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Research Articles, Behavioral/Cognitive

Fast Feedback Responses to Categorical Sensorimotor Errors That Do Not Indicate Error Magnitude Are Optimized Based on Short- and Long-Term Memory

Michael R. McGarity-Shipley, Simona Markovik Jantz, Roland S. Johansson, Daniel M. Wolpert and J. Randall Flanagan
Journal of Neuroscience 6 December 2023, 43 (49) 8525-8535; https://doi.org/10.1523/JNEUROSCI.1990-22.2023
Michael R. McGarity-Shipley
1Centre for Neuroscience Studies, Queen's University, Kingston, Ontario K7L 3N6, Canada
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Simona Markovik Jantz
1Centre for Neuroscience Studies, Queen's University, Kingston, Ontario K7L 3N6, Canada
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Roland S. Johansson
3Physiology Section, Department of Integrative Medical Biology, Umeå University, SE-901 87 Umeå, Sweden
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Daniel M. Wolpert
4Department of Neuroscience, Columbia University, New York, New York, 10027
5Zuckerman Mind Brain Behavior Institute, Columbia University, New York, New York 10027
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J. Randall Flanagan
1Centre for Neuroscience Studies, Queen's University, Kingston, Ontario K7L 3N6, Canada
2Department of Psychology, Queen's University, Kingston, Ontario K7L 3N6, Canada
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    Figure 1.

    Apparatus and data scoring. A, Left, In experiments 1 and 2, participants grasped and lifted a test object with the tips of the index finger and thumb, which contacted sensors that measured the forces applied by the digits (left). Right, In experiment 3, participants held an additional 400 g tungsten disk in the hand while lifting the test object. B, The device used to control the weight of the object. A linear motor was used to position a trolley along a rotating rod, attached via a string running through pulleys, to a hook located in the center of the object. C, Vertical force (VF) and the first (VF Rate) and second derivatives of VF, and vertical position, velocity, and acceleration in a baseline trial in which the object weighed the expected 2 N (green) and a catch trial in which the object weighed 6 N (red). For the catch trial, the three vertical dashed lines mark the onset and offset (Lift-off) of the corrective response (gray zone) and the onset of the hold phase. D, Illustration of the method used to determine the amplitude and period of oscillations in VF during the corrective response.

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    Figure 2.

    Representative trials. A–C, VF, VF rate, and position traces from all trials performed by a participant who completed the 2-4 and 2-6 conditions. For illustrative purposes, we highlighted a single representative trial for each weight (thicker lines) and the first catch trial in each condition (dashed lines). D–F, Corresponding data for a participant who completed the 2-10 condition. Note that the dashed yellow line in F does not increase above zero because in the first lift the object did not lift off within 800 ms of the start of the corrective response. For each participant, the catch trials (blue, red, and yellow traces) are aligned to the onset of the corrective response (A–F). The baseline trials (green traces) were aligned so that the time at which VF reached 1 N matched the mean time at which the force reached 1 N in catch trials.

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    Figure 3.

    Experiment 1 results. A, Differences in predictive VF rate between catch trials and subsequent and prior baseline trials as a function of catch trial number. B, Corrective VF slope as a function of catch trial number in each condition. The dots show group means, and the height of the shaded area indicates ±1 SEM. The blue/red and red/yellow stars indicate significant differences (p < 0.05) between the 2-4 and 2-6 conditions and the 2-6 and 2-10 conditions, respectively. C, Corrective VF slope on the first and last catch trials in the 2-4 and 2-6 conditions shown for each condition order. D, E, Corrective VF slope (D) and total corrective response duration (E) over the last 10 catch trials in each condition. F, Lift height for each object weight over the last 10 trials in each condition. Bars show group means, error bars indicate SEM (D–F), and lines and dots show individual participant means (D, E) or medians (F). The symbols *, **, and *** indicate significant levels of p < 0.05, p < 0.01, and p < 0.001, respectively. The letters n.s. indicate non significance (p > 0.05).

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    Figure 4.

    Characteristics of VF oscillations. A, Estimated amplitude of oscillatory component of VF across conditions and phases; that is, corrective response and hold phase. B, Estimated amplitude of oscillatory component of VF across conditions and phases. Thin lines and circles represent individual participants, and error bars indicate ±1 SEM.

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    Figure 5.

    Results from Experiments 2 and 3. A, B, VF traces for the single catch trial in the 3-20 and 7-20 conditions (A) and the Control (Ctr) condition (B). Each trace represents a single participant, and traces from all participants are shown. Traces are aligned to the start of the corrective response. C, Corrective VF slope over the first 200 ms of the corrective response (A, B, gray regions) in each condition. D, Predictive VF rate in each condition. C, D, Bars show group means, error bars indicate ±1 SEM, and dots show individual participants. The symbols ** and *** indicate significant levels of p < 0.01 and p < 0.001, respectively. The letters n.s. indicate non significance (p > 0.05).

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The Journal of Neuroscience: 43 (49)
Journal of Neuroscience
Vol. 43, Issue 49
6 Dec 2023
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Fast Feedback Responses to Categorical Sensorimotor Errors That Do Not Indicate Error Magnitude Are Optimized Based on Short- and Long-Term Memory
Michael R. McGarity-Shipley, Simona Markovik Jantz, Roland S. Johansson, Daniel M. Wolpert, J. Randall Flanagan
Journal of Neuroscience 6 December 2023, 43 (49) 8525-8535; DOI: 10.1523/JNEUROSCI.1990-22.2023

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Fast Feedback Responses to Categorical Sensorimotor Errors That Do Not Indicate Error Magnitude Are Optimized Based on Short- and Long-Term Memory
Michael R. McGarity-Shipley, Simona Markovik Jantz, Roland S. Johansson, Daniel M. Wolpert, J. Randall Flanagan
Journal of Neuroscience 6 December 2023, 43 (49) 8525-8535; DOI: 10.1523/JNEUROSCI.1990-22.2023
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Keywords

  • adaptive responses
  • fast reflexes
  • object manipulation
  • optimization
  • sensorimotor control

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