CHAPTER 2 The Nervous System and Movement 61
Supraspinal Control of Posture and
62 SECTION 1 Exercise and Responses of Biologic Systems
fi ring patterns during locomotion. This rhythm seems to be generated by the spinal circuitry driven by CPG as well as by sensory feedback.
important roles. There are differences in opinion regarding the relationship of the neural control of posture to that of locomotion. One hypothesis is that the control systems are rather distinct. An alternative hypothesis is that the neu- ral programs for posture and locomotion are highly inte- grated and share extensively in the control of standing and stepping.
Descending pathways for controlling locomotion
The primary anatomical descending pathways for initiat- ing locomotion are the corticospinal, reticulospinal, vestib- ulospinal, and rubrospinal tracts. The motor cortex gives rise to the corticospinal tract that decussates and infl u- ences the spinal circuitry associated primarily with the contralateral limbs. Some of these neurons have rhythmic
FIGURE 2.27 The motor infrastructure. A. Location of different networks (central pattern generators [CPGs]) that coordinate different motor patterns in vertebrates.
These areas can coordinate the activation of different CPGs in a behaviorally relevant order. For instance, if the fl uid intake area is activated, an animal will look for water, walk toward it, position itself, and start drinking. The cerebral cortex is important in particular for fi ne motor coordination involving hands and fi ngers and for speech.
B. General control strategy for vertebrate locomotion. Locomotion is initiated by activity in reticulospinal neurons (RS) of the brainstem locomotor center, which pro- duces the locomotor pattern in close interaction with sensory feedback. With increased activation of the locomotor center, the speed of locomotion increases and interlimb coordination can change ( e.g. , from a walk to a gallop). The basal ganglia exert a tonic inhibitory infl uence on motor centers that is released when a motor pattern is selected.
Experimentally, locomotion can also be elicited pharmacologically by administration of excitatory amino-acid agonists and by sensory input. DLR, diencephalic locomotor area;
MLR, mesopontine locomotor area. (Modifi ed from Grillner S. The motor infrastruc- ture: from ion channels to neuronal networks. Nat Rev Neurosci . 2003;4(7):573–586.)
Spinal cord Protective reflexes Locomotion The motor infrastructure
The vertebrate control scheme for locomotion
Brainstem Respiration Chewing Swallowing Eye movements
Cerebral cortex Fine motor control (speech, hand/finger coordination)
Hypothalamus Feeding Drinking
Basal ganglia Cerebellum
Selection Forebrain
Eye movements
Pharmacologic activation Sensory activation Feeding
Initiation Brainstem
Pattern generation Spinal cord A
B
Locomotion Central spinal network
Movement feedback Basal
ganglia
DLR
RS MLR
KEY POINT
In quadrupeds, the motor cortex has a minimal role in generating the basic locomotor pattern, but it appears to be involved in corrective actions and in making adjustments to weight-bearing levels (67).
The motor cortex, however, does play an important role in executing more skilled movements that are less repeti- tive and in adjusting the basic activation patterns during
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CHAPTER 2 The Nervous System and Movement 63 region activates reticulospinal neurons that, in turn, can
stimulate the spinal centers producing locomotion. Reticu- lospinal neurons become more active during locomotion than when the animal is at rest. The reticulospinal tract in cats is necessary to elicit locomotion when stimulating the MLR. Also, if the ventrolateral funiculi of the spinal cord are cut, a coordinated locomotor pattern cannot be initiated. A second area in the brainstem that can initiate locomotion and that also projects to reticulospinal neurons is the subthalamic locomotor region (66).
The exact manner in which these neurons induce loco- motion is not known. Activity of neurons in the MLR, how- ever, increases during locomotion. There is some evidence that the MLR region is controlled by inhibition and that the initiation of stepping may be induced by disinhibition (66). Neurons that form the reticulospinal, vestibulospinal, and rubrospinal tracts are rhythmically active during loco- motion. Most of the vestibulospinal neurons are active at the beginning of stance. Most of the neurons forming the rubrospinal and reticulospinal tracts are maximally active during the swing phase of a step cycle.
locomotion in a more variable environment. Although cor- ticospinal neurons may provide instruction for refi ning or modifying locomotor movements, it is clear that the basic locomotor patterns can be relatively normal without corti- cospinal input (Fig. 2.28). In primates, including humans, lesions of the motor cortex or spinal cord may produce a greater disruption of the basic locomotor patterns than in lower mammalian species (68). Most of the dysfunction occurs in the distal musculature that controls the wrist, ankle, and digits.
The medial reticular formation of the pons and medulla gives rise to neurons that form the reticulospinal tract.
These axons descend within the ventrolateral funiculi of the spinal cord and a single neuron can project to multiple levels of the spinal cord. The neurons that form the reticu- lospinal tract receive input from the brainstem including the MLR and from the cerebellum. The MLR, just rostral to the medial reticular formation (Fig. 2.29), provides input to the neurons that form the reticulospinal tract. Stimula- tion of the MLR (a 1-mm long strip of cells in the nucleus cuneiformis) can elicit locomotion. Stimulation of the MLR
FIGURE 2.28 Single and multijoint movements and stepping from a clinically incomplete, but severely injured, subject with a spinal cord injury. When the subject is asked to extend the knee, little movement occurred (lower left of A ) and EMG was recorded from one muscle. The subject was slightly more successful when instructed to move the limbs in a cycling motion.
Electromyographic (EMG) activity ( V) from the soleus (SOL), medial gastrocnemius (MG), tibialis anterior (TA), medial hamstrings (MH), vastus lateralis (VL), and rectus femoris (RF); knee and ankle angles (°); and footswitches (black bars indicate stance phase) during an attempted single joint movement ( A ), multijoint movement ( B ), and during weight-bearing stepping at 0.28 m s with 56% body weight support (BWS) ( C ). Minimal EMG was observed only in the VL during attempted knee extension ( A ), and only the MH became more active (although no clear EMG burst) during multi joint effort ( B ). Minimal movement of the knee or ankle occurred. This EMG pattern contrasts with the alternating bursts in each muscle during stepping ( C ). These results emphasize the fact that voluntary control from the brain is not essential for generating stepping.
The TA was largely synchronized with the SOL and MG whereas the MH EMG was reciprocal to that in the VL and RF and with ankle muscles. (Modifi ed from Maegele M, Muller S, Wernig A, et al. Recruitment of spinal motor pools during voluntary movements versus stepping after human spinal cord injury. J Neurotrauma . 2002;19:1217–1229.)
Knee extension Multijoint Movement Stepping
A
(o)(s)(μV)
100 100 100 100 100 100 155 140 150 130
100 100 100 100 100 100 170
9.8 4.9
seconds
0 0
170 150 140
100 100 100 100 100 100 155 140 150 130
B
8.4 4.2
seconds
0 C
10.6 FS RF MH TA MG SOL
VL
KNEE ANKLE
5.3 seconds
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64 SECTION 1 Exercise and Responses of Biologic Systems
FIGURE 2.29 Shik developed a preparation that consisted of a decerebrated ( A ) animal placed in a frame over a treadmill belt. MLR, mesencephalic loco- motor region; LM, corpus mammillare; LC, superior colliculus; RC, inferior colliculus; RH, red nucleus. ( B ). When the brainstem is sliced, so that the superior colliculus and the red nucleus lie just caudal to the slice, the animal can generate full weight-bearing stepping as shown in ( C ). Movements of the limbs are recorded by levers attached to the ankles as shown in ( C ). The timing of the brainstem stimulation is indicated by the thick horizontal line.
Note that stepping begins several seconds after the stimulation is initiated and it continues for a number of seconds after the tonic stimulation is terminated.
LF, left forelimb; RF, right forelimb; LH left hind limb; RH, right hind limb.
An adjustment in stepping cycle rate accommodates the changing speed of the treadmill belt ( D ). AEP, anterior extreme position; FEP, posterior extreme position. (Modifi ed from Orlovsky G, Deliagina T, Grillner S. Neuronal Control of Locomotion: From Mollusc to Man . Oxford University Press; 1999:166.)
D C
A 20 B
P A
15 10
LF RF LH RH Force
LH Speed Stim Speed
5 0
1 s 1 s
AEP FEP 5
1
1
2 7 10
10
3 4
5 6
9 8
LM Pons 2 MLR RC LC
RH
Medulla Cerebellum
Spinal cord
10 15
Thus, these descending tracts seem to have a modu- latory effect on the motoneurons during specifi c phases of the step cycle. It should be noted that the rhythm and fi ring of these descending tracts are due, in large part, to the infl uences from ascending input derived from the spinal cord circuitry. This phasic input (cyclic input associated with stepping) can occur independently of the afferent input from the periphery. For example, in paralyzed and decerebrated cats in which phasic afferent
infl ow from the periphery is precluded, phasic descend- ing and ascending activity between the spinal cord and supraspinal centers is still present during spontaneous motor activity.
KEY POINT
Thus, the vestibulospinal tract seems to facilitate exten- sor motoneurons, whereas the reticulospinal tract mainly facilitates fl exor and inhibits extensor motoneurons.
The rubrospinal and corticospinal tracts mainly facilitate
fl exor motoneurons (66).
Summary
It seems that supraspinal centers such as the MLR can increase or decrease the force or velocity of contraction of a muscle by changing the level of excitatory and/
or inhibitory input to the motoneuronal pools (35). If treadmill speed is kept constant, however, increased input to the midbrain in a decerebrate cat has no effect on the duration of the stance phase or step frequency (69). This suggests that the cycle duration is infl uenced by mechanical factors such as the position or the place- ment of the hind limb and, therefore, is mediated at least in part by proprioceptive signals.
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CHAPTER 2 The Nervous System and Movement 65