The spinocerebellum comprises the vermis and intermediate parts of the cerebellar hemispheres (see Figure 42–2A).
Somatosensory Information Reaches the Spinocerebellum Through Direct and Indirect Mossy Fiber Pathways
The spinocerebellum receives extensive sensory input from the spinal cord, mainly from somatosensory receptors conveying information about touch, pressure, and limb position, through several direct and indirect pathways. This input provides the cerebellum with different reports of the changing state of the organism and its environment and permit comparisons between the two.
Direct pathways originate from interneurons in the spinal gray matter and terminate as mossy fibers in the vermis or spinocerebellum. Indirect pathways from the spinal cord to the cerebellum terminate first on neurons in one of several precerebellar nuclei in the brain stem reticular formation: the lateral reticular nucleus, reticularis tegmenti pontis, and paramedian reticular nucleus.
One fundamental principle of cerebellar operation can be appreciated on the basis of two important pathways from the spinal interneurons. The ventral and dorsal spinocerebellar tracts both transmit signals from the spinal cord directly to the cerebellar cortex but convey two different kinds of information.
The dorsal spinocerebellar tract conveys somatosensory information from muscle and joint receptors, providing the cerebellum with sensory feedback about the consequences of the movement. This information flows whether the limbs are moved passively or voluntarily.
In contrast, the ventral spinocerebellar tract is active only during active movements. Its cells of origin receive the same inputs as spinal motor neurons and interneurons, and it transmits an efference copy or corollary discharge of spinal motor neuron activity that informs the cerebellum about the movement commands assembled at the spinal cord. The cerebellum is thought to compare this information on planned movement with the actual movement reported by the dorsal spinocerebellar tract in order to determine whether the motor command must be modified to achieve the desired movement. The dorsal and ventral spinocerebellar tracts provide inputs from the hind limbs, whereas the cuneocerebellar and rostral spinocerebellar tracts provide similar inputs from more rostral body parts.
The idea that the cerebellum compares the actual and expected sensory consequences of movements is supported by studies of a number of movement systems. As a decerebrated cat walks on a treadmill, for example, the firing rate of neurons in the dorsal and ventral spinocerebellar tracts is rhythmically modulated in phase with the step cycle. However, when the dorsal roots are cut, preventing spinal neurons from receiving peripheral inputs that modulate with the step cycle, neurons of the dorsal spinocerebellar tract fall silent, whereas the firing of neurons of the ventral spinocerebellar tract continues to be modulated.
Recordings from the vestibulocerebellum of monkeys show that Purkinje neurons compare vestibular sensory inputs related to head velocity with corollary inputs related to eye velocity. The simple-spike output from these Purkinje neurons is modulated only when the eye movements are different from those expected from the vestibulo-ocular reflex. The cerebellum participates in the control of smooth eye movement only when the brain stem reflex pathways alone cannot produce the desired motor outputs.
The Spinocerebellum Modulates the Descending Motor Systems
Purkinje neurons in the spinocerebellum project somatotopically to different deep nuclei that control various components of the descending motor pathways. Neurons in the vermis of both the anterior and posterior lobes send axons to the fastigial nucleus. The fastigial nucleus projects bilaterally to the brain stem reticular formation and lateral vestibular nuclei, which in turn project directly to the spinal cord (Figure 42–7).
The spinocerebellum therefore provides important inputs to the brain stem components of the medial descending systems. Its outputs are important for movements of the neck, trunk, and proximal parts of the arm, rather than the wrist and digits, for balance and postural control during voluntary motor tasks. Because these brain stem systems also receive large inputs from descending pathways and from sensory inputs, we think that the cerebellum modulates and initiates, rather than controls, the descending commands to the spinal cord.
Purkinje neurons in the intermediate part of the cerebellar hemispheres project to the interposed nucleus. Some axons of the interposed nucleus exit through the superior cerebellar peduncle and cross to the contralateral side of the brain to terminate in the magnocellular portion of the red nucleus. Axons from the red nucleus cross the midline again and descend to the spinal cord (Figure 42–9). Other axons from the interposed nucleus continue rostrally and terminate in the ventrolateral nucleus of the thalamus. Neurons in the ventrolateral nucleus project to the limb control areas of the primary motor cortex.
Neurons in the intermediate and lateral parts of the cerebellar hemispheres control limb and axial muscles.
The intermediate part of each hemisphere (spinocerebellum) receives sensory information from the limbs and controls the dorsolateral descending systems (rubrospinal and cortico spinal tracts) acting on the ipsilateral limbs. The lateral area of each hemisphere (cerebrocerebellum) receives cortical input via the pontine nuclei and influences the motor and premotor cortices via the ventrolateral nucleus of the thalamus.
By acting on the neurons that give rise to the rubrospinal and corticospinal systems, the intermediate cerebellum focuses its action on limb and axial musculature. Because cerebellar outputs cross the midline twice before reaching the spinal cord, cerebellar lesions disrupt ipsilateral limb movements.
The Vermis Controls Saccadic and Smooth-Pursuit Eye Movements
The vermis is involved in the control of saccades and smooth-pursuit eye movements through Purkinje cells in lobules V, VI, and VII (Figure 42–2C). The cells discharge prior to and during such movements, and lesions of these areas cause deficits in the accuracy of both kinds of movements.
The vermis may be the only area of the cerebellum responsible for saccades, but it seems to share responsibility for smooth pursuit with the lateral part of the flocculonodular lobe. The outputs from neurons of the vermis concerned with saccades are transmitted through a very small region of the caudal fastigial nucleus to the saccade generator in the reticular formation. The exact neural pathways for guidance of pursuit by the vermis are not known, but they involve more synaptic relays than the outputs from the lateral part of the flocculonodular lobe, which reach extraocular motor neurons through two intervening synapses. One idea currently being explored is that the vermis also plays a role in motor learning that corrects errors in saccades and smooth-pursuit movements.
Spinocerebellar Regulation of Movement Follows Three Organizational Principles
In addition to confirming that cerebellar lesions in animals have the same effects as in humans, animal studies have provided an initial understanding of what the cerebellum does in healthy people and why lesions of the cerebellum have the effects they do.
Many experiments using monkeys have recorded the action potentials of single neurons in the interposed and dentate nuclei and the intermediate and lateral cerebellar cortex during arm movements. Other experiments have used cooling probes or substances that temporarily inactivate neurons to compare specific aspects of motor behavior in an active and inactive cerebellum. From these experiments we can draw three basic conclusions regarding the function of the spinocerebellum.
First, both Purkinje neurons and deep cerebellar nucleus neurons discharge vigorously in relation to voluntary movements. Cerebellar output is related to the direction and speed of movement. The deep nuclei are somatopically organized into maps of different limbs and joints, as in the motor cortex. Moreover, the interval between the onset of modulation of the firing of cerebellar neurons and movement is remarkably similar to that for neurons in the motor cortex. This result emphasizes the cerebellum's participation in recurrent circuits that operate synchronously with the cerebral cortex.
Second, the cerebellum provides feed-forward control of muscle contractions to regulate the timing of movements. Rather than awaiting sensory feedback, cerebellar output anticipates the muscular contractions that will be needed to bring a movement smoothly, accurately, and quickly to its desired endpoint. Failure of these mechanisms causes the intention tremor of cerebellar disorders.
Normally a rapid single-joint movement is initiated by the contraction of an agonist muscle and terminated by an appropriately timed contraction of the antagonist. The contraction of the antagonist starts early in the movement, well before there has been time for sensory feedback to reach the brain, and therefore must be programmed as part of the movement. When the dentate and interposed nuclei are experimentally inactivated, however, contraction of the antagonist muscle is delayed until the limb has overshot its target. The programmed contraction seen in normal movements is replaced by a feedback correction driven by sensory input. This correction is itself dysmetric and results in another error, necessitating a new adjustment (Figure 42–10).
The interposed and dentate nuclei are involved in the precise timing of agonist and antagonist activation during rapid movements.
The records show arm position and velocity and electromyographic responses of the biceps and triceps muscles of a trained monkey during a rapid movement. When the deep nuclei are inactivated by cooling, activation of the agonist (biceps) becomes slower and more prolonged. Activation of the antagonist (triceps), which is needed to stop the movement at the correct location, is likewise delayed and protracted so that the initial movement overshoots its appropriate extent. Delays in successive phases of the movement produce oscillations similar to the terminal tremor seen in patients with cerebellar damage.
Third, the cerebellum has internal models of the limbs that automatically take account of limb structure. (See Chapter 33 for a discussion of internal models.) An accurate dynamic model of the arm, for example, can convert a desired final endpoint into a sequence of properly timed and scaled commands for muscular contraction. At the same time, an accurate kinematic model of the relationship between joint angles and finger position can specify the joint angles that are needed to achieve an endpoint. Recordings of the output of the cerebellum have provided evidence compatible with the idea that the cerebellum contains kinematic and dynamic models of both arm and eye movements.
Studies of the movements of patients with cerebellar disorders suggest that the interaction torques of a multi-segment limb are represented by an internal model in the cerebellum. Because of the structure of the arm and the momentum it develops when moving, movement of the forearm alone causes forces that move the upper arm. If a subject wants to flex or extend the elbow without simultaneously moving the shoulder, then muscles acting at the shoulder must contract to prevent its movement. These stabilizing contractions of the shoulder joint occur almost perfectly in control subjects but not in patients with cerebellar damage (Figure 42–11). Patients with cerebellar ataxia are unable to compensate for interaction torques. They experience difficulty controlling the inertial interactions among multiple segments of a limb accounts and greater inaccuracy of multi-joint versus single-joint movements.
Failure of compensation for interaction torques can account for cerebellar ataxia.
Subjects flex their elbows while keeping their shoulder stable. In both the control subject and the cerebellar patient the net elbow torque is large because the elbow is moved. In the control subject there is relatively little net shoulder torque because the interaction torques are automatically cancelled by muscle torques. In the cerebellar patient this compensation fails; the muscle torques are present but are inappropriate to cancel the interaction torques. As a result, the patient cannot flex her elbow without causing a large perturbation of her shoulder position. (Adapted, with permission, from Bastian, Zackowski, and Thach 2000.)
In conclusion, the cerebellum uses internal models to anticipate the forces that result from the mechanical properties of a moving limb and may use its learning capabilities to customize internal models to anticipate those forces accurately.
Recent research suggests that excessive variability of Purkinje-cell output can lead to ataxia, suggesting that the regularity of cerebellar activity must be closely regulated to achieve normal movement. In animal models cerebellar symptoms result when deletion of certain ion channels causes the firing of Purkinje cells to become excessively variable even though the mean firing rate is entirely normal when averaged across many repetitions of a movement.
Are the Parallel Fibers a Mechanism for Motor Coordination?
A conspicuous feature of cerebellar structure is the medial-lateral parallel fiber "beam." Parallel fibers extend up to 6 mm through the molecular layer and excite the dendrites of Purkinje, basket, stellate, and Golgi cells along their course (see Figure 42–4). Basket and stellate axons create inhibitory flanks along the sides of the parallel fiber beam.
One current idea is that the great extent of the parallel fibers allows them to tie together the activity of different cerebellar compartments. Purkinje cells project topographically onto the deep cerebellar nuclei, each of which contains a complete map of body parts and muscles. In each map the representation of the tail is located anteriorly and that of the head posteriorly, with the limbs medially and the trunk laterally. The long trajectory of the parallel fibers could link different body parts in a medial-lateral dimension in different combinations.
In rats trained to reach to a target, for example, Purkinje cells along the medial-lateral parallel fiber beam fire simple spikes simultaneously and in precise synchrony with the movement. Pairs of Purkinje cells that are not situated along the same excitatory beam show no such synchrony. The synchrony may link muscles for multi-muscle movements and synchronize their contractions.
Finally, sagittal splitting of the posterior vermis in children, an operation performed to remove tumors in the fourth ventricle, creates surprisingly little functional deficit. The children can walk and climb stairs without assistance or obvious abnormality, and they can hop on one leg repeatedly almost as well as healthy children. Nevertheless, a striking deficit occurs when they attempt heel-to-toe tandem gait. Without support they fall after three steps. The discrepancy between the large deficit in tandem gait and the normal one-legged hopping is striking because both require the integration of vestibular, somesthetic, and visual sensation. These observations imply that the severed parallel fibers crossing in the vermis are essential to coordination of the projections to the bilateral fastigial nuclei.