BARR'S The Human Nervous System: An anatomical viewpoint, 9th Edition

PART 3 - Review of the Major Systems

Chapter 23

Motor Systems

Important Facts

• A motor unit comprises a group of extrafusal muscle fibers and the alpha motor neuron that innervates them. Gamma motor neurons supply the intrafusal fibers of muscle spindles. The term lower motor neuronis applied collectively to motor neurons.
• A lower motor neuron lesion (e.g., destruction of cell bodies or transection of axons in a ventral root or peripheral nerve) causes flaccid paralysis, loss of the stretch reflex, and considerable atrophy.
• The stretch reflex is normally largely suppressed by the activity of descending pathways that end on motor neurons and nearby interneurons.
• The major descending pathways are the vestibulospinal, reticulospinal, and corticospinal (pyramidal) tracts. The first of these is largely concerned with postural adjustments, and the last is concerned with voluntary movements. Most corticospinal fibers decussate at the caudal end of the medulla.
• An upper motor neuron lesion (e.g., transection of corticospinal and corticoreticular fibers in the internal capsule) causes spastic paralysis, with exaggerated stretch reflexes and the abnormal Babinski reflex. Atrophy is not a prominent feature except when there is prolonged disuse.
• Corticobulbar and other descending axons end in the motor nuclei of cranial nerves, bilaterally in many cases. Transection of these fibers in the internal capsule causes contralateral weakness of muscles of the lower half of the face and of the tongue but not elsewhere in the head.
• The outputs of the cerebellum and the basal ganglia are channeled through the ventral lateral and ventral anterior nuclei of the thalamus to the four motor areas of the cerebral cortex. The connections of the cerebellum are ordered such that each cerebellar hemisphere is concerned with ipsilateral muscles.
• Disorders of the cerebellum cause inaccuracies in the rate, range, direction, and force of movements. Disorders of the basal ganglia cause dyskinesias or abnormalities of movement, including chorea, dystonia, hemiballismus, and parkinsonism.

Except for some visceral functions, overt expression of activity in the central nervous system (CNS) depends on the somatic or skeletal musculature. The muscles are supplied by the motor neurons in the ventral horns of the spinal cord and in the motor nuclei of cranial nerves, with these neurons constituting what Sherrington termed the “final common pathway” for determining muscle action. They are collectively known as the lower motor neuron, especially in clinical medicine. Another clinical expression is upper motor neuron, which embraces all the descending pathways of the brain and spinal cord involved in the volitional control of the musculature.

Components of the brain responsible for the execution of properly coordinated movements include the cerebral cortex, corpus striatum, thalamus, subthalamic nucleus, red nucleus, substantia nigra, reticular formation, vestibular nuclei, inferior olivary complex, and cerebellum. The connections of these structures have been described elsewhere in this book, but here they are reviewed with particular attention to their influence on the lower motor neuron. Although descending pathways can be traced from the motor areas of the cerebral cortex to the motor neurons, it is important to realize that the prefrontal cortex and the association areas of the parietal lobe are also importantly involved in the motivation and planning stages of the formulation of motor commands by the brain.

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Lower Motor Neuron and Muscles

Skeletal muscles are supplied by motor neurons of two types, named alpha and gamma after the diameters of their axons. The large alpha motor neurons innervate the extrafusal fibers that constitute the main mass of the muscle, in which the axon of each neuron branches to supply the muscle fibers. The number supplied by a single neuron varies from fewer than 10 for small muscles whose contractions are precisely controlled to several hundred for large muscles that carry out strong but crude movements. An alpha motor neuron and the muscle fibers it supplies constitute a motor unit.

Different types of extrafusal muscle fiber are recognized on the basis of physiological and histochemical studies. The type I fibers contract slowly, are resistant to fatigue, and contain little stainable myofibrillar adenosine triphosphatase (ATPase). Type II fibers have faster contractions, are more rapidly fatigued than those of type I, and have high concentrations of ATPase in their myofibrils. Using other histochemical criteria, the type II muscle fibers are further divided into types IIA and IIB. All the muscle fibers in a motor unit are of the same type, and experimental evidence indicates that the type of fiber is determined by trophic influence of the innervating neuron. In addition to secreting acetylcholine to make the muscle fibers it supplies contract, a motor neuron provides trophic factors, which direct the differentiation of the muscle fibers and are necessary for their continued health. Proteins with myotrophic properties have been isolated from extracts of peripheral nerves.

CLINICAL NOTE

Lower Motor Neuron Lesions

The syndrome of a lower motor neuron lesion occurs when a muscle is paralyzed or weakened as a result of disease or injury that affects the cell bodies or axons of the innervating neurons.

Typical causes include poliomyelitis, in which a virus selectively attacks ventral horn cells or equivalent neurons in the brain stem andinjuries to peripheral nerves that transect some or all of the axons. The following clinical features are observed.

1. The muscle tone is reduced or absent (flaccid paresis or paralysis), owing to interruption of the efferent limb of the tonic stretch reflex.
2. The tendon-jerk reflexes are weak or absent. The cause is the same as that for flaccidity.
3. The muscles supplied by the affected neurons atrophy progressively. The atrophy is partly caused by loss of specific trophic factors normally provided by the motor nerve and partly to disuse.
4. Fibrillation potentials, caused by random contractions of individual denervated muscle fibers, can be detected by electromyography. Fibrillation should not be confused with fasciculation, which is visible twitching that occurs at irregular intervals within a muscle. Although seen in partly denervated muscles, fasciculation is a rather unreliable diagnostic sign because it is quite common in some normal muscles.
5. In a partly denervated muscle, the intact nerve fibers sprout at the nodes of Ranvier and at motor end plates, with some of the new axonal branches innervating denervated muscle fibers. These changes can be seen in a suitably stained biopsy specimen, and the enlargement of the motor units can be detected by electromyography. Fasciculations in partly denervated muscles are contractions of enlarged motor units.

Signs similar to those of a lower motor neuron lesion occur in diseases of muscle in which synaptic transmission at the motor end plate is impaired (myasthenia gravis) or in which the contractile elements function inadequately (various forms of dystrophy, myopathy, andmyositis). Biopsy and neurophysiological testing are used when a diagnosis cannot be made using clinical criteria.

The different types of muscle fiber respond differently to denervation: type IIB fibers atrophy most rapidly, and type I fibers atrophy most slowly.

Intrafusal muscle fibers supplied by gamma motor neurons control the length and tension

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of the neuromuscular spindles (see Chapter 3). The gamma motor neurons are much less numerous than the alpha motor neurons but are important because their patterns of firing determine the thresholds of the sensory nerve endings in the spindles. These endings are the receptors for the spinal stretch reflex, which is ordinarily suppressed as a result of activity in the descending tracts of the spinal cord. The muscle spindles are also receptors for the conscious awareness of position and movement.

Descending Pathways to the Spinal Cord

Motor neurons in the spinal cord are influenced by descending fibers from the cerebral cortex, central nuclei of the reticular formation, and lateral vestibular nucleus. Large tracts of fibers from these sites descend in the lateral and ventral funiculi of the spinal cord (see Fig. 5-9). Smaller contingents of descending fibers come from certain other nuclei in the brain stem.

CORTICOSPINAL TRACTS

The corticospinal tracts (Figs. 23-1 and 23-2) consist of the axons of cells in the frontal and parietal lobes. Motor corticospinal fibers arise in the primary motor, premotor, supplementary motor, and cingulate motor areas of the frontal lobe (see Chapter 15). Other corticospinal axons are from the first somatic sensory area in the parietal lobe; these probably do not have motor functions (see Chapter 15). The motor cortical areas have several other descending projections in addition to those to the spinal cord.

The organization of motor pathways (corticospinal and corticoreticulospinal) is both parallel, with axons descending from all the motor cortical areas, and hierarchical, with the primary motor cortex receiving association fibers from the other motor areas, which, in turn, receive input from the prefrontal, parietal, and temporal association cortex. Thus, the motor output of the cerebral cortex is influenced by interpreted sensory input so that movements can be guided by touch, vision, and other senses as well as being dictated by those activities of the forebrain that constitute thinking.

The corticospinal fibers pass through the cerebral white matter, converging as they enter the posterior limb of the internal capsule, which is the band of white matter between the lentiform nucleus and thalamus (see Chapter 16). This part of the internal capsule also contains fibers that descend from the cortex to the red nucleus, reticular formation, pontine nuclei, and inferior olivary complex, together with many thalamocortical, corticothalamic, and corticostriate fibers. As will be seen, all these populations of axons are involved in the control of movement.

The internal capsule continues into the basis pedunculi of the midbrain. At this level, some of the corticospinal axons give off branches that terminate in the red nucleus. The corticospinal fibers occupy the middle three fifths of the basis pedunculi, flanked by and partly intermingled with corticopontine fibers. On reaching the ventral (basal) portion of thepons, the corticospinal tract breaks up into fasciculi that pass caudally with the bundles of corticopontine fibers (see Figs. 7-8, 7-9, 7-10, 7-11, and 7-12). At this level, branches of some corticospinal axons enter and end in the central nuclei of the reticular formation.

At the caudal limit of the pons, the corticospinal axons reassemble to form, on the ventral surface of the medulla, the eminence known as the pyramid. The corticospinal fibers are therefore said to constitute the pyramidal tract. The term pyramidal system is applied to the corticospinal tracts together with the functionally equivalent corticobulbar(corticonuclear) fibers, which end in and near the motor nuclei of cranial nerves. At the caudal end of the medulla, in most people, about 85% of the corticospinal fibers cross the midline in the decussation of the pyramids (see Fig. 7-2) and enter the dorsal half of the lateral funiculus of the spinal cord, where they form the lateral corticospinal tract. The remaining 15% of the pyramidal fibers constitute the ventral corticospinal tract, which descends ipsilaterally in the medial part of the ventral funiculus. Most of the ventral corticospinal fibers decussate at segmental levels and end in the gray matter contralateral to their hemisphere of origin. (The relative sizes of the two corticospinal tracts are variable. In a few people, many of the fibers descend ipsilaterally in the ventral tract.)

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FIGURE 23-1 The pyramidal system. Corticobulbar and corticospinal neurons are shown in blue, and the motor neurons (“lower motor neuron”) are shown in red.

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FIGURE 23-2 Origins, courses, and terminal distributions of the major descending pathways concerned with the control of movement. The reticulospinal tracts indicated in green in the diagram represent a population of reticulospinal fibers present in the ventral and ventrolateral funiculi of the spinal white matter (see also Chapter 5). Corticospinal projections are red, and the vestibulospinal tract is blue. Columns of cell bodies of spinal motor neurons are indicated in yellow.

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CLINICAL NOTE

Selective Lesions of the Pyramidal Tract

There are about a dozen human case reports of medullary lesions confined to the pyramid. A contralateral flaccid hemiplegia was followed by recovery of most movements, with permanent clumsiness in movements of the fingers. The stretch reflexes were not abnormal. Neurosurgeons have cut through the middle part of the human basis pedunculi in attempts to relieve certain dyskinesias. The effects of this lesion are similar to those of truly selective transection of the pyramid. These observations and comparable experimental studies in monkeys indicate that the most important function of the pyramidal tract is to control the precision and speed of skilled movements. The Babinski sign or response (described later in connection with upper motor neuron lesions) is probably due to transection of corticospinal fibers, but spasticity and other “upper motor neuron lesion” features are not so easily explained.

Within the spinal gray matter, most corticospinal axons terminate in the intermediate gray matter and the ventral horn. A minority synapse directly with the dendrites or cell bodies of motor neurons. Most corticospinal fibers are able to influence motor neurons only through the mediation of interneurons in the spinal gray matter. The corticospinal fibers that originate in the first somesthetic area of the parietal lobe end in the dorsal horn. These are not motor in function but instead modulate the transmission of data through the somesthetic pathways (see Chapter 19).

RETICULOSPINAL TRACTS

Reticulospinal fibers are present throughout the ventral funiculus and the ventral half of the lateral funiculus of the spinal white matter. Most are the axons of cells in the central group of nuclei of the reticular formation: the oral and caudal pontine reticular nuclei and the gigantocellular reticular nucleus of the medulla, mainly ipsilaterally. Many reticulospinal fibers shift from the ventral into the lateral funiculus as they descend. In humans, the fibers of pontine and medullary origin do not occupy separate zones of the white matter, as was once believed (see Chapter 5). Reticulospinal axons end bilaterally among spinal interneurons of the ventral horn, and a few enter the regions containing the cell bodies of motor neurons.

The central nuclei of the reticular formation receive afferents from all the sensory systems, from the premotor and supplementary motor areas of the cerebral cortex, from the fastigial nucleus of the vestibulocerebellum, and from other parts of the reticular formation (see Chapter 9). Afferents from the pedunculopontine nucleus provide a descending pathway through which the corpus striatum may indirectly modulate the activities of motor neurons.

Within the brain stem, the reticulospinal axons have short branches that synapse with other neurons of the reticular formation. Branching has been demonstrated also in the spinal cord, so that a single reticulospinal axon may have terminations in cervical, thoracic, and lumbar segments. This observation has led to the suggestion that the reticulospinal tracts control coordinated movements of muscles supplied from different segmental levels of the spinal cord, such as those of the upper and lower limbs in walking, running, and swimming.Propriospinal (spinospinalis) fibers may be equally important for synchronization of limb movements.

Most of what is known about the reticulospinal tracts is derived from research with animals. The tracts are present in a wide phylogenetic range of mammals, so it is likely to hold true also for humans. In view of what is known of other major descending pathways, it seems probable that the reticulospinal tracts mediate control over most movements that do not require dexterity or the maintenance of balance. Motor tracts from the human cerebral cortex can be studied by stimulating the motor areas electrically to evoke small movements. Normally, the delay between the stimulus and the beginning of the response is short enough to be attributable to direct (monosynaptic) activation of motor neurons by the corticospinal tract. The existence of a corticoreticulospinal

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pathway is supported by the finding of motor responses with longer delays in patients in whom the corticospinal fibers are known to have degenerated following infarction in the internal capsule.

From the foregoing paragraphs, it can be seen that the corticospinal and corticoreticulospinal pathways are influenced by the activities of several regions of the CNS that have connections with the cerebral cortex and the reticular formation. A greatly oversimplified scheme of these connections (Fig. 23-3) may help readers to envisage the overall organization of these major parts of the motor system.

VESTIBULOSPINAL TRACT

This tract (see Chapter 5 and Fig. 23-2), which arises ipsilaterally from the large cells of the lateral vestibular nucleus (Deiters' nucleus), is also known as the lateral vestibulospinal tract. It is composed of myelinated axons of large caliber descending in the ventral funiculus of the spinal white matter. Most vestibulospinal fibers end in contact with interneurons in the medial part of the ventral horn of the spinal gray matter, but some synapse with the dendrites of motor neurons.

FIGURE 23-3 Diagram showing chains of command from sense organs and from the cerebral cortex to motor neurons, with sites at which the activities of corticospinal, reticulospinal, and vestibulospinal tracts can be modified by the basal ganglia and cerebellum. Descending motor pathways are red; other connections are blue. This simplified diagram omits many connections. For more details, see Figures 23-4 and 23-5.

Electrical stimulation of the lateral vestibular nucleus in animals causes contraction of ipsilateral extensor muscles of the limbs and vertebral column, with relaxation of the flexors. These effects occur to a lesser extent contralaterally as well, probably because there are neurons in the medial part of the ventral horn with axons that cross the midline of the spinal cord. Transection of the brain stem above the vestibular nuclei causes a condition known as decerebrate rigidity, in which the extensor musculature of the whole body is in a continuous state of contraction. This condition is easily produced in laboratory animals and occasionally occurs in patients with large destructive lesions of the midbrain or pons. (The condition

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can be caused by a large tumor or by thrombosis of the basilar artery.) The extensor spasm is abolished by destruction of the lateral vestibular nucleus, indicating that it is caused by the unopposed excessive activity of vestibulospinal neurons. The principal sources of afferent fibers to the lateral vestibular nucleus are the vestibular nerve, fastigial nucleus of the cerebellum, and vestibulocerebellar cortex.

The data summarized above support the view that the vestibulospinal tract is concerned with the maintenance of upright posture, which mainly results from the action of the extensor muscles in opposing gravity. Orderly functioning of the “antigravity” musculature is essential for balance, both at rest and during locomotion. Although the vestibulospinal tract does not mediate “voluntary” movements dictated by the cerebral cortex, it is essential for such highly skilled accomplishments of motor coordination as the feats of a gymnast or an acrobat. The learning of those aspects of skilled movement that involve posture and balance and that are effected through the vestibulospinal tract probably occurs in neuronal circuits that include the inferior olivary complex of nuclei and the cerebellum (see Chapter 10).

OTHER DESCENDING TRACTS

The parts of the brain that connect with the cells of origin of the corticospinal, reticulospinal, and vestibulospinal tracts are summarized in Figure 23-3. This diagram excludes some small descending tracts.

Two tracts in the medial part of the ventral funiculus terminate throughout the cervical segments of the spinal cord. These are the tectospinal tract, from the contralateral superior colliculus and the descending component of the medial longitudinal fasciculus. The former may be insignificantly small in humans. The latter, which is also called the medial vestibulospinal tract, arises from the medial vestibular nuclei of both sides but is mainly ipsilateral. Both tracts influence neurons that innervate the muscles of the neck, including those supplied by the accessory nerve, affecting movements of the head as required for fixation of gaze and maintaining equilibrium. The rubro-spinal tract provides a motor pathway of some importance in most mammals, but in humans, it is small and goes no further caudally than the second cervical segment.

Descending Pathways to Motor Nuclei of Cranial Nerves

Most of the muscles supplied by the cranial nerves participate in voluntarily initiated movements, and some of them are controlled with exquisite precision.

As described in Chapter 8, the oculomotor, trochlear, and abducens nuclei receive afferents through a complicated system of connections involving the cortex of the frontal, parietal and occipital lobes, superior colliculus, and various nuclei in the brain stem. It will be recalled that the cerebral cortex controls coordinated movements of the eyes. The frontal eye fields are necessary for changing the direction of gaze voluntarily. The posterior parietal cortex controls involuntary conjugate movements, as when tracking a moving object, and it also is necessary for convergence of the eyes to look at a near object.

Knowledge of the afferent connections of the other motor nuclei of cranial nerves is less complete. The nuclei concerned are the trigeminal and facial motor nuclei, nucleus ambiguus, and hypoglossal nucleus. Results of studies in animals indicate that corticobulbar fibers from the motor areas of the cortex end mainly in the reticular formation near the motor nuclei, with a few contacting the motor neurons directly. The motor nuclei also receive afferents from the reticular formation that are equivalent to the reticulospinal tracts. Therefore, upper motor neuron paralysis or paresis, caused by a lesion in the internal capsule, for example, is due to interruption of both corticobulbar and corticoreticular fibers.

With a unilateral lesion in the motor cortex or in the posterior limb of the internal capsule, the only paralyzed muscles in the head are those of the lower half of the face (moving the lips and cheeks) and of the tongue, contralaterally. The tongue paralysis is not permanent. The muscles supplied by the trigeminal motor nucleus, rostral portion of the facial motor nucleus, and nucleus

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ambiguus are not affected on either side by a unilateral lesion in the cerebral hemisphere. It has been deduced that descending pathways are distributed bilaterally to all the motor nuclei of the brain stem except the caudal part of the facial motor nucleus, which receives only crossed descending afferents. Partial deafferentation of the bilaterally supplied nuclei is evidently compensated for by the intact connections from the ipsilateral hemisphere. The existence of these functional connections has been confirmed by more recent studies that involve stimulation of the normal human cerebral cortex.

CLINICAL NOTE

Upper Motor Neuron Lesions

The term upper motor neuron is unsatisfactory because it refers collectively to descending pathways that make different contributions to the voluntary control of muscle action. Upper motor neuron lesion is still useful in clinical medicine, however, because it is often necessary to determine whether a group of muscles is weakened or paralyzed as a result of denervation or as a consequence of some lesion in the CNS. Sudden development of paralysis due to a vascular lesion (hemorrhage, thrombosis, or embolism) in the brain constitutes a stroke. An infarction in the posterior limb of the internal capsule, for example, results in contralateral hemiplegia with the typical signs of an upper motor neuron lesion. Similar (although not identical) abnormalities occur below the level of a lesion that partly or completelytransects the spinal cord. The clinical features of an upper motor neuron lesion are as follows.

1. Voluntary movements of the affected muscles are absent or weak.
2. Profound atrophy does not occur in the affected muscles, although there is slow wasting, and contractures may develop over several months if the condition does not improve. The muscles are not denervated, so the myotrophic effect of their motor innervation is preserved.
3. The tone of the muscles is increased. This phenomenon, known as spasticity, results from the continuous operation of the stretch reflex, which normally is suppressed by the activity of the descending tracts. The tendon jerks are exaggerated. When the examining physician attempts passive extension of a flexed joint, resistance is encountered because of operation of the stretch reflex. When greater force is applied, an inhibitory reflex is initiated by the Golgi tendon organs, which respond to tension rather than lengthening, and the muscles relax suddenly. This phenomenon is known as “clasp-knife rigidity.” Alternating contractions and relaxations, known as clonus, may also occur when a tendon is stretched. A test for clonus is application of firm pressure to the ball of the foot, which dorsiflexes the ankle joint, pulls the tendo calcaneus (Achilles' tendon), and stretches the gastrocnemius and soleus muscles. Pushing the patella toward the foot can evoke clonus in the quadriceps muscles.
4. With a cerebral lesion, the extensor muscles of the paralyzed lower limb are stimulated bythe intact vestibulospinal tract: the limb is extended and inwardly rotated. The upper limb is held in flexion at the elbow and wrist, perhaps as a result of activity in the reticulospinal tracts. A lesion in the spinal cord transects vestibulospinal fibers, and all the paralyzed limbs assume positions of flexion.
5. The plantar reflexis abnormal. Normally, there is plantar flexion of the big toe when the lateral margin of the sole is firmly stroked with a hard object. In the abnormal reflex, known as the Babinskisign or response, the toe is dorsiflexed. This movement is frequently associated with flexion at the knee and hip joints, although similar withdrawal is seen in normal people with sensitive soles. The descending tracts involved in the normal plantar reflex include the pyramidal tract. An extensor plantar response is normal in children under 1 year of age, and the response does not become unequivocally flexor until the 18th month. This maturation coincides with the myelination of most of the axons in the corticospinal tracts.
6. The superficial reflexesare suppressed or absent. These reflexes are the abdominal reflex (contraction of the anterior abdominal muscles when the overlying skin is firmly stroked) and the cremasteric reflex (withdrawal of the ipsilateral testis when the medial side of the thigh is stroked). The latter reflex is sluggish or absent in most men but is a useful clinical test in infants. These reflexes are presumed to be mediated by long tracts to and from the cerebral cortex, but their exact anatomical pathways are uncertain.
7. In the case of the facial muscles, only the lower half of the face is involved. For unknown reasons, muscle action expressing emotional changes is usually spared, and often there are abnormal emotional responses, such as laughter or crying on inappropriate occasions.
8. If the causative lesion in a cerebral hemisphere is small, there is gradual recovery of some function. Some patients develop “mirror movements,” which occur symmetrically on attempting to use a single limb. Electrophysiological studies indicate that this is due to branches of corticospinal axons that pass from the intact to the disordered side of the spinal cord. These branches may be formed by axonal sprouting (see Chapter 2). Recovery from stroke is poorer in humans than in other animals with comparable lesions. This discrepancy has been attributed to the absence of a significant corticorubrospinal projection in the human CNS.

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The hypoglossal nucleus receives more crossed than uncrossed afferents, and if the former have been removed, the latter assume control after a few weeks. The accessory nucleus, in the upper cervical segments of the spinal cord, supplies the trapezius muscle, which elevates the shoulder and the sternocleidomastoid muscle, which turns the head to look to the contralateral side. After transection of descending motor fibers, there is paralysis of the contralateral trapezius and of the ipsilateral sternocleidomastoid. Evidently, the fibers descending to the sternocleidomastoid motor neurons do not cross the midline.

Systems That Control the Descending Pathways

The movements elicited by electrical stimulation of the motor cortical areas (see Chapter 15) are much simpler than those that ordinarily occur either in obedience to conscious thoughts or as part of involuntary or habitual patterns of activity. The physiological output of signals from the motor cortex must, therefore, be much more complex than its responses to simple, artificial electrical stimuli. The most numerous afferent connections of the motor areas are the association and commissural fibers from other cortical areas and projection fibers from the thalamus, especially the ventral anterior and ventral lateral nuclei. These thalamic nuclei receive projections from two other systems involved in the control of movement, the cerebellum and basal ganglia. (Connections and functions of the motor cortical areas are discussed at greater length in Chapter 15. For more about the cerebellum and basal ganglia, see also Chapters 10 and 12.)

CEREBELLAR CIRCUITS

In connection with the motor systems, it is appropriate to review some of the connections of the cerebellum (Fig. 23-4). The cortex and central nuclei of the cerebellum receive input from extensive areas of the contralateral neocortex (by way of corticopontine and pontocerebellar projections); from ipsilateral proprioceptors in muscles, tendons, and joints (by way of the spinocerebellar and cuneocerebellar tracts); and from the vestibular apparatus. The inferior olivary complex, which receives most of its afferent fibers from the neocortical motor areas, red nucleus, and spinal cord, projects to the entire cerebellar cortex. In addition to these, the precerebellar reticular nuclei (see Chapter 10) relay information from the spinal cord, vestibular nuclei, and cerebral cortex. The cerebellar nuclei send their efferent fibers to the contralateral thalamus (ventral lateral nucleus) and red nucleus, as well as to the reticular formation bilaterally and to the ipsilateral vestibular nuclei.

Thus, the cerebellum receives information from the cerebral cortex, including motor areas, and it is also informed of changes in the lengths and tensions of muscles and of the position and angular movements of the head. These large contingents of afferent fibers are supplemented by smaller inputs that report on cutaneous, visual, and auditory sensations. The output of the cerebellar nuclei is brought to bear on the primary and supplementary motor areas through a relay in the posterior division of the ventral lateral thalamic nucleus (VLp). Other cerebellar efferents influence lower motor neurons through connections with the vestibular nuclei and the central group of nuclei of the reticular formation.

Electrophysiological investigations indicate that the cerebellum is informed through its olivary afferents of the program of neuronal instructions for any complex movement. The pontocerebellar afferents, which are active earlier than the primary motor area, are involved in the execution of movements. Cerebellar afferents activated by proprioceptive nerve endings enable a program of instructions to be modified in light of the changes in length and tension of muscles that are occurring.

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FIGURE 23-4 Diagram of some neural connections involved in the control of movement, with emphasis on cerebellar circuitry (green neurons) and the major descending tracts (red neurons). Sensory inputs are represented by blue neurons. Other cerebellar connections are explained and illustrated in Chapter 10.

BASAL GANGLIA

The basal ganglia, which are not ganglia but nuclei, are the corpus striatum of the telencephalon, subthalamic nucleus of the diencephalon, and substantia nigra of the mesencephalon. The corpus striatum is functionally subdivided into the striatum and the external and internal divisions of the pallidum. (The unfortunate plethora of names associated with the basal ganglia and corpus striatum is explained in Chapter 12.) The putamen and caudate nucleus constitute the striatum. Its afferent fibers come from the whole neocortex, from the intralaminar thalamic nuclei, and from the substantia nigra (Fig. 23-5). The striatum projects to the pallidum, which influences the premotor and supplementary motor areas through inhibitory relays in the ventral anterior (VA) and the anterior division of the ventral lateral nucleus (VLa) of the thalamus. The activity of the striatum is modulated by a two-way connection with the substantia nigra, and the activity of the pallidum is modulated by a two-way connection with the subthalamic nucleus. These connections are set out in more detail in Chapter 12.

A small contingent of pallidofugal fibers passes caudally and terminates in the pedunculopontine nucleus at the junction of the midbrain and pons (see Chapter 9). Among other projections, the pedunculopontine nucleus sends some fibers to the subthalamic nucleus, some to the pallidum, and some to the central group of nuclei of the reticular formation. A role in the timing of rhythmic activities, including locomotion and sleep, has been suggested for the pedunculopontine nucleus.

Clearly, the basal ganglia comprise a large mass of gray matter influenced by several parts of the CNS. The number and complexity of interconnections within the basal ganglia indicate

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that much integrative activity must be occurring. Only part of the system is devoted to motor activities (see Chapter 12). Electrophysiological studies indicate that in the corpus striatum, as in the cerebellar nuclei, changes in activity precede and accompany movements. It is probable, therefore, that the motor circuitry of the basal ganglia is involved in the transfer of information from the whole of the neocortex to the motor areas, in particular the premotor and supplementary motor areas and that the corpus striatum serves as a repository of instructions for fragments of learned movements. The effects of disease also indicate a role in remembering encoded instructions for the initiation, control, and cessation of all the components of regularly made movements.

FIGURE 23-5 Diagram of some neural connections involved in the control of movement, with emphasis on the basal ganglia, thalamus, and motor cortex. Cortical projections are red; others are blue. For other circuitry of the basal ganglia, see Chapter 12.

CONFUSING TERMINOLOGY

It was once erroneously thought that the pyramidal system controlled all deliberate movements and that there was a parallel “extrapyramidal” system largely concerned with the habitual or automatic activities of the muscles. Unfortunately, the term “extrapyramidal” has been applied not only to the reticulospinal and vestibulospinal tracts but also to pathways that include the corpus striatum, substantia nigra, and subthalamic nucleus because some of these structures were once thought to give rise to numerous descending fibers. From anatomical, physiologic, and clinical evidence, it is more appropriate to bracket the basal ganglia with the neocerebellum; the activity of both regions is directed through the thalamus to the motor areas of the cerebral cortex. Thus, the term “extrapyramidal system” does not represent any real entity and has caused much confusion. It is mentioned here because in clinical practice, dyskinesias (disorders in which abnormal spontaneous movements occur) are sometimes still called “extrapyramidal syndromes.”

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CLINICAL NOTE

Disorders of Movement

Knowledge of the neurotransmitters and their excitatory or inhibitory actions within the motor circuitry might one day make it possible to provide tidy neuroanatomical explanations for different types of disordered movement comparable to those that account for some sensory deficits. Some progress in this direction has been made and is reviewed in Chapter 12. Conditions with well-defined clinical features are caused by circumscribed lesions in certain regions. The most straightforward is the lower motor neuron lesion, described earlier. Some others are now reviewed. Disordered movement is also discussed in Chapters 7, 11, and 12.

UPPER MOTOR NEURON AND CORTICAL LESIONS

The clinical signs comprising the upper motor neuron lesion were identified earlier in this chapter. The syndrome occurs in its most typical form after infarction of the posterior limb of the internal capsule, resulting in the severance of ascending and descending tracts, including corticospinal and corticobulbar fibers, together with corticopontine, cortico-olivary, corticoreticular, corticorubral, and thalamocortical projections. Destruction of both the primary motor and the premotor cortex, such as often follows occlusion of the middle cerebral artery, has similar consequences.

Lesions confined to the primary motor area cause a flaccid paralysis of the part of the body appropriate to the exact position of the destroyed cortex. As with other lesions in which only small cortical areas are damaged, recovery usually occurs as the functions are taken over by adjacent areas. Destruction of the premotor area causes contralateral weakness of the muscles that move the shoulder and hip joints. Locomotion is also impaired. The hand cannot be brought into a useful position for many ordinary tasks, and impairment of sequential actions of muscles and faulty execution of visually guided movement may also be present. (Sequences and logical ordering generally require the integrity of cortex rostral to the prefrontal area.) An ineffective movement may be repeated without improvement.

If the supplementary motor area is destroyed, the patient has a severe contralateral motor disability in which movements cannot be initiated. Bilateral lesions, especially if they involve the adjacent cingulate motor area, cause akinetic mutism. These symptoms are consonant with the normal involvement of the supplementary and cingulate motor areas in the initiation of movements (see Chapter 15), including those of the muscles used in speech. Akinetic mutism caused by bilateral medial cortical lesions must not be confused with the consequences of a destructive lesion in the upper pons in which the patient is apparently asleep with relaxed musculature. In the latter condition, also called akinetic mutism, the eyes open in response to loud sounds and follow moving objects, but other sensory stimuli are ineffective, and there is no other movement or speech.

A related condition, seen with a midpontine lesion, is the locked-in syndrome, in which the patient is awake but mute, with all muscles paralyzed except those that move the eyes. A lesion causing the locked-in syndrome transects the descending motor tracts but spares the somesthetic and special sensory pathways. A magazine editor, Jean-Dominique Bauby (1952-1997), became locked in after a brain stem stroke in 1995. He wrote a remarkable autobiographical book, dictated letter by letter with a code based on movements of his left eyelid. He also founded, in 1996, the Association du Locked-in Syndrome, based in Boulogne-Billancourt, France. The locked-in syndrome is extremely rare. Large pontine vascular lesions usually cause sudden death. Bauby wrote: “In the past … you simply died. But improved resuscitation techniques have now prolonged and refined the agony.”

DYSKINESIAS

Dyskinesias are diseases in which unwanted superfluous movements occur. Chorea and various kinds of dystonia, which are thought to result from lesions of the corpora striata, are discussed in Chapter 12. Ballism, consisting of sudden flailing movements at the proximal joints of limbs, is usually caused by a vascular lesion in the contralateral subthalamic nucleus (see Chapters 11 and 12). The most frequently encountered dyskinesia is Parkinson's disease, which is characterized by muscular rigidity, tremor of distal muscles, and poverty of movement (bradykinesia). The primary lesion is loss of dopaminergic neurons in the pars compacta of the substantia nigra (see Chapters 7and 12). Normally, such neurons are active at all times, irrespective of any movement being made, exerting a continuous modulating influence

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on the striatum and, indirectly, on the premotor and supplementary motor areas of the neocortex. The bradykinesia of parkinsonism has been attributed to withdrawal of an excitatory action of dopamine on some striatal neurons. This releases the pallidum from inhibition by the striatum, resulting in increased pallidal inhibition of the VLa nucleus of the thalamus. This thalamic nucleus is excitatory to the premotor cortex, so in Parkinson's disease, the cortical activity is reduced. (Refer to Fig. 12-6 to follow the logic of this argument, which, unfortunately, does not account for the tremors and rigidity.)

CEREBELLAR DYSFUNCTION

Finally, lesions of the cerebellum lead to a variety of motor disturbances, including a specific type of ataxia, hypotonia, and a characteristic intention tremor (see Chapter 10). Cerebellar lesions may be said to generally lead to errors in the rate, range, force, and direction of willed movements. Unilateral damage to a cerebellar hemisphere (vascular occlusion, a tumor, or demyelination of white matter in one or more cerebellar peduncles) results in symptoms that affect the same side of the body. Cerebellar dysfunction, which may be bilateral, is a common feature of multiple sclerosis (MS), an autoimmune disease in which plaques of demyelination develop in white matter throughout the brain and spinal cord. Cerebellothalamic fibers are often affected in MS. Lesions in the midline of the cerebellum affect the vestibular and spinal connections, so an ataxic gait is the most prominent abnormality.

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