flanagan, J.R. Principles of sensorimotor learning. Nat. Rev. Neurosci. 12, 739-751 (2011).
13. Scott, S.H. Optimal feedback control and the neural basis of volitional motor control. Nat. Rev. Neurosci. 5, 532-546 (2004).
14. Todorov, E. & Jordan, M.I. Optimal feedback control as a theory of motor coordination. Nat. Neurosci. 5, 1226-1235 (2002).
15. Wolpert, D.M. & Flanagan, J.R. Motor learning. Curr. Biol. 20, R467-R472 (2010).
16. Todorov, E. Optimality principles in sensorimotor control. Nat. Neurosci. 7, 907-915 (2004).
17. Cluff, T. & Scott, S.H. Rapid feedback responses correlate with reach adaptation and properties of novel upper limb loads. J. Neurosci. 33, 15903-15914 (2013).
18. Franklin, S., Wolpert, D.M. & Franklin, D.W. Visuomotor feedback gains upregulate during the learning of novel dynamics. J. Neurophysiol. 108, 467-478 (2012).
19. Diedrichsen, J. Optimal task-dependent changes of bimanual feedback control and adaptation. Curr. Biol. 17, 1675-1679 (2007).
20. Dimitriou, M., Franklin, D.W. & Wolpert, D.M. Task-dependent coordination of rapid bimanual motor responses. J. Neurophysiol. 107, 890-901 (2012).
21. Pruszynski, J.A. et al. Primary motor cortex underlies multi-joint integration for fast feedback control. Nature 478, 387-390 (2011).
22. Franklin, D.W. & Wolpert, D.M. Specificity of reflex adaptation for task-relevant variability. J. Neurosci. 28, 14165-14175 (2008).
23. Nashed, J.Y., Crevecoeur, F. & Scott, S.H. Influence of the behavioral goal and environmental obstacles on rapid feedback responses. J. Neurophysiol. 108, 999-1009 (2012).
24. Knill, D.C., Bondada, A. & Chhabra, M. Flexible, task-dependent use of sensory feedback to control hand movements. J. Neurosci. 31, 1219-1237 (2011).
25. Dimitriou, M., Wolpert, D.M. & Franklin, D.W. The temporal evolution of feedback gains rapidly update to task demands. J. Neurosci. 33, 10898-10909 (2013).
26. Smith, M.A., Ghazizadeh, A. & Shadmehr, R. Interacting adaptive processes with different timescales underlie short-term motor learning. PLoS Biol. 4, e179 (2006).
27. Haith, A.M., Huberdeau, D.M. & Krakauer, J.W. Hedging your bets: intermediate movements as optimal behavior in the context of an incomplete decision. PLOS Comput. Biol. 11, e1004171 (2015).
28. Gallivan, J.P. et al. One to four, and nothing more: nonconscious parallel individuation of objects during action planning. Psychol. Sci. 22, 803-811 (2011).
29. Hudson, T.E., Maloney, L.T. & Landy, M.S. Movement planning with probabilistic target information. J. Neurophysiol. 98, 3034-3046 (2007).
30. Izawa, J. & Shadmehr, R. On-line processing of uncertain information in visuomotor control. J. Neurosci. 28, 11360-11368 (2008).
31. Gallivan, J.P., Barton, K.S., Chapman, C.S., Wolpert, D.M. & Randall Flanagan, J. Action plan co-optimization reveals the parallel encoding of competing reach movements. Nat. Commun. 6, 7428 (2015).
32. Corneil, B.D., Olivier, E. & Munoz, D.P. Visual responses on neck muscles reveal selective gating that prevents express saccades. Neuron 42, 831-841 (2004).
33. Saijo, N., Murakami, I., Nishida, S. & Gomi, H. Large-field visual motion directly induces an involuntary rapid manual following response. J. Neurosci. 25, 4941-4951 (2005).
34. Gomi, H., Abekawa, N. & Nishida, S. Spatiotemporal tuning of rapid interactions between visual-motion analysis and reaching movement. J. Neurosci. 26, 5301-5308 (2006).
35. Prablanc, C. & Martin, O. Automatic control during hand reaching at undetected two-dimensional target displacements. J. Neurophysiol. 67, 455-469 (1992).
36. Day, B.L. & Lyon, I.N. Voluntary modification of automatic arm movements evoked by motion of a visual target. Exp. Brain Res. 130, 159-168 (2000).
37. Saunders, J.A. & Knill, D.C. Visual feedback control of hand movements. J. Neurosci. 24, 3223-3234 (2004).
38. Brenner, E. & Smeets, J.B. Perceptual requirements for fast manual responses. Exp. Brain Res. 153, 246-252 (2003).
39. Goodale, M.A., Pelisson, D. & Prablanc, C. Large adjustments in visually guided reaching do not depend on vision of the hand or perception of target displacement. Nature 320, 748-750 (1986).
40. Körding, K.P. & Wolpert, D.M. Bayesian integration in sensorimotor learning. Nature 427, 244-247 (2004).
41. Braun, D.A., Aertsen, A., Wolpert, D.M. & Mehring, C. Learning optimal adaptation strategies in unpredictable motor tasks. J. Neurosci. 29, 6472-6478 (2009).
42. Orbán, G. & Wolpert, D.M. Representations of uncertainty in sensorimotor control. Curr. Opin. Neurobiol. 21, 629-635 (2011).
43. Franklin, D.W., Osu, R., Burdet, E., Kawato, M. & Milner, T.E. Adaptation to stable and unstable dynamics achieved by combined impedance control and inverse dynamics model. J. Neurophysiol. 90, 3270-3282 (2003).
44. Crevecoeur, F., McIntyre, J., Thonnard, J.L. & Lefèvre, P. Movement stability under uncertain internal models of dynamics. J. Neurophysiol. 104, 1301-1313 (2010).
45. Munoz, D.P. & Wurtz, R.H. Saccade-related activity in monkey superior colliculus. II. Spread of activity during saccades. J. Neurophysiol. 73, 2334-2348 (1995).
46. Song, J.H. & Nakayama, K. Hidden cognitive states revealed in choice reaching tasks. Trends Cogn. Sci. 13, 360-366 (2009).
47. Gallivan, J.P. & Chapman, C.S. Three-dimensional reach trajectories as a probe of real-time decision-making between multiple competing targets. Front. Neurosci. 8, 215 (2014).
48. Churchland, M.M., Santhanam, G. & Shenoy, K.V. Preparatory activity in premotor and motor cortex reflects the speed of the upcoming reach. J. Neurophysiol. 96, 3130-3146 (2006).
49. Manohar, S.G. et al. Reward Pays the Cost of Noise Reduction in Motor and Cognitive Control. Curr. Biol. 25, 1707-1716 (2015).
50. Christopoulos, V. & Schrater, P.R. Dynamic Integration of Value Information into a Common Probability Currency as a Theory for Flexible Decision Making. PLOS Comput. Biol. 11, e1004402 (2015).
51. Howard, I.S., Ingram, J.N. & Wolpert, D.M. A modular planar robotic manipulandum with end-point torque control. J. Neurosci. Methods 181, 199-211 (2009).
52. Liu, D. & Todorov, E. Evidence for the flexible sensorimotor strategies predicted by optimal feedback control. J. Neurosci. 27, 9354-9368 (2007).
53. Ingram, J.N., Flanagan, J.R. & Wolpert, D.M. Context-dependent decay of motor memories during skill acquisition. Curr. Biol. 23, 1107-1112 (2013).
54. Huang, V.S., Haith, A., Mazzoni, P. & Krakauer, J.W. Rethinking motor learning and savings in adaptation paradigms: model-free memory for successful actions combines with internal models. Neuron 70, 787-801 (2011).
55. Galea, J.M., Mallia, E., Rothwell, J. & Diedrichsen, J. The dissociable effects of punishment and reward on motor learning. Nat. Neurosci. 18, 597-602 (2015).
56. Baugh, L.A., Kao, M., Johansson, R.S. & Flanagan, J.R. Material evidence: interaction of well-learned priors and sensorimotor memory when lifting objects. J. Neurophysiol. 108, 1262-1269 (2012).
57. Ingram, J.N., Howard, I.S., Flanagan, J.R. & Wolpert, D.M. Multiple grasp-specific representations of tool dynamics mediate skillful manipulation. Curr. Biol. 20, 618-623 (2010).