Feedback control during voluntary motor actions

doi:10.1016/j.conb.2015.03.006

Current Opinion in Neurobiology

Volume 33, August 2015, Pages 85-94

https://doi.org/10.1016/j.conb.2015.03.006 Get rights and content

Highlights

•
Advanced control theory highlights the role of sensory feedback for motor function.
•
Goal-directed feedback begins in muscle activity ∼60 ms after the limb is disturbed.
•
Goal-directed feedback begins in muscle activity ∼100 ms after vision of the limb or goal is altered.
•
Frontoparietal and subcortical brain circuits generate these goal-directed responses.

Humans possess an impressive ability to generate goal-oriented motor actions to move and interact with the environment. The planning and initiation of these body movements is supported by highly distributed cortical and subcortical circuits. Recent studies, inspired by advanced control theory, highlight similar sophistication when we make online corrections to counter small disturbances of the limb or altered visual feedback. Such goal-directed feedback is likely generated by the same neural circuits associated with motor planning and initiation. These common neural substrates afford a highly responsive system to maintain goal-directed control and rapidly select new motor actions as required to deftly move and interact in a complex world.

Introduction

Over the last two decades, most research on voluntary motor control has focused on the planning and initiation of motor actions, with little emphasis on afferent feedback from the moving limb. The ideas of optimal feedback control and other advanced control theories have refocused attention on the importance of sensory feedback in biological control. The result is a renaissance in exploring the complex ways in which somatosensory and visual feedback can influence ongoing motor actions. Here we review studies demonstrating that small corrective responses during voluntary motor actions possess most, if not all, of the complexities associated with motor planning and movement initiation. Further, we discuss how these sophisticated corrective responses reflect processing in a highly distributed network of cortical and subcortical circuits.

There have been several recent reviews to discuss the principles of feedback control and their application to biological control [1, 2], with several in-depth reviews focused on the importance of somatosensory feedback [3, 4, 5, 6, 7], visual feedback [8, 9], or the integration of vision and somatosensory feedback during voluntary actions [10]. Related topics of interest are the importance of sensory feedback in motor decisions [11] and the use of dynamical systems theory to interpret the cortical control of movement [12].

Section snippets

Somatosensory feedback: upper limb

A common paradigm to explore how somatosensory feedback influences voluntary control is to observe how subjects respond to small mechanical perturbations [5, 6, 7]. Recent studies have shown that corrective responses are faster when the urgency to respond is increased by manipulating the return time, or size and shape of the spatial goal [13, 14]. Rapid corrective responses occur even for very small disturbances that approach the natural variability of limb motion [15], illustrating that

Neural implementation of feedback control

The voluntary motor system is hierarchically organized, and correspondingly, corrective responses reflect contributions from many levels of this hierarchy (Figure 2). It has been assumed that co-contraction of antagonist muscles plays an important role in minimizing the effect of disturbances. However, estimates for muscle stiffness commonly used in the field are almost an order of magnitude too high, as they include contributions from neural feedback processes [28^•]. The main benefit of

Conclusions

A growing body of literature highlights the surprising sophistication of rapid corrective responses generated by visual and somatosensory feedback. Long-latency stretch responses are highly context-dependent reflecting the behavioural goal and many other factors essential for moving and interacting in the world. These corrective responses share most, if not all, of the complexities typically ascribed to voluntary control. Considerable work remains to understand how these feedback processes are

Conflict of interests

SHS is associated with BKIN Technologies, which commercializes the KINARM robot used in some studies described in this review. TC, CRL and TT do not have any conflicts of interest.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

• of special interest
•• of outstanding interest

Acknowledgements

This work was supported by grants from the Natural Sciences and Engineering Research Council of Canada (NSERC) and the Canadian Institutes of Health Research (CIHR). SHS is supported by a GSK-CIHR Chair in Neuroscience. TC is supported by a Banting Postdoctoral Fellowship.

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View full text

Feedback control during voluntary motor actions

Highlights

Introduction

Section snippets

Somatosensory feedback: upper limb

Neural implementation of feedback control

Conclusions

Conflict of interests

References and recommended reading

Acknowledgements

Curr Opin Neurobiol

Clin Neurophysiol

Trends Cogn Sci

Trends Cogn Sci

J Neural Transm

Nature

Exp Brain Res

PLoS Comput Biol

J Neurosci

Cell

Nature

J Neurophysiol

J Neurophysiol

Front Hum Neurosci

J Neurol Sci

Front Syst Neurosci

Computational approaches for goal-directed movement planning and execution

The Cognitive Neurosciences

Optimal feedback control and the long-latency stretch response

Exp Brain Res

Primary motor cortex and fast feedback responses to mechanical perturbations: a primer on what we know now and some suggestions on what we should find out next

Front Integr Neurosci

The influence of visual target information on the online control of movements

Vision Res

Visually-guided correction of hand reaching movements: the neurophysiological bases in the cerebral cortex

Vision Res

A perspective on multisensory integration and rapid perturbation responses

Vision Res

On the challenges and mechanisms of embodied decisions

Philos Trans R Soc B Biol Sci

Cortical control of arm movements: a dynamical systems perspective

Annu Rev Neurosci

Feedback responses rapidly scale with the urgency to correct for external perturbations

J Neurophysiol

Influence of the behavioral goal and environmental obstacles on rapid feedback responses

J Neurophysiol

Fast corrective responses are evoked by perturbations approaching the natural variability of posture and movement tasks

J Neurophysiol

Context-dependent inhibition of unloaded muscles during the long-latency epoch

J Neurophysiol

Rapid online selection between multiple motor plans

J Neurosci

Dependence of EMG responses evoked by imposed wrist displacements on pre-existing activity in the stretched muscles

Can J Neurol Sci J Can Sci Neurol

Observations on the automatic compensation of reflex gain on varying the pre-existing level of motor discharge in man

J Physiol

Temporal evolution of “automatic gain-scaling”

J Neurophysiol

Deliberation in the motor system: reflex gains track evolving evidence leading to a decision

J Neurosci

Motor control is decision-making

Curr Opin Neurobiol

Long-latency muscle activity reflects continuous, delayed sensorimotor feedback of task-level and not joint-level error

J Neurophysiol

Sensorimotor feedback based on task-relevant error robustly predicts temporal recruitment and multidirectional tuning of muscle synergies

J Neurophysiol

Contributions of feed-forward and feedback strategies at the human ankle during control of unstable loads

Exp Brain Res

Acceleration dependence and task-specific modulation of short- and medium-latency reflexes in the ankle extensors

Physiol Rep

Beyond muscles stiffness: importance of state-estimation to account for very fast motor corrections

PLoS Comput Biol

Interactions with compliant loads alter stretch reflex gains but not intermuscular coordination

J Neurophysiol

Task-dependent coordination of rapid bimanual motor responses

J Neurophysiol

Rapid feedback corrections during a bimanual postural task

J Neurophysiol

Flexible switching of feedback control mechanisms allows for learning of different task dynamics

PLoS ONE