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Voluntary Movement: The Primary Motor Cortex
Motor Functions Are Localized within the Cerebral Cortex Many Cortical Areas Contribute to the Control of Voluntary Movements Voluntary Motor Control Appears to Require Serial Processing The Functional Anatomy of Precentral Motor Areas is Complex The Anatomical Connections of the Precentral Motor Areas Do Not Validate a Strictly Serial Organization The Primary Motor Cortex Plays an Important Role in the Generation of Motor Commands Motor Commands Are Population Codes The Motor Cortex Encodes Both the Kinematics and Kinetics of Movement Hand and Finger Movements Are Directly Controlled by the Motor Cortex Sensory Inputs from Somatic Mechanoreceptors Have Feedback, Feed-Forward, and Adaptive Learning Roles The Motor Map Is Dynamic and Adaptable The Motor Cortex Contributes to Motor Skill Learning An Overall View
“…. The physiology of movements is basically a study of the purposive activity of the nervous system as a whole.” — Gelfand et al., 1966
O
ne of the main functions of the brain is to direct the body’s purposeful interaction with the environment. Understanding how the brain
fulfils this role is one of the great challenges in neural science. Because large areas of the cerebral cortex are implicated in voluntary motor control, the study of the cortical control of voluntary movement provides important insights into the functional organization of the cerebral cortex as a whole. Evolution has endowed mammals with adaptive neural circuitry that allows them to interact in sophis- ticated ways with the complex environments in which they live. Adaptive patterning of voluntary move- ments gives mammals a distinct advantage in locat- ing food, finding mates, and avoiding predators, all of which enhance the survival potential of the individual and a species. The ability to use fingers, hands, and arms in voluntary actions independent of locomotion further helps primates, and especially humans, exploit their environment. Most animals must search their envi- ronment for food when hungry. In contrast, humans can also “forage” by using their hands to cook a meal or simply punch a few buttons on a telephone and order takeout. The central neural circuits responsible for such nonlocomotor behavior emerged from and remain intimately associated with the phylogenetically older circuits that control the forelimb during locomo- tor behaviors. In this and the following chapter we focus on the control of voluntary movements of the hand and arm in primates. In this chapter we describe the cortical net- works that control voluntary movement, particularly the role of the primary motor cortex in the generation of motor commands. In the next chapter we address broader questions about cortical control of voluntary motor behavior, in particular how the cerebral cortex
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organizes the stream of incoming sensory information to guide voluntary movement. Voluntary movements differ from reflexes and basic locomotor rhythms in several important ways. By definition they are intentional—they are initiated by an internal decision to act—whereas reflexes are auto- matically triggered by external stimuli. Even when a voluntary action is directed toward an object, such as reaching for a cup, the cause of action is not the object but an internal decision to interact with the object. The presence of the object provides only the opportunity for acting. Voluntary actions involve choices between alternatives, including the choice not to act. Further- more, they are organized to achieve some goal in the near or distant future. Voluntary movements often have a labile, con- text-dependent association with sensory inputs. The same object can evoke different voluntary actions or no response at all depending on the context in which it appears. That is, the neural circuits controlling vol- untary behavior are able to differentiate between an object’s physical properties and its behavioral salience. The nature and effectiveness of voluntary move- ments often improve with experience. The motor system can learn new behavioral strategies or new reactions to familiar stimuli to improve behavioral out- comes, and it can learn new skills to cope with predict- able variations and perturbations of the environment. Thus the neural control of voluntary movement involves far more than simply generating a particular pattern of muscle activity. It also involves processes that are usually considered to be more sensory, per- ceptual, and cognitive in nature. As we shall see, these processes are not rigidly compartmentalized into dif- ferent neural structures or neural populations.
Motor Functions Are Localized within the
Cerebral Cortex
For centuries it was believed that the human cerebral cortex was responsible for only higher-order, con- scious mental functions. In the middle of the 19th cen- tury the English neurologist John Hughlings Jackson made the controversial proposal that a specific part of the cerebral cortex anterior to the central sulcus has a causal role in movement. He reached this conclusion from treating patients with epileptic seizures that were characterized by repeated spasmodic involuntary movements that sometimes resembled fragments of purposive voluntary actions.
During each episode the seizures always spread to different body parts in a fixed temporal sequence that varied from patient to patient, a pattern called Jacksonian march. Jackson concluded that paroxysmal neural activity generated by epileptic foci located near the central sulcus caused the involuntary seizures. He speculated that the progression of seizures across the body resulted from the spread of paroxysmal activity across small clusters of neurons lying along the central sulcus, each of which controlled movement of a differ- ent body part. Jackson’s proposal that a discrete corti- cal region is involved in the control of movement was a strong argument for the localization of different func- tions in distinct parts of the cerebral cortex. His obser- vations, along with contemporaneous studies by Pierre Paul Broca and Karl Wernicke on the language deficits resulting from specific cortical lesions, laid the founda- tion for the modern scientific study of cortical function. It was not until later in the 19th century, how- ever, when improved anesthesia and aseptic surgical techniques allowed direct experimental study of the cerebral cortex in live subjects, that conclusive experi- mental evidence for a discrete region of the cerebral cortex devoted to motor function was possible. Gustav Fritsch and Eduard Hitzig in Berlin and David Ferrier in England showed that electrical stimulation of the surface of a limited area of cortex of different surgically anesthetized mammals evoked movements of parts of the contralateral body. The electric currents needed to evoke movements were lowest in a narrow strip along the rostral bank of the central sulcus. Their experiments demonstrated that, even within this strip of tissue, discrete sites contained neurons with distinctive functions. Stimulation of adjacent sites evoked movements in adjacent body parts, starting with the foot, leg, and tail medially, and proceeding to the trunk, arm, hand, face, mouth, and tongue more laterally. When they lesioned a cortical site at which stimulation had evoked movements of a part of the body, motor control of that body part was perturbed or lost after the animal recovered from surgery. These early experiments showed that the motor strip con- tains an orderly motor map of the contralateral body and that the integrity of the motor map is necessary for voluntary control of the corresponding body parts. In the first half of the 20th century more focal elec- trical stimulation allowed the motor map to be defined in greater detail. Clinton Woolsey and his colleagues tested the functional organization of the motor cortex in several species of mammals, whereas Wilder Pen- field and co-workers tested discrete sites in human neurosurgical patients (Figure 37–1). Their findings
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Figure 37–2 Internal organization of the motor map of the arm in the motor cortex. A. The arm motor map in monkeys has a concentric, horse- shoe-shaped organization: Neurons that control the distal arm (digits and wrist) are concentrated in a central core (yellow) surrounded by neurons that control the proximal arm (elbow and shoulder; blue). The neuron populations that control the distal and proximal parts of the arm overlap extensively in a zone of proximal-distal cofacilitation (green). The arm motor representation is seen in its normal anatomical location in the anterior bank of the central sulcus (left), and also after flatten- ing and rotation to bring it into approximate alignment with the microstimulation maps in part B. (Reproduced, with permission, from Park et al. 2001.)
B. Microstimulation of several sites in the arm motor map can produce rotations of the same joint. Neurons that control wrist movements are concentrated in the central core whereas those that regulate shoulder movements are distributed around the core, with some overlap between the two populations. In these maps, the height of each peak is scaled to the inverse of the stimulation current: the higher the peak, the lower the current necessary to produce a response. The distribution and overlap of stimulation sites that evoke contractions of muscles in the shoulder (deltoid) and wrist (extensor carpi radialis) are even more extensive than that of sites for joint rotations. The yellow, green, and blue color zones on these maps correspond only approximately to the functional zones identified in the motor map of part A. (Reproduced, with permission, from Humphrey and Tanji 1991.)
Chapter 37 / Voluntary Movement: The Primary Motor Cortex 839
The final stage, execution of the chosen motor plan, also appears to be serial in nature. It has often been modeled as a series of sensorimotor transforma- tions of representations of a movement into different coordinate frameworks, progressing from a general description of the overall form of the movement to increasingly specific details, culminating in patterns of muscle activity (Figure 37–3B). According to this serial scheme, each sequential operation is encoded by a different neuronal popu- lation. Each population encodes specific features or parameters of the intended movement in a particular coordinate system, such as the direction of movement of the hand through space or the patterns of muscle contractions and forces. These several populations are connected serially and only the last population in the chain projects to the spinal cord. As we shall see in this and the next chapter, this model has some heuristic value for describing how the brain is organized to control voluntary movement,
Many Cortical Areas Contribute to the Control
of Voluntary Movements
Voluntary Motor Control Appears to Require Serial Processing
Much of what we do in everyday life involves a sequence of actions. One normally does not take a shower after getting dressed or put cake ingredients into the oven to bake before blending them into a batter. It seems logical that most brain functions are also serial. Largely on the basis of indirect psychological stud- ies, the neural processes by which the brain controls voluntary behavior are commonly divided into three sequential stages. First, perceptual mechanisms generate a unified sensory representation of the external world and the individual within it. Next, cognitive processes use this internal replica of the world to decide on a course of action. Finally, the selected motor plan is relayed to action systems for implementation (Figure 37–3A).
Stimulus Perception Cognition (^) Action Response
Extrinsic Intention kinematics Kinetics Response
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Figure 37–3 Cortical control of voluntary behavior appears to be organized in a hierarchical series of operations. A. The brain’s control of voluntary behavior has often been divided into three main operational stages, in which perception generates an internal neuronal image of the world, cognition analyzes and reflects on this image to decide what to do, and the final decision is relayed to action systems for execution. However, this three-stage serial organization was largely based on introspective psychological studies rather than on direct neurophysiological study of neural mechanisms. B. Each of the three main operational stages is presumed to involve its own serial processes. For example, the “action” stage that converts an intention into a physical movement is
often presumed to involve a hierarchy of operations that trans- form a general plan into progressively more detailed instruc- tions about its implementation. The model shown here, inspired by early controller designs for multijoint robots, suggests that the brain plans a chosen reaching movement by first calculating the extrinsic kinematics of the movement (eg, target location, trajectory of hand displacement from the starting location to the target location), then calculating the required intrinsic kinematics (eg, joint rotations) and finally the causal kinetics or dynamics of movement (eg, forces, torques, and muscle activ- ity). (See also Figure 33–2.)
Chapter 37 / Voluntary Movement: The Primary Motor Cortex 841
The Anatomical Connections of the Precentral Motor Areas Do Not Validate a Strictly Serial Organization
To understand the roles of these multiple precentral motor areas in voluntary motor control, it is important to know their connections with one another, their con- nections with other cortical areas, and their descend- ing projections. The cortical motor areas are interconnected by complex patterns of reciprocal, convergent, and diver- gent projections rather than simple serial pathways. The supplementary motor area, dorsal premotor cor- tex, and ventral premotor cortex have somatotopically organized reciprocal connections not only with the primary motor cortex but also with each other. The primary motor cortex and supplementary motor area receive somatotopically organized input from the pri- mary somatosensory cortex and the rostral parietal cor- tex, whereas the dorsal and ventral premotor areas are reciprocally connected with progressively more caudal, medial, and lateral parts of the parietal cortex. These somatosensory and parietal inputs provide the pri- mary motor cortex and caudal premotor regions with sensory information to organize and guide motor acts. In contrast, the pre-supplementary and pre-dorsal premotor areas do not project to the primary motor cor- tex and are only weakly connected with the parietal lobe. They receive higher-order cognitive information through reciprocal connections with the prefrontal cortex and so may impose more arbitrary context-dependent control over voluntary behavior. Several cortical motor regions project in multiple parallel tracts to subcortical areas of the brain as well as the spinal cord. The best studied output path is the pyramidal tract, which originates in cortical layer V in a number of precentral and parietal cortical areas. Precentral areas include not only primary motor cor- tex but also the supplementary motor and dorsal and ventral premotor areas. The pre-supplementary motor and pre-dorsal premotor areas do not send axons to the spinal cord; their descending output reaches the spinal cord indirectly through projections to other subcorti- cal structures. Parietal areas that contribute descend- ing axons to the pyramidal tract include the primary somatosensory cortex and adjacent rostral parts of the superior and inferior parietal lobules. Many pyramidal tract axons decussate at the pyra- mid and project to the spinal cord itself, forming the corticospinal tract (Figure 37–5A). Because several cor- tical areas contribute axons to the corticospinal tract, the traditional view that the primary motor cortex is the “final common path” from the cerebral cortex to the
his colleagues discovered that movements of the con- tralateral body can be evoked not only by electrical stimulation of the primary motor cortex, but also by stimulating a second region in a part of the premotor cortex on the medial surface of the cerebral hemisphere now known as the supplementary motor area (Figure 37–4B). The motor map of different body parts evoked by stimulation of the supplementary motor area is less detailed than that of the primary motor cortex and lacks the enlarged distal arm and hand representa- tion seen in the primary motor cortex. Stimulation of the supplementary motor area can evoke movements on both sides of the body or halt ongoing voluntary movements, effects that rarely result from stimulation of the primary motor cortex. Anatomical and functional studies in humans and nonhuman primates over the past 25 years have radi- cally changed the view of how the precentral cortex is organized functionally. First, architectonic studies demonstrated that Brodmann’s area 6 is not homoge- neous but consists of several distinct subareas. Second, these subareas have specific connections among them- selves and with the rest of the cerebral cortex. Third, functional studies found that each subarea separately controls movements of some or all parts of the body and that the properties of neurons in each subarea dif- fer in important ways. These areas are identified by two different nomenclatures in the literature. As a result, in current maps of the precentral cor- tex Brodmann’s area 6 is usually divided into five or six functional areas in addition to the primary motor cortex (or area F1) in Brodmann’s area 4 (Figure 37–4B). The clas- sical supplementary motor area originally identified by Woolsey on the medial cortical surface is now split into two functional regions. The more caudal part is called the supplementary motor area proper (area F3), whereas the more rostral part is the pre-supplementary motor area (F6). The caudal and rostral parts of the dorsal convexity of area 6 are called the dorsal premotor cortex (F2) and pre- dorsal premotor cortex (F7), respectively. The ventral con- vexity of Brodmann’s area 6 has also been identified as a separate functional area called the ventral premotor cortex , and has been further subdivided into two subareas called F4 and F5 (Figure 37–4B). Finally, three additional motor areas outside Brodmann’s area 6, in the rostral cin- gulate cortex, have been delineated recently. The multiplicity of cortical motor areas would seem redundant if their only role was to initiate or coordinate muscle activity. However, we now know that neurons in these areas have unique properties and interact to perform diverse operations that select, plan, and generate actions appropriate to external and inter- nal needs and context.
842 Part VI / Movement
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Primary motor cortex Supplementary motor area Cingulate motor areas
Figure 37–5 Cortical origins of the corticospinal tract. (Reproduced, with permission, from Dum and Strick 2002.) A. Neurons that modulate muscle activity in the contralateral arm and hand originate in the primary motor cortex (M1) and many subdivisions of the premotor cortex (PMd, PMv, SMA) and project their axons into the spinal cord cervical enlarge- ment. Corticospinal fibers projecting to the leg, trunk, and other somatotopic parts of the brain stem and spinal motor system originate in the other parts of the motor and premotor cortex. (M1, primary motor cortex; SMA, supplementary motor area; PMd, dorsal premotor cortex; PMv, ventral premotor cortex; CMAd, dorsal cingulate motor area; CMAv, ventral cingulate motor area; CMAr, rostral cingulate motor area.)
B. The axons of corticospinal fibers from the primary motor cortex, supplementary motor area, and cingulate motor areas terminate on interneuronal networks in the intermediate laminae (VI, VII, and VIII) of the spinal cord. Only the primary motor cortex contains neurons whose axons terminate directly on spinal motor neurons in the most ventral and lateral part of the spinal ventral horn. Rexed’s laminae I to IX of the dorsal and ventral horns are shown in faint outline. The dense cluster of labeled axons adjacent to the dorsal horn (upper left) in each section are the corticospinal axons descending in the dorso- lateral funiculus, before entering the spinal intermediate and ventral laminae.
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Figure 37–6 Corticomotoneurons activate complex muscle patterns through divergent connections with spinal motor neurons that innervate different arm muscles. A. Corticomotoneurons, which project monosynaptically to spinal motor neurons, are located almost exclusively in the cau- dal part of the primary motor cortex (M1), within the anterior bank of the central sulcus. The corticomotoneurons that control a single hand muscle are widely distributed throughout the arm motor map, and there is extensive overlap of the distribution of neurons projecting to different hand muscles. The distributions of the cell bodies of corticomotoneurons that project to the spinal motor neuron pools that innervate the adductor pollicis, abductor pollicis longus, and extensor digitorum communis (shown on the right), illustrate this pattern. (R, rostral; M medial.) (Reproduced, with permission, from Rathelot and Strick 2006.) B. A single corticomotoneuron axon terminal is shown arborized in the ventral horn of one segment of the spinal cord.
It forms synapses with the spinal motor neuron pools of four different intrinsic hand muscles (yellow and blue zones) as well as with surrounding interneuronal networks. Each axon has several such terminal arborizations distributed along several spinal segments. (Reproduced, with permission, from Shinoda, Yokata, and Futami 1981.) C. Different colonies of corticomotoneurons in the primary motor cortex terminate on different combinations of spinal interneuron networks and spinal motor neuron pools, thus activating different combinations of agonist and antagonist muscles. Many other corticospinal axons terminate only on spinal interneurons (not shown). The figure shows corticomo- toneuronal projections largely onto extensor motor neuron pools. Flexor motor pools receive similar complex projections (not shown). (Modified, with permission, from Cheney, Fetz, and Palmer 1985.)
Chapter 37 / Voluntary Movement: The Primary Motor Cortex 845
Box 37–1 Lesion Studies of Voluntary Motor Control
Naturally occurring or experimentally induced lesions have long been used to infer the roles of different neu- ral structures in motor control. However, the effects of lesions must always be interpreted with caution. It is often incorrect to conclude that the function perturbed by an insult to a part of the motor system resides uniquely in the damaged structure, or that the injured neurons explicitly perform that function. Fur- thermore, the effects of lesions can be masked or altered by compensatory mechanisms in remaining, intact structures. Nevertheless, lesion experiments have been fundamental in differentiating the functional roles of cortical motor areas as well as the pyramidal tract. Focal lesions of the primary motor cortex typically result in such symptoms as muscle weakness, slowing and imprecision of movements, and discoordination of multijoint motions, perhaps as a result of selective per- turbations of the control circuitry for specific muscles (Figure 37–7). Larger lesions lead to temporary or per- manent paralysis. If the lesion is limited to a part of the motor map, the paralysis affects primarily the movements repre- sented in that sector, such as the contralateral arm, leg, or face. There is diminished use of the affected body parts, and movements of the distal extremities are much more affected than those of the proximal arm and trunk. The severity of the deficit as a result of focal lesions also depends on the degree of required skill. Control of fine motor skills, such as independent movements of the fingers and hand and precision grip, is abolished. Any residual control of the fingers and the hand is usually reduced to clumsy, claw-like, synchronous flexion and extension motions of all fingers, not unlike the unskilled grasps of young infants. Even remaining motor func- tions, such as postural activity, locomotion, reaching, and grasping objects with the whole hand, are often clumsy and lack refinement. Large lesions of the motor cortex or its descend- ing pathways (for example the internal capsule) often produce a suite of symptoms known as the pyramidal syndrome (Figure 37–8). This condition is characterized by contralateral paralysis; increase of muscular tone (spasticity), often preceded by a transient phase of flac- cid paralysis with decreased muscle tone; increase of deep reflexes (such as the patellar reflex); disappearance of superficial reflexes (such as the abdominal reflex); and appearance of the Babinski reflex (dorsiflexion of the great toe and fanning of the other toes when a blunt needle is drawn along the lateral edge of the sole). The increase in muscle tone alters the patient’s posture, such
that the arm contralateral to the lesion is flexed and adducted whereas the leg is extended. The term “pyramidal syndrome” is a misnomer. In fact, the symptoms result from lesions of descending cortical projections to several subcortical sites, not just the pyramidal tract. Spasticity, for instance, results from damage to nonpyramidal fibers, specifically those that innervate the brain stem centers involved in the control of muscular tone. Clear evidence for this comes from observation of the behavior of monkeys following surgi- cal transection of the medullary pyramid, an anatomi- cal structure that contains only pyramidal tract fibers. Transection at this level produces contralateral hypo- tonia rather than spasticity. Lesions of the primary motor cortex in humans perturb the dexterous execution of movements, with deficits ranging from weakness and discoordination to complete paralysis. Lesions of other cortical regions, in contrast, do not result in paralysis and have less impact on the execution of movements than on the organization of action. One effect is difficulty in suppressing the natu- ral motor response to a stimulus in favor of other actions that would be more appropriate to accomplish a goal. For example, when a normal monkey sees a tasty food treat behind a small transparent barrier, it read- ily reaches around the barrier to grasp it. However, after a large premotor cortex lesion the monkey persist- ently tries to reach directly toward the treat rather than making a detour around the barrier, and thus repeatedly strikes the barrier with its hand. Focal lesions of premotor areas cause a variety of more selective deficits that do not result from an inabil- ity to perform individual actions but rather an inability to choose the appropriate course of action. Lesions or inactivation of the ventral premotor cortex perturb the ability to use visual information about an object to shape the hand appropriately for the object’s size, shape, and orientation before grasping it. Lesions of the dorsal pre- motor cortex or supplementary motor area impact the ability to learn and recall arbitrary sensorimotor map- pings such as visuomotor rotations, conditional stim- ulus-response associations, and temporal sequences of movement. The effects of motor cortex lesions also differ across species. Large lesions in cats do not cause paralysis; the animals can move and walk on a flat surface. However, they have severe difficulties using visual information to navigate within a complex environment, avoid obstacles, or climb the rungs of a ladder. Trevor Drew and col-
(continued)
Chapter 37 / Voluntary Movement: The Primary Motor Cortex 847
A Normal B After sectioning of pyramidal tract fibers
Figure 37–8 A lesion of the pyramidal tract abol- ishes fine grasping movements. A. A monkey is normally able to make individuated movements of the wrist, fingers, and thumb in order to pick up food in a small well. B. After bilateral sectioning of the pyramidal tract the monkey can remove the food only by grabbing it clumsily with the whole hand. This change results mainly from the loss of direct inputs from corticomo- toneurons onto spinal motor neurons. A pyramidal tract transection is not equivalent to a motor cortex lesion, however, because not all pyramidal tract axons terminate in the spinal cord. The axons that do project to the spinal cord originate in several cortical areas, including the motor cortex, and the corticospinal tract is only one of several parallel output pathways of the motor cortex. (Reproduced, with permission, from Lawrence and Kuypers 1968.)
leagues have shown that pyramidal tract neurons in the motor cortex of cats are much more strongly activated when the cats must modify their normal stepping to clear an obstacle under visual guidance than during normal, unimpeded locomotion over a flat, featureless surface. Similar lesions of motor cortex in monkeys have more drastic consequences, including initial paralysis and usually the permanent loss of independent, frac- tionated movements of the thumb and fingers. Mon- keys nevertheless recover some ability to make clumsy
movements of the hands and arms and to walk and climb, even after large lesions (Figure 37–8). In humans large lesions of the motor cortex are particularly devas- tating, often resulting in flaccid or spastic paralysis with a limited potential for recovery. These differences in primates and man presumably reflect the increased importance in man of descend- ing signals from motor cortex and a correspondingly diminished capacity of subcortical motor structures to compensate for the loss of those descending signals.
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Figure 37–9 The discharge of individual pyramidal tract neurons varies with particular movements of specific parts of the body. The discharge of a motor cortex neuron with an axon that projects down the pyramidal tract is recorded while a monkey makes a sequence of flexion and extension movements of the wrist. The three parts of the figure show three consecu- tive flexion-extension cycles, proceeding from top to bottom. In the trace showing wrist position the direction of flexion is down and extension up. The pyramidal tract neuron discharges before and during extensions and is reciprocally silent during flexion movements. It does not discharge during movements of other body parts. Other motor cortex neurons show the opposite pattern of activity, discharging before and during flexion move- ments. (Reproduced, with permission, from Evarts 1968.)
joint and are reciprocally suppressed during exten- sion, whereas other cells display the opposite pattern. This movement-related activity typically begins 50 to 150 ms before the onset of agonist muscle activity. These pioneering studies suggested that single neurons in primary motor cortex generate signals that provide specific information about movements of specific parts of the body before those movements are executed. Many subsequent studies have provided further insight into the contribution of different cortical motor areas to the control of voluntary movements. In general, the output signals from premotor areas are strongly dependent on the context in which the action is per- formed, such as the stimulus-response associations and the rules that guide which movement to make. In con- trast, the commands generated by the primary motor cortex are more closely related to the mechanical details of the movement and are usually less influenced by the behavioral context. However, the relative role of these different areas to voluntary motor control, including the primary motor cortex itself, continues to be an area of active research and controversy. The rest of this chap- ter and Chapter 38 describe our current understanding of the different roles of cortical motor areas.
Columnar arrays of neurons with similar response properties are a prominent feature of many sensory areas of cortex. It is surprising therefore that there is only weak evidence for such functional columns in the primary motor cortex. The cell bodies and apical dendrites of primary motor cortex neurons tend to form radially oriented columns. The terminal arbors of thalamocortical and corticocortical axons form localized columns or bands and corticomotoneurons tend to cluster in small groups with similar muscle fields. Motor cortex neurons recorded successively as a microelectrode descends perpendicularly through the neuronal layers between the pial surface and the white matter typically discharge during movements of the same part of body and can have similar preferred movement directions. Nevertheless, adjacent cells often show very different response patterns.
Motor Commands Are Population Codes
The complex overlapping organization of the motor map for the arm and hand suggests at least two differ- ent ways to generate the motor command for a given movement. The map could function as a look-up table
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The Motor Cortex Encodes Both the Kinematics and Kinetics of Movement
Population-vector analyses show that neural activ- ity in the primary motor cortex contains information about the trajectory of hand motions during reaching and drawing movements. However, to execute those movements the motor system must implement the desired motions by generating particular patterns of muscle activity. Electrical stimulation of the primary motor cortex readily evokes muscle contractions, and some cells in this region have direct access to spinal motor neu- rons. Indeed, it was long assumed that the major role of the primary motor cortex was to specify the muscle activity that generates voluntary movements. Because muscle contractions generate the forces that displace a joint or limb in a particular direction, a critical question is whether primary motor cortex neurons signal the desired spatiotemporal form of a behavior or the forces and muscle activity required to generate the move- ment. That is, do these neurons encode the kinematics or the kinetics of an intended movement (Box 37–2)? Kinematics refers to the parameters that describe the spatiotemporal form of movement, such as direc- tion, amplitude, speed, and path. Kinetics concerns the causal forces and muscle activity. It is also useful to distinguish the dynamic forces that cause movements from the static forces required to maintain a given pos- ture against constant external forces such as gravity. Evarts was the first to address this question with single-neuron recordings. Using a system of pulleys and weights, he applied a load to the wrist of a monkey to pull the wrist in the direction of flexion or extension. To make a particular movement the animal had to alter its level of muscle activity to compensate for the load. As a result, the kinematics (direction and amplitude) of wrist movements remained constant but the kinetics (forces and muscle activity) changed with the load. The activity of many primary motor cortex neurons associ- ated with movements of the hand and wrist increased during movements in their preferred direction when the load opposed that movement but decreased when the load assisted it (Figure 37–12). These changes in neural activity paralleled the changes in muscle activ- ity required to compensate for the external loads. This was the first study to show that the activity of many primary motor cortex neurons is more closely related to how a movement is performed, the kinetics of motion, than to what movement is performed, the correspond- ing kinematics. A later study confirmed this property of motor cor- tex activity during whole-arm reaching movements.
All directions were represented in the neuronal pop- ulation. Cells with similar preferred directions were located at several different sites in the arm motor map, and nearby cells often had different preferred direc- tions. As a result, many cells with a broad range of pre- ferred directions discharged at different intensities at many locations across the arm motor map during each reaching movement. Despite the apparent complexity of the response properties of single neurons, Georgopoulos found that the global pattern of activity of the entire population provided a clear signal for each movement. He repre- sented each cell’s activity by a vector pointing in the cell’s preferred direction. The vector’s length for each direction of movement was proportional to the mean level of activity of that cell averaged over the duration of the movement (Figure 37–10B). This vectorial repre- sentation implied that an increase of activity of a given cell is a signal that the arm should move in the cell’s pre- ferred direction, and that the strength of this directional influence varies continuously for different reach direc- tions as a function of the neuron’s directional tuning. Vectorial addition of all of the single-cell contribu- tions to each output command produces a population vector that corresponds closely to the actual movement direction. That is, an unambiguous signal about the desired motor output is encoded by the summed activ- ity of a large population of active neurons throughout the arm motor map in the primary motor cortex. As a result, neurons in all parts of the arm motor map con- tribute to the motor command for each reaching move- ment, and the pattern of activity across the motor map changes continuously as a function of the intended direction of the reaching movement. Andrew Schwartz and colleagues used the same population-vector analysis to represent temporal variations in the activity of populations of primary motor cortex neurons every 25 ms while monkeys performed continuous arm movements. In the result- ing time sequence of population vectors, each vector predicts the instantaneous direction and speed of the motion of the monkey’s arm approximately 100 ms later (Figure 37–11). These results show that the pat- tern of neural activity distributed across the arm motor map varies continuously in time during complex arm movements, signaling the moment-to-moment details of the desired movement. Further studies have confirmed that similar population-coding mechanisms are used in all cor- tical motor areas. This common coding mechanism undoubtedly facilitates the communication of move- ment-related information between the multiple areas of motor cortex during voluntary behavior.
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of many motor cortex neurons changed systematically with the direction of the external load even though the movement path did not change. When the load opposed the direction of reach, the single-cell and total population activity increased. When the load assisted the reaching direction, the neural activity decreased
A monkey made arm movements exactly as in the task used by Georgopoulos (Figure 37–10), but additional external loads pulled the arm in different directions. To continue to move the arm along the same path, the monkey had to change the activity of its arm muscles to counteract the external loads. The level of activity
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A Finger trajectories
B Temporal sequence of movement vectors
C Predicted trajectories made by joining instantaneous population vectors from part B tip to tail
Figure 37–11 The moment-to-moment activity of a population of motor cortex neurons predicts arm movements over time. (Reproduced, with permission, from Moran and Schwartz 1999.) A. A monkey uses its arm to trace spirals with its finger. B. Temporal sequences of vectors, reading left to right, illustrate the instantaneous direction and speed of move- ment of the finger (Mov) and the net population vector signal (Pop) of the activity of 241 motor cortex neurons every 25 ms during the drawing movements. The popula- tion vectors precede the hand displacement vectors by approximately 100 ms. C. Joining the instantaneous population vectors tip to tail produces “neural trajectories” that predict the spatial trajectory of movement of the finger along the spiral path approximately 100 ms in the future.
Chapter 37 / Voluntary Movement: The Primary Motor Cortex 853
Flexors
Extensors Neuron
B Load opposes flexors
Flexors
Extensors Neuron
C Load assists flexors
Flexors Extensors Neuron
Recording from neuron in wrist area of M
Restraint
Potentiometer measures wrist angle
Weight opposes flexors
Pulley
Flexion
Extension
Weight assists flexors
Lever position
A No load
Figure 37–12 Activity of a motor cortex neuron correlates with changes in the direction and amplitude of muscle forces during wrist movements. The records are from a primary motor cortex (M1) neuron with an axon that projected down the pyramidal tract. The monkey flexes its wrist under three load conditions. When no load is applied to the wrist, the neuron fires before and during flexion (A). When a load oppos- ing flexion is applied, the activity of the flexor muscles and the
neuron increases (B). When a load assisting wrist flexion is applied, the flexor muscles and neuron fall silent (C). In all three conditions the wrist displacement is the same, but the neuronal activity changes as the loads and compensatory muscle activity change. Thus the activity of this motor cortex neuron is better related to the direction and level of forces and muscle activ- ity exerted during the movement than to the direction of wrist displacement. (Reproduced, with permission, from Evarts 1968.)
854 Part VI / Movement
muscles of the distal arm, hand, and fingers. This arrangement allows the primary motor cortex to regu- late the activity of those muscles directly, in contrast to its indirect regulation of muscles through the reflex and pattern-generating functions of the spinal circuits. It also provides primates and humans with a greatly enhanced capacity for individuated control of hand and finger movements. Large lesions of the primary motor cortex permanently destroy this capacity. Although monkeys and humans can make isolated movements of the thumb and fingers, most hand and finger actions involve combinations of stereotypical hand and finger configurations and coordinated wrist and digit movements. This has led to the hypothesis that separate cortical circuits selectively control these different stereotypical hand actions, and that the pri- mary motor cortex converts these signals into more specific motor commands (see Chapter 38). The anatomy of the muscles of the wrist and fin- gers further complicates the commands for individu- ated finger and hand movements. Several muscles have long, bifurcating tendons that act across several joints and even act on several fingers rather than just one. As a consequence, individuated control of hand
However, the experimental evidence suggests that a strictly serial model is too simplistic. The response prop- erties of primary motor cortex neurons are not homo- geneous. Signals about both the desired kinematics and required kinetics of movements may be generated simul- taneously in different, or possibly even overlapping, pop- ulations of primary motor cortex neurons. Rather than representing only what movement to make (kinematics) or how to make it (kinetics), the true role of the motor cortex may be to perform the transformation between these two representations of voluntary movements. Delineating the movement-related information encoded in motor cortex activity is increasingly impor- tant for the development of brain-controlled interfaces and neuroprosthetic controllers that allow patients with severe motor deficits to control remote devices such as a computer cursor, a wheelchair, or a robotic limb by neural activity alone (Box 37–3).
Hand and Finger Movements Are Directly Controlled by the Motor Cortex
The monosynaptic projection from the primary motor cortex onto spinal motor neurons is most dense for
A Reaching leftward B Reaching rightward
Figure 37–13 Activity of primary motor cortex neurons varies with the forces required to maintain the direction of reaching movements against external loads. A vectorial representation of the directional activity of approximately 260 motor cortex neurons (black lines) when a monkey makes reaching movements to the left and right. The vectors in the center represent activity when no external load is applied to the arm, whereas the vector clusters around the center represent the activity of the same 260 neurons when an external load pulls the arm in different directions. The location of each vector
cluster relative to the central cluster corresponds to the direc- tion in which the external load pulls on the arm. The change in population vectors (blue arrows) for the vector clusters around the center indicates that the strength and overall directional bias of the activity of the neural population vary systematically with the direction of the external load, in order to counteract its effect, even though the trajectory of the movement does not change. (Reproduced, with permission, from Kalaska et al. 1989.)
