A generative learning model for saccade adaptation

PLoS Comput Biol. 2019 Aug 9;15(8):e1006695. doi: 10.1371/journal.pcbi.1006695. eCollection 2019 Aug.

Abstract

Plasticity in the oculomotor system ensures that saccadic eye movements reliably meet their visual goals-to bring regions of interest into foveal, high-acuity vision. Here, we present a comprehensive description of sensorimotor learning in saccades. We induced continuous adaptation of saccade amplitudes using a double-step paradigm, in which participants saccade to a peripheral target stimulus, which then undergoes a surreptitious, intra-saccadic shift (ISS) as the eyes are in flight. In our experiments, the ISS followed a systematic variation, increasing or decreasing from one saccade to the next as a sinusoidal function of the trial number. Over a large range of frequencies, we confirm that adaptation gain shows (1) a periodic response, reflecting the frequency of the ISS with a delay of a number of trials, and (2) a simultaneous drift towards lower saccade gains. We then show that state-space-based linear time-invariant systems (LTIS) represent suitable generative models for this evolution of saccade gain over time. This state-equation algorithm computes the prediction of an internal (or hidden state-) variable by learning from recent feedback errors, and it can be compared to experimentally observed adaptation gain. The algorithm also includes a forgetting rate that quantifies per-trial leaks in the adaptation gain, as well as a systematic, non-error-based bias. Finally, we study how the parameters of the generative models depend on features of the ISS. Driven by a sinusoidal disturbance, the state-equation admits an exact analytical solution that expresses the parameters of the phenomenological description as functions of those of the generative model. Together with statistical model selection criteria, we use these correspondences to characterize and refine the structure of compatible state-equation models. We discuss the relation of these findings to established results and suggest that they may guide further design of experimental research across domains of sensorimotor adaptation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Physiological*
  • Algorithms
  • Computational Biology
  • Humans
  • Learning / physiology
  • Models, Biological*
  • Models, Psychological
  • Saccades / physiology*

Grants and funding

This work was supported by Deutsche Forschungsgemeinschaft (DFG) grants to MR (RO 3579/2-1, RO 3579/3-1, and RO 3579/8-1). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.