Feedback and feedforward adaptation to visuomotor delay during reaching and slicing movements

• Published in: The European journal of neuroscience Vol. 38; no. 1; pp. 2108 - 2123
• Main Authors: Botzer, Lior, Karniel, Amir
• Format: Journal Article
• Language: English
• Published: Oxford Blackwell Publishing Ltd 01.07.2013; Blackwell
• Subjects: Adaptation, Physiological; ballistic movement; Biological and medical sciences; Biomechanical Phenomena; Brain - physiology; feedback control; Feedback, Sensory; forward model; Fundamental and applied biological sciences. Psychology; Hand - innervation; Hand - physiology; human; Humans; internal model; Models, Neurological; Movement; Photic Stimulation; Proprioception - physiology; Psychomotor Performance - physiology; Reaction Time; Vertebrates: nervous system and sense organs; Vision, Ocular - physiology; visuomotor delay; Human; forward model; feedback control; Models; internal model; visuomotor delay; ballistic movement; Adaptation; human
• ISSN: 0953-816X; 1460-9568; 1460-9568
• DOI: 10.1111/ejn.12211

It has been suggested that the brain and in particular the cerebellum and motor cortex adapt to represent the environment during reaching movements under various visuomotor perturbations. It is well known that significant delay is present in neural conductance and processing; however, the possible representation of delay and adaptation to delayed visual feedback has been largely overlooked. Here we investigated the control of reaching movements in human subjects during an imposed visuomotor delay in a virtual reality environment. In the first experiment, when visual feedback was unexpectedly delayed, the hand movement overshot the end‐point target, indicating a vision‐based feedback control. Over the ensuing trials, movements gradually adapted and became accurate. When the delay was removed unexpectedly, movements systematically undershot the target, demonstrating that adaptation occurred within the vision‐based feedback control mechanism. In a second experiment designed to broaden our understanding of the underlying mechanisms, we revealed similar after‐effects for rhythmic reversal (out‐and‐back) movements. We present a computational model accounting for these results based on two adapted forward models, each tuned for a specific modality delay (proprioception or vision), and a third feedforward controller. The computational model, along with the experimental results, refutes delay representation in a pure forward vision‐based predictor and suggests that adaptation occurred in the forward vision‐based predictor, and concurrently in the state‐based feedforward controller. Understanding how the brain compensates for conductance and processing delays is essential for understanding certain impairments concerning these neural delays as well as for the development of brain–machine interfaces. We investigated the control of reaching movements during an imposed visuomotor delay. In a series of two experiments, subjects learned to reach and to perform rhythmic movements using a visual feedback cue to a spatial target. Our findings show that subjects can adapt to visual delay, and our computational model and simulations explain these results based on two adapted forward models and a third feedforward controller, while refuting delay representation in a pure forward vision‐based predictor.