Cognitive Functions of the Premotor Systems
The Four Premotor Areas of the Primate Brain Also Have Direct Connections in the Spinal Cord
Motor Circuits Involved in Voluntary Actions Are Organized to Achieve Specific Goals
The Hand Has a Critical Role in Primate Behavior
The Joint Activity of Neurons in the Parietal and Premotor Cortex Encodes Potential Motor Acts
Some Neurons Encode the Possibilities for Interaction with an Object
Potential Motor Acts Are Suppressed or Released by Motor Planning Centers
IN CHAPTER 18 WE SURVEYED the higher-order organization of sensory systems. In this chapter we turn to the higher-order functioning of the motor systems, by examining how the brain represents behavioral goals and how voluntary actions are planned to achieve those goals. To illustrate how the motor systems generate goal-oriented behavior, we focus on reaching and grasping, actions that are possible because of the prehensile hand.
The evolution of the prehensile hand greatly enriched the development of cognitive capacities in primates. Indeed, the two are interdependent. As the German philosopher Friedrich Engels wrote: “Man alone has succeeded in impressing his stamp on nature. He has accomplished this primarily and essentially by means of the hand. But step by step with the development of the hand went that of the brain.”
The prehensile hand radically changed the way in which primates relate to the external world; but the change occurred slowly, and required the evolution of cortical circuits for a variety of new specialized movements adapted to different objects. In his book The Sensory Hand, Vernon Mountcastle, one of the pioneers in the study of the connection between sensation and action, quotes Herbert Spencer (Principles of Psychology, 1885) on why the hand is so critical to understanding action:
All that we need notice here is the extent to which in the human race a perfect tactual apparatus subserves the highest processes of the intellect. I do not mean merely that the tangible attributes of things rendered completely cognisable by the complex adjustments of the human hands, and the accompanying manipulative powers have made possible those populous societies in which alone a wide intelligence can be evolved. I mean the most far-reaching cognitions, and inferences (even those) most remote from perception, have their roots in the … impression which the human hands can receive.
The final neural pathway for all bodily actions, including movement of the hand, is through motor neurons in the ventral horn of the spinal cord. These motor neurons are not simply responding to independently generated sensory information, however. The sensory information needed for action is the product of interaction between the motor systems and sensory systems. Under many circumstances, therefore, action and perception are inseparable. Indeed, many sensory functions serve only to allow for the planning of motor acts. As we focus on and reach for a cup of coffee, our arm is controlled in a manner that is independent of conscious experience—we do not think about which movements to perform and which muscles to contract.
Perception of space, and even more complex cognitive acts, were once thought to be represented only in higher-order sensory and association areas of cerebral cortex. In a radical departure from previous thinking, we now believe that the premotor areas in the cortex may also have cognitive functions.
At the highest levels of sensory-motor interaction, neurons do not simply encode the physical features of the sensory stimulus or the force or direction of movement. Rather, they encode something more abstract that includes features of both the object and the movement: They encode the relationship between the body and the object with respect to a particular goal. For example, in anticipation of drinking they may represent a configuration of the hand in relation to graspable features of a cup.
Direct Connections Between the Cerebral Cortex and Spinal Cord Play a Fundamental Role in the Organization of Voluntary Movements
Although picking up a cup appears to be a simple mechanical action, the neural machinery underlying it is surprisingly complex, requiring a number of preparatory steps in the parietal and frontal premotor and motor cortex.
As discussed in Chapter 1, the discovery that electrical stimulation of different parts of the frontal lobe produces movements of the opposite side of the body had a major effect on thinking about localization of function in the brain. Brodmann’s area 4, the area in the frontal lobe in which the lowest-intensity stimulation elicited movement, was designated the primary motor cortex (Figure 19-1). By systematically stimulating the primary motor cortex and attributing the movement elicited with each stimulus to the activation of neurons near the electrodes, researchers identified groups of neurons that controlled movement of specific body parts and learned that these functional groups were distributed on the cortex in the form of a somatotopic map.
Figure 19-1 The cortical motor areas. The cortical motor areas lie largely in Brodmann’s area 4 and area 6. Area 6 includes the supplementary motor area located largely on the medial brain surface, and the dorsal and ventral premotor areas located on the lateral surface. Area 4 includes the face, arm, and leg representations of the primary motor cortex. Additional motor areas are located in and around the banks of the cingulate sulcus.
In recent years our understanding of the functional organization of the motor areas of the cerebral cortex has changed dramatically, and a new picture of the cortical control of movement is emerging. The functional organization of the primary motor cortex is not simply an isomorphic map of the body in which adjacent peripheral sites are represented in adjacent cortical sites. Instead, individual muscles and joints are represented in the cortex multiple times in a complex mosaic. This makes it possible for the cortex to organize combinations of elemental movements suitable to specific tasks.
Each muscle and joint is represented by a column of neurons whose axons branch and terminate in several functionally related spinal motor nuclei (this branching is minimal for cortical cells that control distal muscles because these muscles require more independent control). The cortical neurons also form synapses with interneurons in the spinal cord. These connections allow voluntary movements to switch on entire spinal circuits—the motor neurons, interneurons, and central pattern generators that execute reflex actions. These circuits are then able to integrate and convert local sensory input to motor output without further direction from cortical centers.
In the 1930s physiologists discovered that movement could also be elicited by stimulation of premotor areas. Brodmann’s area 6 contains four main premotor areas that project directly to the spinal cord. Two areas lie on the lateral surface and two on the medial surface in Brodmann’s area 6 (Figure 19-1.) Each of these four cortical areas may be viewed as a relay in a densely interconnected network that controls reaching and grasping by activating spinal motor circuits.
In contrast to neurons in the primary motor cortex, movement-related neurons in the premotor areas fire in connection with a variety of movements because these neurons encode a general goal-directed command such as “grasp the cup” or “pick up the raisin.” Neurons called set-related neurons, common in premotor areas but relatively rare in the primary motor cortex, are more active in the absence of any overt behavior, such as during the delay between a behavioral cue and the behavior. Other neurons encode global sensorimotor transformations, such as “always move at 180 degrees from the visual stimulus.” Thus, just as there is a hierarchy of spinal and supraspinal motor control, there is a hierarchy of representations of movement features within the different motor and premotor areas of the cortex.
To produce movement, signals from premotor and motor areas of the cortex must ultimately reach motor neurons in the spinal cord. The Dutch anatomist Hans Kuypers identified three motor pathways: a direct corticospinal pathway and two indirect pathways, the medial and lateral brain stem systems (Figure 19-2).
Figure 19-2 Direct and indirect motor pathways to the spinal cord. In the lateral view of the human brain; numbered areas are functional areas identified by Brodmann. The transverse section of the spinal cord shows three functional areas. The dorsal horn contains the sensory neurons of the spinal cord; the intermediate zone contains interneurons; and the motor nuclei zone contains the motor neurons that innervate the muscles.
A. The corticospinal tract, also called the pyramidal tract, originates in a vast region around the central sulcus that includes the parietal lobe and the posterior part of the frontal lobe (areas 4 and 6). Area 4, the primary motor cortex, is the only area of motor cortex that directly connects with spinal motor neurons. Area 6 comprises various subareas, most of which send fibers to interneurons in the intermediate zone of the spinal cord. The parietal lobe sends fibers to the dorsal horns.
B. Indirect pathways to spinal motor neurons originate in area 4 and area 6 and terminate in medial and lateral areas of the brain stem. The main components of the medial pathways are the reticulospinal, medial and lateral vestibulospinal, and tectospinal tracts; they descend in the ventral column and terminate in the ventromedial area of the spinal gray matter. The main lateral pathway is the rubrospinal tract, which originates in the magno-cellular portion of the red nucleus, descends in the contralateral dorsolateral column, and terminates in the dorsolateral area of the spinal gray matter.
The historically well-known corticospinal system is involved in the control of all aspects of body and limb movement but has a special role in the fractionated movements necessary for skilled motor acts such as playing the piano or typing. Much of the control of fractionated movements is exercised by the primary motor cortex. Thus, a lesion of the primary motor cortex destroys the ability to oppose the thumb and first finger so as to pick up a raisin or grasp a cup. A patient with such damage is unable to move the fingers independently and can only grasp a cup clumsily.
In humans the corticospinal tract consists of approximately one million axons, of which 30% to 40% originate from neurons in the primary motor cortex. The rest of the axons have their origins mainly in the premotor and supplementary motor cortices, and in the parietal areas lying posterior to the precentral sulcus. Together, corticospinal axons from these various areas descend through the subcortical white matter, internal capsule, and cerebral peduncle. As the fibers of the corticospinal tract descend they form the medullary pyramids, prominent protuberances on the ventral surface of the medulla. Consequently the entire projection is sometimes called the pyramidal tract. Like the ascending somatosensory system, most fibers of the descending corticospinal tract cross the midline in the medulla, at the pyramidal decussation, to terminate in the spinal cord of the opposite side.
The motor information carried in the corticospinal tract is significantly modulated by a continuous stream of information from other motor regions as well as tactile, visual, and proprioceptive information needed to make voluntary movement both accurate and properly sequenced.
The medial brain stem system originates in portions of the reticular formation, vestibular nuclei, and superior colliculus. This system receives information from the cortex and other motor centers for the control of posture and locomotion. The lateral brain stem system originates from the red nucleus. It receives input from the cortex as well but is involved in the control of arm and hand movements.
Spinal motor circuits are not regulated solely by descending commands. Reflex circuits and pattern generators within the spinal cord can coordinate stereotyped movements such as stepping without descending signals (see Chapter 35). A newborn infant, whose descending pathways cannot yet control the spinal cord, is able to execute stepping movements when lifted into the air. Descending systems coordinate reflex and patterned movements generated by spinal motor circuits and can even create new patterns of muscle activation through direct action on motor neurons. This cortical control enables greater flexibility of movements than is possible through exclusively local coordination among the spinal motor circuits.
The cortical motor areas and brain stem in turn receive input from two major subcortical structures: the cerebellum and basal ganglia (Figure 19-3, and see Figure 16-9). These two structures provide feedback essential for the smooth execution of skilled movements and thus are important for motor learning, the improvement in motor skills through practice. The cerebellum and the basal ganglia store memory for unconscious motor skills through pathways that are separate from those used to store factual memories of events that can be recalled consciously (see Chapter 66).
Figure 19-3 The major subcortical brain systems that initiate and control motor actions. Both the basal ganglia and cerebellum influence cortical motor circuits through connections in the thalamus. The motor cortex determines which muscle groups are activated and the magnitude of force to exert. Based on inputs from the motor cortex, basal ganglia, cerebellum, and other brain stem nuclei, the spinal cord initiates appropriate muscle contractions to accomplish purposeful movement.
The cerebellum receives somatosensory information directly from primary afferent fibers arising in the spinal cord as well as information about movement from corticospinal axons descending from the neocortex. The basal ganglia receive direct projections from much of the neocortex, which supply both sensory information and information about movement (see Figure 16-9).
The Four Premotor Areas of the Primate Brain Also Have Direct Connections in the Spinal Cord
In primates four functionally distinct premotor areas also send direct connections to the spinal cord (see Figure 19-1).
The two areas on the lateral surface are the lateral ventral premotor area and lateral dorsal premotor area. As we shall see later, the ventral premotor cortex mostly controls mouth and hand movements. Most of its neurons do not discharge in association with simple movements toward an object. They only become active during goal-directed actions such as grasping, holding, or manipulating an object. The two areas on the medial surface are the supplementary motor area, which lies in the medial wall of Brodmann’s area 6, and the cingulate motor areas, a group of motor areas buried in the cingulate sulcus. Similar premotor areas also exist in humans, but differences in size and sulcal patterns make it difficult to identify homologous areas with precision.
These four premotor areas are connected to the primary motor cortex. In addition, like the primary motor cortex, each premotor area has neurons that project to the brain stem as well as neurons that project directly to the spinal cord. Thus voluntary movements are controlled by descending signals from several cortical areas. For this reason, the task of generating limb movements is thought to be broken up into multiple subtasks, each managed in parallel by one of the several cortical motor areas.
These premotor areas also have dense reciprocal connections with the association areas in the posterior parietal cortex (Figure 19-4). These reciprocal connections constitute the visuomotor circuits that mediate different types of visually guided motor behavior such as mouth movements, arm reaching, and hand grasping.
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