Abstract
The motor system shows a remarkable capacity to generalize learned behavior to new contexts while simultaneously permitting learning of multiple and sometimes conflicting skills. To examine the influence of proprioceptive state on this capacity, we compared the effectiveness of changes in workspace location and limb orientation (horizontal vs. parasagittal plane posture) in facilitating learning of opposing dynamic force-field perturbations. When opposing fields were encountered in similar workspace positions and limb orientations, subjects failed to learn the two tasks. In contrast, differences in initial limb proprioceptive state were sufficient for significant learning to take place. The extent of learning was similar when the two fields were encountered in different arm orientations in a similar workspace location as compared to when learning took place in spatially separated workspace locations, consistent with the generalization of learning mainly in intrinsic joint coordinates. In keeping with these observations, examination of how trial-to-trial adaptation generalized showed that generalization tended to be greater across similar limb postures. However, when the two fields were encountered in distinct spatial locations, the extent of generalization of adaptation to one field depended on the limb orientation in which the other field was encountered. These results suggest that three-dimensional proprioceptive limb state plays an important role in modulating generalization patterns so as to permit the best compromise between broad generalization and the simultaneous learning of conflicting skills.
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References
Addou T, Krouchev N, Kalaska JF (2011) Colored context cues can facilitate the ability to learn and to switch between multiple dynamical force fields. J Neurophysiol 106:163–183
Andersen RA, Essick GK, Siegel RM (1985) Encoding of spatial location by posterior parietal neurons. Science 230:456–458
Andersen RA, Bracewell RM, Barash S, Gnadt JW, Fogassi L (1990) Eye position effects on visual, memory, and saccade-related activity in areas LIP and 7a of macaque. J Neurosci 10:1176–1196
Arce F, Novick I, Mandelblat-Cerf Y, Israel Z, Ghez C, Vaadia E (2010a) Combined adaptiveness of specific motor cortical ensembles underlies learning. J Neurosci 30:5415–5425
Arce F, Novick I, Mandelblat-Cerf Y, Vaadia E (2010b) Neuronal correlates of memory formation in motor cortex after adaptation to force field. J Neurosci 30:9189–9198
Berniker M, Franklin DW, Flanagan JR, Wolpert DM, Kording K (2014) Motor learning of novel dynamics is not represented in a single global coordinate system: evaluation of mixed coordinate representations and local learning. J Neurophysiol 111:1165–1182
Brashers-Krug T, Shadmehr R, Bizzi E (1996) Consolidation in human motor memory. Nature 382:252–255
Brayanov JB, Press DZ, Smith MA (2012) Motor memory is encoded as a gain-field combination of intrinsic and extrinsic action representations. J Neurosci 32:14951–14965
Caithness G, Osu R, Bays P et al (2004) Failure to consolidate the consolidation theory of learning for sensorimotor adaptation tasks. J Neurosci 24:8662–8671
Caminiti R, Johnson PB, Urbano A (1990) Making arm movements within different parts of space: dynamic aspects in the primate motor cortex. J Neurosci 10:2039–2058
Castro LN, Wu HG, Smith MA (2011) Adaptation to dynamic environments displays local generalization for voluntary reaching movements. In: Conference proceedings of the IEEE engineering in medicine and biology society, pp 4050–4052
Cherian A, Fernandes HL, Miller LE (2013) Primary motor cortical discharge during force field adaptation reflects muscle-like dynamics. J Neurophysiol 110:768–783
Conditt MA, Gandolfo F, Mussa-Ivaldi FA (1997) The motor system does not learn the dynamics of the arm by rote memorization of past experience. J Neurophysiol 78:554–560
Criscimagna-Hemminger SE, Donchin O, Gazzaniga MS, Shadmehr R (2003) Learned dynamics of reaching movements generalize from dominant to nondominant arm. J Neurophysiol 89:168–176
Donchin O, Francis JT, Shadmehr R (2003) Quantifying generalization from trial-by-trial behavior of adaptive systems that learn with basis functions: theory and experiments in human motor control. J Neurosci 23:9032–9045
Gandolfo F, Mussa-Ivaldi FA, Bizzi E (1996) Motor learning by field approximation. Proc Natl Acad Sci USA 93:3843–3846
Gandolfo F, Li C, Benda BJ, Schioppa CP, Bizzi E (2000) Cortical correlates of learning in monkeys adapting to a new dynamical environment. Proc Natl Acad Sci USA 97:2259–2263
Georgopoulos AP, Kalaska JF, Caminiti R, Massey JT (1982) On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex. J Neurosci 2:1527–1537
Georgopoulos AP, Caminiti R, Kalaska JF (1984) Static spatial effects in motor cortex and area 5: quantitative relations in a two-dimensional space. Exp Brain Res 54:446–454
Green AM, Labelle J-P, Shadmehr R, Kalaska JF (2006) The influence of proprioceptive state on learning control of reach dynamics. In: Society for neuroscience meeting, vol Program No. 57.23. Neuroscience Meeting Planner, Atlanta, GA
Hirashima M, Nozaki D (2012) Distinct motor plans form and retrieve distinct motor memories for physically identical movements. Curr Biol 22:432–436
Howard IS, Ingram JN, Wolpert DM (2010) Context-dependent partitioning of motor learning in bimanual movements. J Neurophysiol 104:2082–2091
Howard IS, Wolpert DM, Franklin DW (2013) The effect of contextual cues on the encoding of motor memories. J Neurophysiol 109:2632–2644
Hwang EJ, Shadmehr R (2005) Internal models of limb dynamics and the encoding of limb state. J Neural Eng 2:S266–S278
Hwang EJ, Donchin O, Smith MA, Shadmehr R (2003) A gain-field encoding of limb position and velocity in the internal model of arm dynamics. PLoS Biol 1:E25
Hwang EJ, Smith MA, Shadmehr R (2006) Dissociable effects of the implicit and explicit memory systems on learning control of reaching. Exp Brain Res 173:425–437
Kakei S, Hoffman DS, Strick PL (1999) Muscle and movement representations in the primary motor cortex. Science 285:2136–2139
Kalaska JF (2009) From intention to action: motor cortex and the control of reaching movements. Adv Exp Med Biol 629:139–178
Kalaska JF, Cohen DA, Hyde ML, Prud’homme M (1989) A comparison of movement direction-related versus load direction-related activity in primate motor cortex, using a two-dimensional reaching task. J Neurosci 9:2080–2102
Karniel A, Mussa-Ivaldi FA (2002) Does the motor control system use multiple models and context switching to cope with a variable environment? Exp Brain Res 143:520–524
Krakauer JW, Ghilardi MF, Ghez C (1999) Independent learning of internal models for kinematic and dynamic control of reaching. Nat Neurosci 2:1026–1031
Lackner JR, Dizio P (1994) Rapid adaptation to Coriolis force perturbations of arm trajectory. J Neurophysiol 72:299–313
Li CS, Padoa-Schioppa C, Bizzi E (2001) Neuronal correlates of motor performance and motor learning in the primary motor cortex of monkeys adapting to an external force field. Neuron 30:593–607
Malfait N, Ostry DJ (2004) Is interlimb transfer of force-field adaptation a cognitive response to the sudden introduction of load? J Neurosci 24:8084–8089
Malfait N, Shiller DM, Ostry DJ (2002) Transfer of motor learning across arm configurations. J Neurosci 22:9656–9660
Malfait N, Gribble PL, Ostry DJ (2005) Generalization of motor learning based on multiple field exposures and local adaptation. J Neurophysiol 93:3327–3338
Mussa-Ivaldi FA, Giszter SF (1992) Vector field approximation: a computational paradigm for motor control and learning. Biol Cybern 67:491–500
Nozaki D, Kurtzer I, Scott SH (2006) Limited transfer of learning between unimanual and bimanual skills within the same limb. Nat Neurosci 9:1364–1366
Poggio T, Bizzi E (2004) Generalization in vision and motor control. Nature 431:768–774
Pouget A, Snyder LH (2000) Computational approaches to sensorimotor transformations. Nat Neurosci 3(Suppl):1192–1198
Scott SH, Kalaska JF (1997) Reaching movements with similar hand paths but different arm orientations. I. Activity of individual cells in motor cortex. J Neurophysiol 77:826–852
Sergio LE, Kalaska JF (2003) Systematic changes in motor cortex cell activity with arm posture during directional isometric force generation. J Neurophysiol 89:212–228
Sergio LE, Hamel-Paquet C, Kalaska JF (2005) Motor cortex neural correlates of output kinematics and kinetics during isometric-force and arm-reaching tasks. J Neurophysiol 94:2353–2378
Shadmehr R (2004) Generalization as a behavioral window to the neural mechanisms of learning internal models. Hum Mov Sci 23:543–568
Shadmehr R, Moussavi ZM (2000) Spatial generalization from learning dynamics of reaching movements. J Neurosci 20:7807–7815
Shadmehr R, Mussa-Ivaldi FA (1994) Adaptive representation of dynamics during learning of a motor task. J Neurosci 14:3208–3224
Shadmehr R, Smith MA, Krakauer JW (2010) Error correction, sensory prediction, and adaptation in motor control. Annu Rev Neurosci 33:89–108
Sing GC, Joiner WM, Nanayakkara T, Brayanov JB, Smith MA (2009) Primitives for motor adaptation reflect correlated neural tuning to position and velocity. Neuron 64:575–589
Soechting JF, Buneo CA, Herrmann U, Flanders M (1995) Moving effortlessly in three dimensions: does Donders’ law apply to arm movement? J Neurosci 15:6271–6280
Thoroughman KA, Shadmehr R (2000) Learning of action through adaptive combination of motor primitives. Nature 407:742–747
Thoroughman KA, Taylor JA (2005) Rapid reshaping of human motor generalization. J Neurosci 25:8948–8953
Trumbower RD, Krutky MA, Yang BS, Perreault EJ (2009) Use of self-selected postures to regulate multi-joint stiffness during unconstrained tasks. PLoS One 4:e5411. doi:10.1371/journal.pone.0005411
Verstynen T, Sabes PN (2011) How each movement changes the next: an experimental and theoretical study of fast adaptive priors in reaching. J Neurosci 31:10050–10059
Wolpert DM, Diedrichsen J, Flanagan JR (2011) Principles of sensorimotor learning. Nat Rev Neurosci 12:739–751
Wu W, Hatsopoulos N (2006) Evidence against a single coordinate system representation in the motor cortex. Exp Brain Res 175:197–210
Yokoi A, Hirashima M, Nozaki D (2011) Gain field encoding of the kinematics of both arms in the internal model enables flexible bimanual action. J Neurosci 31:17058–17068
Zhang K, Sejnowski TJ (1999) A theory of geometric constraints on neural activity for natural three-dimensional movement. J Neurosci 19:3122–3145
Acknowledgments
We thank J. Kalaska and P. Cisek for comments on the manuscript and R. Shadmehr for helpful discussions. This work was supported by operating grants from the Canadian Institutes for Health Research (MOP 84454) and the National Institutes of Health Research (R01 NS046033).
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Green, A.M., Labelle, JP. The influence of proprioceptive state on learning control of reach dynamics. Exp Brain Res 233, 2961–2975 (2015). https://doi.org/10.1007/s00221-015-4366-x
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DOI: https://doi.org/10.1007/s00221-015-4366-x