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Multiple motor memories are learned to control different points on a tool

Abstract

Skilful object manipulation requires learning the dynamics of objects, linking applied force to motion1,2. This involves the formation of a motor memory3,4, which has been assumed to be associated with the object, independent of the point on the object that one chooses to control. Importantly, in manipulation tasks, different control points on an object, such as the rim of a cup when drinking or its base when setting it down, can be associated with distinct dynamics. Here, we show that opposing dynamic perturbations, which interfere when controlling a single location on an object, can be learned when each is associated with a separate control point. This demonstrates that motor memory formation is linked to control points on the object, rather than the object per se. We also show that the motor system only generates separate memories for different control points if they are linked to different dynamics, allowing efficient use of motor memory. To account for these results, we develop a normative switching state-space model of motor learning, in which the association between cues (control points) and contexts (dynamics) is learned rather than fixed. Our findings uncover an important mechanism through which the motor system generates flexible and dexterous behaviour.

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Fig. 1: Separate motor memories are formed for different control points.
Fig. 2: Control points are represented in an object-centred frame of reference.
Fig. 3: The encoding of dynamics for different control points depends on the fields experienced.
Fig. 4: Learning to associate contexts with cues in the SSSM.

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Acknowledgements

We thank G. Žalalytė and A. Pantelides for assistance with the experiments, and S. Singh for advice on the model. We thank the Wellcome Trust, Royal Society (Noreen Murray Professorship in Neurobiology to D.M.W.), Engineering and Physical Sciences Research Council and Canadian Institutes of Health Research for support. The funders had no role in the study design, data collection and analysis, decision to publish or preparation of the manuscript.

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All authors conceived and designed the experiments. J.B.H. performed the experiments, and developed and fit the SSSM. All authors wrote the paper, discussed the results and edited the manuscript.

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Correspondence to James B. Heald.

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Heald, J.B., Ingram, J.N., Flanagan, J.R. et al. Multiple motor memories are learned to control different points on a tool. Nat Hum Behav 2, 300–311 (2018). https://doi.org/10.1038/s41562-018-0324-5

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