I have briefly presented the modern theories of motor control & learning many months ago. Although such concepts appeared after the '90s, the field has been in existence ever since the beginning of the last century. The current post is meant like a historical summary that stems from behavior perspectives. People began to ponder the basis and characteristics of movement productions as far back as 19th century. The field was heavily influenced by two separate but related fields: psychology (which was dominated by behaviorists) and the birth of neurophysiology (the study of the nervous system through electrophysiological recordings in animals).
Woodworth (1899) was one of the earliest pioneers in studying rapid arm movements and laid down the foundation of measurement such as movement speed, performance error, etc. Edward Thorndike (1914), in his Law of Effect, proposed how actions that are rewarded tend to be repeated. His ideas gave the foundation of instrumental conditioning in the field of psychology. Almost during the same period, Charles Sherrington talked about the concepts of reflexes, the final common pathway (alpha motor neurons), and sensory receptor of movements in which he coined the term proprioception. Moving to Eastern Europe, a Soviet scientist N. Bernstein made an influential contribution during 1930s where he called motor control as a degree-of-freedom problem (redundancy problem). This is because our limbs consist of various joints and each joint is connected to hundreds of muscle fibers that can be active separately. Correspondingly, different sets of motor activities capable of producing the same behavior are called motor equivalence. How does the brain know which muscle(s) to control among the various possible combination? A decade later, K. Lashley did studies on handwriting (1946) where he suggested the concept of a motor program inherent in each voluntary movement. This idea suggests the movements are based on an open-loop concept, undermining the role of sensory feedback. After WW-II ended, advancement in mathematics and information theory helped the formulation of a speed-accuracy trade-off by Paul Fitts (1954, 1964). Using a neat methodology, he discovered the link between movement speed and accuracy, now known as the Fitts' Law.
At the end of 1950's, the field of psychology shifted to themes in cognitive science that talked about attention and memory, a new euphoria for the scientific community. The concept of higher-order brain functions emerged and the flavor of motor behavior research shifted. Soon after, a strong interest focusing on "learning" appeared. In 1971, Jack Adams proposed a concept of closed-loop theory of motor learning in addition to other studies, e.g. short-term memory of movements. Mike Posner (1969) studied the role of attention, short-term memory, and movement control, expanding the concept of short-term memory storage and motor behavior. Fitts and Posner (1967) perhaps were known for their concept of three stages in motor skill acquisition. The role of attention on motor control and learning was also studied by S. Keele. His motor control thesis on the motor program was also quite influential (1968, 1986).
By the end of 1980s, integration of motor behavior and sports science gained momentum with goals of understanding motor skill learning, maintaining, and maximizing performance (e.g. F. Henry, John Whitting). At the same time, the field of neurophysiology also gained maturity in both animal studies and clinical works. This is the precursor of modern neuroscience. Rather than focusing on observable or products of behavior, scientists tried to elucidate the role of the brain or nervous system in performing movements. For example, Merton & Merton, Ian Boyd studied muscle spindles; Evarts and Georgopoulos respectively studied the neural discharge of a single neuron and ensemble of neurons in the motor cortex in awake behaving monkeys; Milner, Tulving, Tolman studied long-term memory; and Teuber for modern neuropsychology.
Interests in Bernstein's muscle coordination and redundancy problem reappeared in 1980's. On two separate occasions, Feldman and Bizzi came forward with his equilibrium point hypothesis to explain motor control. Another scientist, Latash proposed an improved theory of muscular coordination (or synergy). He said that the degree of freedom problem is solved in the brain by controlling a set of muscles doing the same job. The theory has been expanded: rather than the synergy of different neural circuits controlling movements, it refers to the synergy of the pattern of coordination such that the movement outcomes are stable and at the same time flexible. See Latash et al. (2007) for a nice summary.
Open-loop Processes and Motor Program
William James (1890) said that movement control is born out of a muscular contraction in response to either an external or internal event. This contraction produces a set of sensory feedback (now known as proprioception) from the muscles which in turn triggers another muscular contraction and so on. This sequence of events is also called the response-chaining hypothesis. In skilled movement, attention is needed for the initiation of the first action and subsequent series of actions can be 'automatically' running. The fundamental element of learning is by associating given feedback with the next action. This is the first proponent of an open-loop motor process. Our brain creates the very first muscular contraction in an effector or limb. There is no output monitoring, in the sense, no error correction. If something goes wrong or the environment changes, open-loop control can do no corrective actions. In contrast, a closed-loop process is used when we perform the online correction. In this particular case, afferent feedback provides information on the movement outcome. The discrepancy between the actual and planned (reference) movement is the basis for error correction.
Studies with deafferented animals and patients have shown that sensory feedback from the muscles is not critical for motor control. Although the trajectory isn't as smooth and accurate, movement production is still possible. James' theory is therefore not universally complete. Still, though, there are other experiments that may point to the existence of an open-loop executive controller. For example, the central pattern generator (the most popular experiment is the one involving decerebrated cats on a treadmill [FV Severin, et al. 1966]) and reflex responses. Furthermore, because sensory processing is slow, how can rapid movements be executed other than through an open-loop process?
Challenges to the concept of a motor program include storage space and producing novel movements never learned before. In terms of speech, e.g., if there are 100 types of sound produced, how many motor programs should a person have? For these reasons, Schmidt (1975) proposed a generalized motor program or GMP, that contains parameters that can be adjusted depending on the situation and purpose. Invariant features of certain movements are thought to be as a result of GMP. Each movement has its own invariant features or signatures. Parameters to be adjusted include: relative timing or duration, the sequence of events, force (impulse) generation, and thus muscles recruitment. Accordingly, the motor program tells the muscles when to turn on, how much force to produce, and when to turn off.
Equilibrium-point Hypothesis
According to this theory, the movement end-points are programmed by the brain and biomechanical properties of the muscle determine the trajectory. In other words, to produce a movement, the brain has to only specify where, not how/when. The model sees our musculoskeletal system as a mass-spring mechanism with stiffness, a force-length relationship. Inherently, muscle fibers are behaving like a spring where certain tension (unit: Newton) is associated with a certain muscle length or elbow angle (cm or degree). The length and tension become two invariant characteristics of the model. The best example comes from using biceps-triceps of the upper arm, an example of antagonistic muscles. Extension occurs because there is a "force" acting to stretch to the biceps. This force increases tension in the biceps but reduces tension in the triceps. Upon sudden "removal" of the force, the musculoskeletal structure goes back to an equilibrium point.
Close-loop Processes
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| Open loop (left) and close-loop (right) processes |
Contrary to the open-loop motor control, the closed-loop model says that sensory feedback plays a crucial role in movement execution. According to this theory, an executive controller continuously monitors the difference between the actual movement produced by the effector or limb, and the intended movement goal (reference). If there is a discrepancy (error), the executive controller sends the command to the limb to correct for this error. This process is generally slower as it requires information processing, e.g. attention control. This is even so as the reference point may change from time to time. In addition, we now know that sensory afferents contain noise and require time (~200 msec) to travel to the cerebral cortex.
One source of sensory feedback comes from the somatosensory and vestibular systems. Although our limbs contain somatosensory feedback in the form of proprioception or kinaesthesia (spindles, joints, tendon organ), the visual system is arguably the most predominant source of perception. This has been shown in the classic literature (e.g. by Gibson, 1943; Adams, 1975; and Jordan, 1972 ). The notion "perception drives action" is the key to Gibson's theory. While the information carried by the proprioception is limited to own-body, the visual system tells us information about both own-body and external world or environment. Such a feedback source is called exteroceptor. For example: while performing an action, we understand that the body moves and at the same time the surrounding moves. Specifically, the apparent motion of objects in the visual scene caused by the relative motion between an observer and a scene is known as optical flow. We now know that the brain contains two visual streams: ventral visual stream (for object recognition or visual perception), and dorsal visual stream (for movement or motion, vision for action!).
The greatest strength of the closed-loop model is the ability to explain movements that are slow, e.g. tracking and tracing. Woodworth's throwing task shows how vision is useful especially when movement duration is > 200 msec. Further, visual feedback is useful during anticipatory activity if the stimulus is available long enough. Close-loop control is important for muscle stiffness by making use of information from the muscle spindle (Houk, 1976). Daily activities that require corrective actions are also considered, e.g. rotating a ball using the index finger. Unfortunately, many other movements that we make are much faster, e.g. aiming to grab a falling item, throwing or kicking a ball, etc. Such quick movements are termed ballistic and require rapid muscle contractions producing high movement velocity. In such a scenario, it is impossible to continuously process sensory feedback (Schmidt, 1972).
One evidence of the feedback influence to rapid movement comes from studies involving long-loop or transcortical reflex. Studies in primates and humans suggest the existence of a long-loop reflex following sudden perturbation of arm/hand position. The existence of two distinct EMG or electromyograph spikes, for example, indicates that there is another signal, M2 (~50-70 msec latency) to the motor neurons following the first, involuntary, short-latency monosynaptic reflex M1 (~30-50 msec latency). Once a source of controversy, this M2 signal is thought to be supraspinal, requires no conscious attention, and can be influenced by prior instructions. The next EMG burst following M2 is the voluntary movement itself and it is regulated by the cerebral cortex (> 150 msec latency).
Ballistic Movement: Reaching
In principle, a motor task can be divided according to the start and endpoint into discrete, continuous, and serial tasks or skills. A discrete task is a motor task where there are a clear start and endpoint. A continuous task, on the other hand, is a motor task that is continuous and repeated (cyclical). A serial task is a special form of a discrete task in which movements are performed according to a certain sequence. In terms of speed, the motor task can be divided into slow and rapid or ballistic movements. We'll talk briefly about reaching movement here.
Woodworth first discussed this topic in detail a century ago. Ballistic reaching is prevalent in everyday lives, e.g. from movements performed during boxing, playing tennis, and daily voluntary movements such as reaching and grasping (prehension). Such movements are characterized by fast muscle contractions that yield very high speed/acceleration. Scientists thought this mechanism is too fast to be managed by a closed-loop controller in the brain.
While reaching primarily involves the muscular control that rotates shoulder and elbow joints, grasping involves more complex coordination among the five fingers. In most cases, both movements typically occur almost within one intended action in daily lives. The opening of the hand to grasp an object often happens well before the whole arm reaches the object. Does this mean reach-and-grasp is managed by the same motor GMP? According to Jeannerod (1984), reach-and-grasp consists of two behavior phases that utilize two independent neural channels working in parallel, both require a visual system to make visuomotor coordination possible. The two paths are:
1) A fast initial, transport phase that brings the hand closer to the object,
- Requires a channel that processes the object's extrinsic properties.
- E.g. object location w.r.t the body, orientation, direction; viewer-centered coordinates.
2) A slow, open-the-hand phase during which the hand makes contact with the object.
- Requires another channel that uses the object's intrinsic properties.
- These properties include e.g. object size, shape.
In later studies, Arbib et al. proposed that both channels are interdependent through temporal coordination which is necessary to ensure both phases are fulfilled correctly. Opponents to this theory (e.g. by Wing et al.) suggested another concept where spatial, instead of temporal, coordination is required. In another premise, Smeets and Brenner proposed that reach-and-grasp has no distinct temporal components and is nothing but pointing using thumb and finger.
Speed and accuracy
"Haste makes waste". The fact that faster movements lead to lesser accuracy is known as the principle of a speed-accuracy trade-off. It was Woodworth who first did an experiment studying the relationship between voluntary aiming and its accuracy. He said that manual aiming consists of two phases. The first is an initial open-loop phase (initial adjustment) that propels the hand towards a target. The second phase is a current-control phase using visual feedback to land into the target. This and the following experiment make up a cornerstone of human motor control.
Half a century later, Fitts revisited the concept and showed a formulation of this trade-off. The formula says that average movement time (MT) is linearly related to the index of difficulty. This index is log [2A/W] where A is movement amplitude and W is target width to aim. Both A and W are tightly controlled during the experiment. His law suggests an inverse relationship between 'difficulty' of a movement and the completion time or speed. In the mathematical equation, a and b are Y-intercept and slope respectively. The slope represents a measure of 'controllability', the additional MT caused by an increase in the index of difficulty by a unit. Movements utilizing an upper limb exhibits a steeper slope than fingers. A higher slope is also shown in older adults. The log relationship is presumably due to information load (related to e.g. Hick's study). Subsequent studies have suggested that Fitts' Law can be found in many different situations: cyclical and discrete tasks, in children, adults, and used in neurological patients.
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| Experiment setup used by Fitts in his early days |
Some models attempt to explain Fitts' Law. The most important one is probably the impulse variability model (Schmidt et al., 1979), a model of simple rapid aiming movements in which the variability of the impulse of forces leads directly to variations in the movement end-point of a limb. With this model, the initial phase (initial-impulse) of a ballistic movement is therefore crucial. Related to GMP, this impulse is like a code that tells arm muscles to produce forces within a certain time. The theory maintains that as the distance from a target increases, more force must be exerted, leading to greater variability in movement trajectory, decreasing the chances of hitting the target. To compensate for this, the movement time can be slowed down. A variant of this is by Meyer et al. called the optimized impulse variability model. According to this model, if an error occurs while performing an extremely rapid movement (e.g. the target overshoot or undershoot), a quick corrective movement follows after.
Although Fitts' Law was originally studied in terms of spatial accuracy, later studies discussed the characteristics of a temporal trade-off. This is relevant for example movement reaction time, preparatory time, etc, in baseball (see, e,g. Wing-Kristofferson timing model)
Reference: The writing and diagrams are based on a textbook, "Motor Control & Learning: a Behavioral Emphasis, 5ed" by RA Schmidt & T Lee.
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