Contextual effects in sensorimotor adaptation adhere to associative learning rules

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Abstract

Traditional associative learning tasks focus on the formation of associations between salient events and arbitrary stimuli that predict those events. This is exemplified in cerebellar-dependent delay eyeblink conditioning, where arbitrary cues such as a light or tone act as conditioning stimuli (CSs) that predict aversive sensations at the cornea (unconditioned stimulus, US). Here we ask if a similar framework could be applied to another type of cerebellar-dependent sensorimotor learning – sensorimotor adaptation. Models of sensorimotor adaptation posit that the introduction of an environmental perturbation results in an error signal that is used to update an internal model of a sensorimotor map for motor planning. Here we take a step towards an integrative account of these two forms of cerebellar-dependent learning, examining the relevance of core concepts from associative learning for sensorimotor adaptation. Using a visuomotor adaptation reaching task, we paired movement-related feedback (US) with neutral auditory or visual contextual cues that served as conditioning stimuli (CSs). Trial-by-trial changes in feedforward movement kinematics exhibited three key signatures of associative learning: Differential conditioning, sensitivity to the CS-US interval, and compound conditioning. Moreover, after compound conditioning, a robust negative correlation was observed between responses to the two elemental CSs of the compound (i.e., overshadowing), consistent with the additivity principle posited by theories of associative learning. The existence of associative learning effects in sensorimotor adaptation provides a proof-of-concept for linking cerebellar-dependent learning paradigms within a common theoretical framework.

Data availability

All data generated or analysed during this study are included in the manuscript; Source Data files have been provided for Figures 2B, 2C, 2D, 5B, 6B, 6C, 6D, 7B, 7C, 7D, 8B, 8C, 8E and 8F.All raw data files and codes for data analysis and simulations are available from the GitHub repository: https://github.com/guyavr/AssociativeMotorAdaptation.git

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Author details

Guy Avraham

Department of Psychology, University of California, Berkeley, Berkeley, United States

For correspondence
guyavraham@berkeley.edu

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0002-6170-1041
Jordan A Taylor

Department of Psychology, Princeton University, Princeton, United States

Competing interests
No competing interests declared.
Assaf Breska

Department of Psychology, University of California, Berkeley, Berkeley,, United States

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0002-6233-073X
Richard B Ivry

Department of Psychology, University of California, Berkeley, Berkeley, United States

Competing interests
Richard B Ivry, Senior editor, eLife, and a co-founder with equity in Magnetic Tides, Inc..

"This ORCID iD identifies the author of this article:" 0000-0003-4728-5130
Samuel David McDougle

Department of Psychology, Yale University, New Haven, United States

For correspondence
samuel.mcdougle@yale.edu

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0001-8100-4238

Funding

National Institutes of Health (NS084948)

Jordan A Taylor

National Science Foundation (1838462)

Jordan A Taylor

National Science Foundation (1827550)

Jordan A Taylor

Office of Naval Research (N00014-18-1-2873)

Jordan A Taylor

National Institutes of Health (NS116883)

Richard B Ivry

National Institutes of Health (DC077091)

Richard B Ivry

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Human subjects: The study was approved by the Institutional Review Board at the University of California, Berkeley (Protocol 2016-02-8439) and adhered to the principles expressed in the Declaration of Helsinki. All participants provided written informed consent to participate in the study.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.