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Optimal Feedback Control and the Neural Basis of Volitional Motor Control

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Optimal Feedback Control and the Neural Basis of Volitional Motor Control REVIEWS OPTIMAL FEEDBACK CONTROL AND THE NEURAL BASIS OF VOLITIONAL MOTOR CONTROL Stephen H. Scott Skilled motor behaviour, from the graceful leap of a ballerina to a precise pitch by a baseball player, appears effortless but reflects an intimate interaction between the complex mechanical properties of the body and control by a highly distributed circuit in the CNS. An important challenge for understanding motor function is to connect these three levels of the motor system — motor behaviour, limb mechanics and neural control. Optimal feedback control theory might provide the important link across these levels of the motor system and help to unravel how the primary motor cortex and other regions of the brain plan and control movement. Perhaps the most surprising feature of the motor system The goal of this review is to bring all three levels of is the ease with which humans and other animals can the motor system together, to illustrate how M1 is move. It is only when we observe the clumsy movements linked to limb physics and motor behaviour. The key of a child, or the motor challenges faced by individuals ingredient is the use of optimal feedback control as a with neurological disorders, that we become aware of model of motor control in which sophisticated behav- the inherent difficulties of motor control. iours are created by low-level control signals (BOX 2). The efforts of systems neuroscientists to understand I begin with a brief review of each level of the motor how the brain controls movement include studies system, followed by a more detailed description of how on the physics of the musculoskeletal system, neuro- optimal feedback control predicts many features of physiological studies to explore neural control, and neural processing in M1. investigations of motor behaviour (BOX 1).As knowl- edge continues to grow in each area, it becomes more Limb mechanics challenging to link these levels of the motor system and The peripheral motor system is a complex filter that to maintain a cohesive framework within which to converts patterns of muscle activity into purposeful describe motor function or to interpret the role of a movement. The basic building block of motor output is brain region. the motor unit — a motor neuron and the muscle fibres Take, for example, the primary motor cortex (M1). it innervates. The conversion of patterns of motor unit It has been known for more than 100 years that M1 is activity into muscle force depends on muscle fibre length, important for controlling volitional movements, but velocity, histochemical type and history-dependencies more detailed statements on its function vary greatly1. such as fatigue2–6.Muscle force is also influenced by Department of Anatomy and Cell Biology, Centre Studies of neural activity in M1 tend either to relate architectural features, including tendon and fascicle for Neuroscience Studies, neural activity to details of motor output, thereby length, the orientation of muscle fibres (pennation angle) Queen’s University, connecting motor cortical function to the motor and passive muscle elasticity7,8.Muscle morphometry Kingston, Ontario K7L 3N6, periphery, or to relate neural activity to hand motion, varies widely even across synergistic muscles9,10.The Canada. e-mail: thereby connecting motor cortical function to the goals effective joint torque that is generated by a muscle [email protected] of motor behaviour. Which view is correct? Are both depends on its mechanical advantage (moment arm) doi:10.1038/nrn1427 correct, and if so, how? about that joint, which often varies with joint angle11. 534 | JULY 2004 | VOLUME 5 www.nature.com/reviews/neuro © 2004 Nature Publishing Group REVIEWS Box 1 | Three main divisions of motor system research The musculoskeletal system is made up of Neural control muscles that act on a multi-articulated SMA skeleton. The translation of limb movement from muscle activity is dPM M1 S1 5 7 influenced by muscle and limb mechanics. PF Motor behaviour describes how the limb or body moves during a motor task, reflecting the combined action of the neural circuit that controls movement and the BG V1 mechanical properties of the limb. The neural basis of movement examines how RN different regions of the brain and spinal cord control motor output. C The CNS is generally viewed as having a RF hierarchical organization with three levels VN — the spinal cord, brainstem and cortex. The spinal cord is the lowest level, including Motor behaviour motor neurons, the final common pathway for all motor output, and interneurons that integrate sensory feedback from the skin, muscle and joints with descending commands from higher centres. The motor repertoire at this level includes Spinal cord stereotypical multi-joint and even multi- limb reflex patterns, and basic locomotor patterns. At the second level, brainstem regions Musculoskeletal mechanics such as the reticular formation (RF) and vestibular nuclei (VN) select and enhance the spinal repertoire by improving postural control, and can vary the speed and quality of oscillatory patterns for locomotion. The highest level of control is provided by the cerebral cortex, which supports a large and adaptable motor repertoire. The diagram illustrates some of the key regions that are involved in goal-directed reaching movements. (For more complete details, see REF.48.) Motor planning and visual feedback are provided through several parietal and premotor regions. The primary motor cortex (M1) contributes the largest number of axons to the corticospinal tract and receives input from other cortical regions that are predominantly involved in motor planning. Somatosensory information is provided through the primary somatosensory cortex (S1), parietal cortex area 5 (5) and cerebellar pathways. The basal ganglia (BG) and cerebellum (C) are also important for motor function through their connections with M1 and other brain regions. (RN, red nucleus; V1, primary visual cortex; 7, region of posterior parietal cortex; dPM, dorsal premotor cortex; SMA, supplementary motor area; PF,prefrontal cortex.) .. 2 Θ Θ Skeletal organization has a profound influence on Te = (I2 + m2c2 + m2l1c2 cos e) s + 22.. the conversion of muscle forces into limb motion. Limb (I + m c )Θ + (m l c sinΘ )Θ (2) mechanics are relatively straightforward when move- 2 2 2 e 2 1 2 e s ment is constrained to occur at only a single joint and where 1 and 2 reflect properties of the upper arm and with only one degree of mechanical freedom (flexion or forearm/hand, respectively, and s and e denote shoulder extension)... MUSCULAR TORQUE (T) is defined simply.. as and elbow, respectively. Muscular torque at a joint T = IΘ ,where I equals the moment of inertia, and Θ is depends on several parameters that relate to each the angular acceleration of the joint. This angular segment’s moment of inertia (I), length (l), mass (m) version of the familiar equation, force = mass × linear and centre of mass (c)1. acceleration, means that there is a direct relationship These equations of motion mean that there is no between joint motion and torque. This simple relation- longer a one-to-one mapping between joint motion and MUSCULAR TORQUE ship disappears when movement involves more than muscular torque, so that torque at one joint can generate (or moment). Each muscle one joint. The equations of motion to describe muscular motion at other joints12,13.The mechanics of multi-joint generates force from muscle torque at the shoulder (Ts) and elbow (Te) are movements cannot be predicted from the physics of contraction (active) and elastic (equations 1,2): single-joint movements14,15 (BOX 3).The equations forces (passive). Muscular torque .. for a muscle equals its total force 222 Θ Θ of motion expand when more joints are involved and Ts = (I1 + I2 + m1c1 + m2 (l1 + c2 + 2l1c2 cos e)) s multiplied by its moment arm 22.. when joints have multiple degrees of freedom. (the perpendicular distance + (I + m c + m l c cosΘ )Θ – (m l c sinΘ )Θ – 2 2 2 ..2 1 2 e e 2 1 2 e e Furthermore, a hand-held object or environmental between a muscle’s line of action Θ Θ Θ (2m2l1c2 sin e) s e (1) forces such as ground reaction forces during walking and the joint centre of rotation). NATURE REVIEWS | NEUROSCIENCE VOLUME 5 | JULY 2004 | 535 © 2004 Nature Publishing Group REVIEWS Motor behaviour Box 2 | Optimal feedback control Body movements are smooth, despite the complexities a Noise of the peripheral motor system. For example, hand Movement trajectories remain relatively straight from start to end, Optimal Motor and hand velocity follows a smooth, bell-shaped pro- Task selection feedback commands 19,20 (FIG. 1) control law file .This smoothness at least partially reflects the low-pass filter properties of muscle21.Perturbations Efferent System state copy Noise of the hand during slow movements are corrected back (positions, velocities, towards the unperturbed trajectory, indicating that forces) feedback is used to maintain a relatively straight hand Optimal Sensory 22 state estimator feedback trajectory, at least under these conditions .Such simple features of hand motion mean that the CNS compen- b Optimal control X Redundancy elimination sates for the complexities of limb mechanics. – 2 2 X The motor system can also adapt to changes in Initial + Initial X 1 the mechanical environment. Lackner and DiZio23 Task error observed how subjects performed reaching movements 2 2 X Final X before, during and after they sat in a room that rotated Final X at 6 rpm, creating a coriolis force on the limb. When R 1 – e d X subjects performed their first reaching movements 0 u 2 n d a with the right arm in the rotating room, after the otolith n 02 t X1 X1 organs no longer sensed room rotations, the move- ments were curved to the right.
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