Dietz

The Parkinson's-Reversing Breakthrough

Treatment Options for Parkinsons

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Spinal Cord Injury Center, University Hospital Balgrist, Zurich, Switzerland

19.1 Summary

This chapter deals with the neuronal mechanisms underlying impaired gait as a paradigm of movement disorder with the aim of first, a better understanding the underlying pathophysiology and second, the selection of an adequate treatment and rehabilitation. For the patient usually one of the first symptoms of a lesion within the central motor system represents the movement disorder, which is most characteristic during locomotion in patients with spasticity or Parkinson's disease. The clinical examination reveals changes in tendon tap reflexes and muscle tone, typical for an impairment of the motor system. However, there exists only a weak relationship between the physical signs obtained during the clinical examination in a passive motor condition and the impaired neuronal mechanisms being in operation during an active movement such as locomotion. By the recording and analysis of electrophysiological and biomechanical signals during a movement, the significance of impaired reflex behaviour or muscle tone and its contribution to the movement disorder can reliably be assessed. Consequently, an adequate treatment should not be restricted to the correction of an isolated clinical parameter but should be based on the pathophysi-ology and the mechanisms underlying the disorder of movement which impairs the patient. Actual therapy should be directed to take advantage of the plasticity of the central nervous system (CNS). In the future a combination of repair and functional training will further improve mobility of severely disabled patients.

19.2 Introduction

The study of movement control has relevance to our understanding of brain and spinal cord function. However, it also has implications for various fields, such as neurology, cognitive neuroscience, rehabilitation medicine and robotics. The understanding of movement disorders and their appropriate treatment critically depends on the knowledge of the neuronal mechanisms underlying functional movements. Movement disorders are one of the most expanding fields in medicine, leading to increasing costs for treatment and rehabilitation. This chapter will focus on the role of neuronal mechanisms underlying gait disorders and the therapeutic consequences.

Locomotion is a subconciously performed everyday movement with a high reproducibility. It is automatically adapted to the actual conditions, such as ground irregularities with a large security range. Characteristic locomotor disorders are frequently the first sign of a central or peripheral lesion of the motor system. The neurological examination in such cases is characterised by changes in reflex excitability and muscle tone and leads to an appropriate diagnosis underlying the gait disorder. The physical signs obtained during the clinical examination can, however, give little information about the pathophysiol-ogy underlying the movement disorder: stretch reflex excitability and muscle tone are basically different in the passive (clinical examination) compared to an active motor condition (movement). In addition, during a movement such as gait, several reflex systems are involved in its execution and control. Therefore, for an adequate treatment of a movement disorder, we have to know about the function of reflexes and supraspinal motor centres involved in the respective motor task (see Volume II, Chapter 2). A movement such as locomotion is determined by the strength of electromyographical (EMG; Volume II, Chapter 4) activation of antagonistic leg muscles as well as intrinsic and passive muscle properties. The EMG activity recorded from the leg muscles reflects the action and interaction between central programs and afferent inputs from various sources, which can only be separated to a limited degree. For an assessment of the neuronal control of locomotion we have to record the EMG activity from several antagonistic leg muscles and the resulting biomechanical parameters such as joint movements and, eventually, of muscle tension. By such an approach it is possible to evaluate the behaviour of neuronal and biomechan-ical parameters during a gait disorder. Any changes in the neuronal or biomechanical systems may lead to a movement disorder.

Furthermore, impaired movement is not only the consequence of a defective central programme or proprioception. Rather, the movement disorder also reflects secondary compensatory processes induced by the primary lesion. In many cases, the altered motor response can be considered as an optimal outcome for a given lesion of the motor system (cf. Latash and Anson, 1996). The complexity of primary and secondary effects of a lesion requires a detailed analysis of movement disorder to define the target of any treatment.

19.3 Physiological basis of locomotion in humans

Leg muscle activation during locomotion is produced by spinal neuronal circuits within the spinal cord, the spinal pattern generator (central pattern generator (CPG), for reviews see Dietz, 1992a and Volume I, Chapter 13 of this textbook). For the control of human locomotion, afferent information from a variety of sources within the visual, vestibular and proprioceptive systems is utilized by the CPG. The convergence of spinal reflex pathways and descending pathways on common spinal interneurons seem to play an integrative role (for review see Dietz, 2002a), similar as in the cat (Schomburg, 1990). The generation of an appropriate locomotor pattern depends on a combination of central programming and afferent inputs as well as the instruction for a respective motor condition. This information determines the mode of organization of muscle synergies (Horak and Nashner 1986) which are designed to meet multiple conditions of stance and gait (Dietz, 1992a, for review see Mackay-Lyons, 2002).

Central mechanisms and afferent inputs interact in such a way that the strength of a reflex in a muscle or a synergistic group of muscles follows a programme that is dependent on the actual task. The actual weighting of proprioceptive, vestibular and visual inputs to the equilibrium control is context-dependent and can profoundly modify the central programme. Through this weighting, inappropriate responses are largely eliminated (for review see Mackay-Lyons, 2002). Any evaluation of reflex function has to be assessed in connection with the actual motor programme, the bio-mechanical events, including their needs and their restraints.

19.4 Gait disorder in Parkinson's disease

Evidence is accumulating that different regions of the basal ganglia have direct descending output connections to different parts of brainstem motor regulating centres: to the locomotor drive centres in the subthalamic area and in the mesencephalon, and to the centres involved in posture regulation in the pontine reticular formation (Marsden, 1990; Murray and Clarkson, 1996). The mesencephalic locomotor system exerts its descending control via bulbopontine and reticulospinal pathways. Studies on the activity in reticulospinal pathways indicate an inadequate function of these systems in Parkinson's disease (Delwaide et al., 1999).

Pathophysiological^, an impaired neuronal control of gait associated with rigid and poorly modulated motor performance represents a major deficit of Parkinson's disease (Martin, 1967). These abnormalities are thought to result from varying combinations of hypokinesia, rigidity, and from deficits of posture and equilibrium (Murray, 1967; Knutsson, 1972). Furthermore, by quantitative gait analysis distinct differences can be evaluated between the gait pattern of patients with vascular or idiopathic Parkinson's disease (Zijlmans et al., 1996), or of those with normal pressure hydrocephalus (Stolze et al., 2001). Little, however, is known about the extent to which such postural instability reflects deficits in the programmed adjustments or alternatively, in reflex mechanisms or compensation. Figure 19.1 shows the mechanisms that are suggested to be

Figure 19.1. Schematic diagram of the mechanisms involved in the movement disorder in Parkinson's disease. The disease of the extrapyramidal system leads to a defective utilisation of afferent input by the CPG. The consequence is a loss of leg extensor activation during the stance phase of gait, associated with an enhanced leg flexor activity, which control strongly depends on visual input. The combination of all sequels of impaired supraspinal control leads to the typical movement disorder (from Dietz, 2003).

Figure 19.1. Schematic diagram of the mechanisms involved in the movement disorder in Parkinson's disease. The disease of the extrapyramidal system leads to a defective utilisation of afferent input by the CPG. The consequence is a loss of leg extensor activation during the stance phase of gait, associated with an enhanced leg flexor activity, which control strongly depends on visual input. The combination of all sequels of impaired supraspinal control leads to the typical movement disorder (from Dietz, 2003).

involved in the movement disorder in patients with Parkinson's disease. For additional details on the pathophysiology, clinical features and rehabilitation of Parkinson's disease, see Volume II, Chapter 35.

Central mechanisms

In patients with Parkinson's disease several studies on gait indicate an impaired programming (for review see Dietz, 1992a). The electrophysiological gait analysis of patients with Parkinson's disease, in addition to showing slow and reduced movements, reveals a characteristic pattern of leg muscle activation with a reduced amplitude and little modulated EMG activity in the leg extensor muscles during the stance phase and an increased tibialis anterior activity during swing. Furthermore, the characteristic coordination of normal plantigrade gait is lost (Forssberg et al., 1984). The close similarity of gait between parkinsonian patients and children who had not yet developed a plantigrade gait has led to the suggestion that an immature pattern may reappear in Parkinson's disease as a result of deficits in the neuronal circuits controlling plantigrade locomotion (Forssberg et al., 1984).

Furthermore, coordination between lower limbs during walking is impaired in parkinsonian patients compared to age-matched healthy subjects (Dietz et al., 1996): 1. In the patients leg muscle EMG activity is less modulated and gastrocnemius EMG amplitude is small during normal and split-belt walking; 2. The amount of co-activation of antagonistic leg muscles during the support phase of the stride cycle is greater in the patients compared to healthy subjects. It was suggested that reduced EMG modulation and recruitment in the leg extensors may contribute to the impaired walking of the patient (Dietz et al., 1996).

This is in line with observations made on the leg muscle EMG pattern induced by feet displacement which also indicates an impairment of leg muscle activation (Dietz et al., 1988; 1993). In such a condition, the polysynaptic compensatory gastrocnemius EMG responses are smaller than those obtained in an age-matched group of healthy subjects due to a reduced reflex sensitivity (Dietz et al., 1988). This impaired function of polysynaptic reflexes confirms earlier suggestions of alterations in central response-ness (Berardelli et al., 1983) and defective utilization of sensory input (Tatton et al., 1984b) in these patients. The reduced sensitivity of polysynaptic reflexes in the leg extensor muscles appears to be a direct consequence of the dopamine deficiency in Parkinsonian patients, as it is also observed in young normal subjects following intake of a single dose of haloperidol (Dietz et al., 1990). Conversely, only some gait parameters (kinematic) are L-Dopa-sensitive, while others (temporal) are L-Dopa-resistant (Blin et al., 1991).

The diminished gastrocnemius activation is followed by a significantly stronger tibialis anterior activation in Parkinsonian patients, which might correspond to the so-called shortening reaction (for review see Angel, 1983; Berardelli and Hallett, 1984; Westphal, 1987). This may be a result of an impaired proprioceptive feedback control that was suggested to be partially compensated in Parkinsonian patients by a greater amount of leg flexor activation which leads to a higher degree of co-activation. Visual input plays a role in the control of this increased activation (Brouwer and Ashby, 1992; Dietz et al., 1997). In addition, Parkinsonian patients are inflexible in adapting and modifying their postural responses to changing support conditions (Schieppati and Nardone, 1991). The idea of an impaired central regulation is an agreement with the concept of an overcompensated and faulty predictive feedback system suggested elsewhere (Tatton et al., 1984a).

The changes in the behaviour of central mechanisms and reflexes described for Parkinsonian patients do not require the introduction of a qualitatively new pattern. These changes also characterize differences between elderly and young normal subjects, although they are more pronounced in Parkinsonian patients (Dietz et al., 1997).

Proprioceptive reflexes and muscle tone

Several observations indicate an impaired function of proprioceptive reflexes in Parkinsonian patients, which additionally contributes to the instability of Parkinsonian patients during gait (for review see Abbruzzese and Berardelli, 2003). This may be a major reason why these patients rely more on visual information for the regulation of gait (Bronstein et al., 1990).

Furthermore, there is evidence for associated changes of inherent muscle stiffness in Parkinson's disease (Dietz et al., 1988), which was attributed to altered mechanical properties of gastrocnemius muscle in Parkinson's disease and may contribute to rigid muscle tone. Such changes in muscle stiffness may be advantageous in so for as a higher resistance to stretch helps to compensate for a perturbation. Changes of inherent mechanical properties of muscle in Parkinson's disease have also been reported in upper limb muscles (Berardelli et al., 1983; Watts et al., 1986).

The differences in reflex function depend on the condition of the investigation. A great number of electrophysiological studies in Parkinson's disease are concerned with the reflex function during limb displacement in a sitting position. In contrast to the compensatory responses described for perturbations of stance or gait, most of these investigations show an increase in the amplitude of the long-latency EMG response (Chan et al., 1979; Berardelli et al., 1983; Cody et al., 1986). An increase of reflex gain at a central site has been postulated (Burke et al., 1977). The discrepant finding of a reduced stretch sensitivity of proprioceptive postural reflexes may arise primarily from the difference in motor tasks investigated. Locomotion represents a functional condition, with a convergence of several afferent inputs and an interaction with central mechanisms.

Load receptor function

Several studies on motor control in patients with Parkinson's disease are in line with the assumption of a defective load control in these patients (Stelmach, 1991; Burne and Lippold, 1996). The low activation of the leg extensor muscles during conditions of stance and locomotion was assumed to be due to a impaired proprioceptive feedback input

Supraspinal

Supraspinal

Figure 19.2. Schematical drawing of the neuronal mechanisms involved in the human gait. (a) Physiological condition. Leg muscles become activated by a programmed pattern that is generated in spinal neuronal circuits. This pattern is modulated by multi-sensory afferent input, which adapts the pattern to meet existing requirements. Both the programmed pattern and the reflex mechanisms are under supraspinal control. In addition, there is differential neuronal control of leg extensor and flexor muscles. Whereas extensors are mainly activated by proprioceptive feedback, the flexors are predominantly under central control. (b) Proposed situation in Parkinson's disease. In this condition, a load-related impairment of proprioceptive feedback can be assumed (dotted lines). This leads to reduced leg extensor activation during the stance phases, which is poorly adapted to actual requirements (e.g., ground conditions) (from Dietz, 2002a).

from extensor load receptors (Dietz et al., 1993). This defective control is illustrated in Fig. 19.2. It may be partially compensated for in Parkinsonian patients by a greater amount of leg flexor activation.

Furthermore, when body becomes unloaded during treadmill locomotion the leg extensor muscles show a load sensitivity in both Parkinsonian patients and healthy subjects (Dietz et al., 1997). However, the absolute level of leg extensor EMG amplitude during the stance phase is smaller in patients with Parkinson's disease than in the age-matched healthy subjects. This suggests that in Parkinson's disease the threshold of load receptor reflex loop is maladjusted or biased. This leads to a changed magnitude of this reflex response which is essential for the maintenance of body equilibrium.

19.5 Spastic gait disorder

Spasticity produces numerous physical signs such as exaggerated reflexes, clonus and muscle hypertonia (Volume II, Chapter 17). Clinically spastic hypertonia has been defined as a resistance of passive muscle to stretch in a velocity-dependent manner following activation of tonic stretch reflexes (Lance, 1980). On the basis of clinical observations a widely accepted conclusion was drawn for the pathophysiology and treatment of spasticity such that exaggerated reflexes are responsible for the observed muscle hypertonia, and therefore the movement disorder. The function of these reflexes during natural movements and the relationship between exaggerated reflexes and movement disorder is usually not considered (cf. Dietz, 2003a).

The physical signs of spasticity bear, however, little relationship to the patient's disability which is due to a movement disorder. In patients with spinal cord or brain lesions, a characteristic gait impairment is seen. This can be evaluated by the recording of electrophysiological and biomechani-cal parameters. There is some difference between spasticity of cerebral and of spinal origin, but the main features, such as leg muscle activation during locomotion and the pathophysiology of spastic muscle tone are quite similar (Dietz, 1992b). An overview about the mechanisms that are suggested

Figure 19.3. Schematic diagram of the mechanism that contribute to spastic paresis and spastic movement disorder. A central motor lesion leads to an impaired reflex control by the CPG and to a loss of supraspinal drive. The consequence is a hyperexcitability of short-latency reflexes and a loss of long-latency reflexes, as well as changes in muscle properties. The combination of all sequels of the primary lesion leads to spastic movement disorder. (from Dietz, 2002a).

Figure 19.3. Schematic diagram of the mechanism that contribute to spastic paresis and spastic movement disorder. A central motor lesion leads to an impaired reflex control by the CPG and to a loss of supraspinal drive. The consequence is a hyperexcitability of short-latency reflexes and a loss of long-latency reflexes, as well as changes in muscle properties. The combination of all sequels of the primary lesion leads to spastic movement disorder. (from Dietz, 2002a).

to be involved in spastic movement disorder are shown in Fig. 19.3.

Reflexes and muscle tone

It has been suggested that neuronal reorganization occurs following central lesions in both cat (Mendell, 1984) and man (Carr et al., 1993). Novel connections (e.g. sprouting, functional strengthening of existing connections, removed depression of previously inactive connections) may cause changes in the strength of inhibition among neuronal circuits. In addition, supersensitivity caused by the denervation may occur (Mendell, 1984). Although recent observations have indicated that spinal cord lesions do not cause sprouting of primary afferents in either cat (Nacimiento et al., 1993) or man (Ashby, 1989), changes in the reduction of pre-synaptic inhibition of group Ia fibres occur (Burke and Ashby, 1972) which correlate with the enhanced excitability of tendon tap reflexes. In addition, reduction of pre-synaptic inhibition is stronger in patients with paraplegia compared to those with hemiplegia (Faist et al., 1994). However, no correlation is seen between decreased presynaptic inhibition of Ia terminals and the degree of spasticity measured by Ashworth's scale (Faist et al., 1994). Probably also change in transmission in group II pathways may play a role in the pathophysiology of spasticity (Rémy-Néris et al., 2003).

The treatment of spasticity is usually directed towards reducing stretch reflex activity as it was thought that exaggerated reflexes are responsible for increased muscle tone and therefore the movement disorders. Studies on muscle tone and reflex activity have usually been performed under passive motor conditions (Thilmann et al., 1990; 1991; Ibrahim et al., 1993). In such a condition, increased elbow torque following a displacement is associated with an increased EMG activity in the flexor muscles of the spastic side compared to the unaffected side in patients with spastic hemiparesis. Nevertheless, in patients with spastic hemiparesis following stroke, muscle hypertonia was found to be more closely associated with muscle fibre contracture than with reflex hyperexcitability (O'Dwyer et al., 1996).

Investigations on functional movements of leg (Dietz et al., 1981; Dietz and Berger, 1983; Berger et al., 1984) and arm (Powers et al., 1989; Dietz et al., 1991; Ibrahim et al., 1993) muscles have not revealed any causal relationship between exaggerated reflexes and movement disorder. In adult patients with cerebral or spinal lesions the reciprocal mode of leg muscle activation during gait is preserved in spasticity. Exaggerated short-latency stretch reflexes in spasticity are associated with an absence or reduction of functionally essential polysynaptic (long-latency) reflexes. In addition, both cutaneous (Jones and Yang, 1994) and stretch (Sinkjaer et al., 1993; 1996) reflex modulation are impaired in patients with spinal cord lesion during walking. It was proposed that impaired modulation of the stretch reflex along with increased ankle joint stiffness contribute to the impaired walking ability in these patients.

In spastic patients the EMG activity in the calf muscles during gait is smaller in amplitude compared to healthy subjects, which is most probably due to the impaired function of polysynaptic reflexes in EMG activity. The reduction corresponds to the degree of paresis observed during both gait (Berger et al., 1984) and elbow movements (Dietz et al., 1991). Fast regulation of motoneuron discharge, which characterizes the normal muscle, is absent in spasticity (Rosenfalck and Andreassen, 1980; Dietz et al., 1986). This corresponds to a loss of EMG modulation during gait.

In spastic paresis (acquired at an early or later stage), a fundamentally different development of tension of the triceps surae takes place during the stance phase of the stride cycle (Berger et al., 1984). In the unaffected leg, the tension development correlates with the modulation of EMG activity (the same is true in healthy subjects), while in the spastic leg tension development is connected to the stretching period of the tonically activated (with small EMG amplitude) muscle. During gait there is no visible influence of short-latency reflex potentials on the tension developed by the triceps surae. A similar discrepancy between the resistance to stretch and the level of EMG activity has been described for flexor muscles of the upper limb in spastic patients (Lee et al., 1987; Powers et al., 1988).

Muscle tone during functional movements in patients with spastic paresis cannot be explained by an increased activity of motoneurons. Instead, a transformation of motor units such that a higher tension to EMG activity relationship occurs during the stretching phase of the triceps surae. This has the consequence that regulation of muscle tension takes place at a lower level of neuronal organization. The changed regulation of spastic gait can be considered as optimal for the given state of the motor system (e.g. Latash and Anson, 1996).

Motor unit transformation

There are several findings which support the suggestion that changes in mechanical muscle fibre properties occur in spasticity. Torque motor experiments applied to lower limb muscles indicate a major, non-reflex contribution to the spastic muscle tone in the antigravity muscles, that is in the leg extensors (Hufschmidt and Mauritz, 1985; Sinkjaer et al., 1993). Histochemistry and morphometry studies of spastic muscle have revealed neurogeni-cal changes of the muscle fibres (Edstrom, 1970; Dietz et al., 1986). A significant part of changes of mechanical muscle fibre properties might, however, be attributed to a shortening of muscle length as a result of a decrease in the number of sarcomeres in series along the myofibrils accompanied by an increase in resistance to stretch (O'Dwyer and Ada, 1996). Such muscle contracture can be produced in experimental animal by plaster cast immobilization of muscles in shortened positions.

The alteration to a simpler regulation of muscle tension following paresis due to spinal or supraspinal lesions is basically advantageous for the patient as it enables him to support the body during gait and, consequently, to achieve mobility (Dietz et al., 1981). However, rapid movements are no longer possible. Following a severe spinal or supraspinal lesion, these transformative processes can overshoot with unwelcome consequences, (i.e. painful spasms and involuntarily movements).

Consequently, in mobile patients primarily phys-iotherapeutic approaches should be applied, while antispastic during therapy represents a second tool. Only in immobilized patients antispastic drugs may be of benefit to relieve muscle spasms and improve nursing care (cf. Dietz, 2003a).

In children with cerebral palsy, that is when the central nervous lesion is acquired at an early stage, the leg-muscle activity during functional movements, such as locomotion, has characteristic signs of impaired maturation of the normal gait pattern (Berger et al., 1982). This pattern consists of a co-activation of antagonistic leg muscles during the stance phase of a gait cycle and a general reduction in EMG amplitude. In contrast, when the cerebral lesion is acquired at a later stage and the reciprocal mode of leg muscle activity is already established (i.e. at around 4 years), reciprocal activation of antagonistic leg muscles is preserved during spastic gait.

19.6 Target for rehabilitation: plasticity of the CNS

There is increasing evidence that a defective utilization of afferent input, in combination with secondary compensatory processes is involved in typical central movement disorders, such as spasticity and Parkinson's disease. Furthermore, cat (for review see Pearson, 2000) and human (for review see Dietz, 2002a; 2003b) experiments show that neuronal networks underlying the generation of motor patterns are quite flexible after central or peripheral neural lesions (see Volume I, Chapters 8 and 14). Therefore, the aim of rehabilitation should concentrate on the improvement of function by taking advantage of the plasticity of neuronal centres, and should less be directed to the correction of isolated clinical signs, such as the reflex excitability.

There is convincing evidence in spinal animals that a use-dependent plasticity of the spinal cord exists (Edgerton et al., 1997; Pearson, 2000). When stepping is practiced in spinal cat, this task can be performed more successfully than when it is not practiced (Lovely et al., 1986; 1990). The training of any motor task provides sufficient stimulation to initiate a reorganization of neural networks within the spinal cord and, for example, to generate locomotion. Consequently, the loss of motor capacity following neural injury can become enhanced when locomotor networks are no longer used, for example following a stroke (Edgerton et al., 1997). In contrast, a much greater level of functional recovery might be possible if the concept of use-dependence is applied in both the clinical and rehabilitative settings (Edgerton et al., 1997).

A considerable degree of locomotor recovery in mammals with a spinal cord injury (SCI) can be attributed to a reorganization of spared neural pathways (Curt and Dietz, 1997; Curt et al., 1998; for review see Curt and Dietz, 1999). It has been estimated that if as little as 10-15% of the descending spinal tracts are spared, some locomotor function can recover (Basso, 2000; Metz et al., 2000). If the loss of supraspinal input to the spinal cord is complete, these neuronal networks that exist below the level of the lesion adapt to generate locomotor activity even in the absence of supraspinal input (De Leon et al., 1998a, b; Wirz et al., 2001).

19.7 Locomotor function after SCI

Neuronal capacity of spinal cord from cat to humans

In the cat, recovery of locomotor function following spinal cord transsection can be improved using regular training even in adult animals (Barbeau and Rossignol, 1987; see Volume I, Chapter 13). When stepping was not stimulated, the cat lost the ability to step spontaneously. During such a locomotor training the animal was supported and thus only beared a part of its body weight. Locomotor movements of the hindlimbs were induced by a treadmill while the fore-limbs stood on a platform. With ongoing training the body support was decreased associated with improving locomotor abilities. Later on the cat was able to completely take over body weight and perform well-coordinated stepping movements (Barbeau and Rossignol, 1994). The locomotor pattern at this stage closely resembled the pattern of the normal adult cat. Furthermore, hindlimb exercise in adult rats after spinal cord transection can normalize the excitability of spinal reflexes (Skinner et al., 1996). Thus, it can be concluded that the training represents an important factor for the recovery of locomotor function. Recently, stepping movements could also be demonstrated in a monkey after transection of the spinal cord, suggesting that also the isolated primate spinal cord is capable of generating hindlimb stepping movements (Vilensky and O'Connor, 1988).

Human locomotion is not basically different from that described for the cat but is based on a quadrupedal neuronal co-ordination (for review see Dietz, 2002b). Step-like movements are present at birth and can be initiated spontaneously or by peripheral stimuli. The EMG activity underlying this newborn stepping is centrally programmed and, as it has also been observed in anencephalic children, it is likely that spinal mechanisms generate the EMG activity (Forssberg, 1992). The apparent loss of locomotor movements in accidentally spinalized humans has been suggested to be due to a greater predominance of supraspinal over spinal neuronal mechanisms (Kuhn, 1950). Nevertheless, there are indications that in humans spinal interneuronal circuits exist which are involved in the generation of locomotor EMG activity (Calancie et al., 1994) similar to those described for the cat (Barbeau and Rossignol, 1994). Furthermore, involuntary step-like leg movements described in a patient with an incomplete injury to the spinal cord (Nicol et al., 1995; Harkema et al., 1997), as well as the behaviour of a propriospinal clonus released after cervical trauma (Brown et al., 1994), are indicative for a spinal pattern generator in humans.

Effect of locomotor training in paraplegic patients

In patients with incomplete or complete paraplegia a bilateral leg muscle activation combined with coordinated stepping movements can be induced in partially unloaded patients standing on a moving treadmill (Dietz et al., 1994, 1995). The leg movements have to be assisted during the first phases of the training (dependent upon the severity of paresis), in incomplete and during the whole training period in complete paraplegic patients. Walking in incomplete SCI patients is usually achieved only at a low speed (Pépin et al., 2003). While the pattern of leg muscle EMG activity is similar to that seen in healthy subjects, the EMG amplitude is considerably smaller in complete paraplegics compared to incomplete paraplegis. Both patient groups have smaller EMG levels compared to the healthy subjects. Despite the reduced EMG activity, spastic symptoms (e.g. increased muscle tone, exaggerated reflexes) are present in both patient groups. This supports earlier suggestions claiming that alterations of mechanical muscle fibre properties are mainly responsible for the clinical signs of spasticity (see "Spastic gait disorder").

When the EMG of tibialis anterior and gastrocne-mius muscles is analysed over the step cycle, it becomes evident that leg muscle EMG activity is about equally distributed during muscle lengthening and shortening in both healthy subjects and patients during locomotion. Furthermore, imposing locomotor movements in complete paraplegic patients with full body unloading does not lead to a significant leg muscle activation (Dietz et al., 2002). This indicates that stretch reflexes are unlikely to play a major role in the generation of the leg muscle EMG pattern in these patients, but that it is rather programmed at a spinal level.

During the course of a daily locomotor training programme, the amplitude of gastrocnemius EMG activity increases significantly during the stance phase, while an inappropriate tibialis anterior activation decreases (Dietz et al., 1994, 1995). This is associated with a greater weight bearing function of the extensors (i.e. body unloading during treadmill locomotion can be reduced). These training effects are seen in both incomplete and complete paraplegic patients. Only patients with incomplete paraplegia benefit from the training programme in so far as they learn to perform unsupported stepping movements on solid ground. Patients with complete paraplegia experience positive effects upon the cardiovascular and musculo-skeletal systems (i.e. they suffer less from the spastic symptoms). Successive reloading of the body during the training may serve as a stimulus for extensor load receptors, which have been shown to be essential for leg extensor activation during locomotion in both cat (Pearson and Collins, 1993) and man (Dietz et al., 1992; Dietz and Colombo, 1996). The generally smaller EMG amplitude in patients with complete paraplegia may be due to a loss of input from descending noradrenergic pathways to spinal locomotor centres (Barbeau and Rossignol, 1994).

For an improved locomotor training during the last years special devices were developed. A driven gait orthosis (DGO) was designed primarily for the training of patients with a SCI (Colombo et al., 2000; 2001) and an electromechanical gait trainer for the restoration of gait in stroke patients (Werner et al., 2002).

Relevant afferent input

For a successful training of patients with a spinal or cerebral lesion, the appropriate afferent input has to be provided to activate spinal neuronal circuits. In healthy subjects during locomotion multi-sensory proprioceptive feedback is continuously weighted and selected. According to recent observations made in healthy subjects (Dietz et al., 1989a, b; 1992), small children (Pang and Yang, 2000) and patients with paraplegia (Harkema et al., 1997; Dietz et al., 2002) afferent inputs from load receptors and hip joints essentially contribute to the activation pattern of leg muscles during locomotion.

It is suggested that proprioceptive input from extensor muscles, and probably also from mechano-receptors, in the foot sole provide load information (Dietz and Duysens, 2000). The signals arising from load receptors are likely to be integrated into the polysynaptic spinal reflex pathway, which adapts the programmed locomotor pattern to the actual ground condition. The afferents that signal hip joint position are suggested to come from muscles around the hip. The role of this afferent activity is to shape the locomotor pattern, to control phase-transitions and to reinforce ongoing activity. Short-latency stretch- and cutaneous reflexes may be involved in the compensation of irregularities and in the adaptation to the actual ground conditions.

19.8 Assessment of function during rehabilitation

Owing to the exquisite task-dependent regulation of nervous-system function clinical tests must be functional and specific. At present it is a common, well-accepted approach to score isolated clinical measures, such as reflex excitability, muscle tone, or voluntary force of single muscles. For example, muscle tone and spasm frequency can be assessed by the Ashworth scale and Penn spasm frequency scale, respectively (Priebe et al., 1996). For patients with SCI, the American Spinal Injury Association (ASIA) has developed a standardised neurological assessment, that is the ASIA-classification of motor and sensory deficits (Maynard et al., 1997). The question is first, whether such scoring systems can serve as a sensitive outcome measure for new interventional therapies and second, whether they can reflect the functional impairment, which is the most important aspect in terms of the patients' quality of life (see Volume II, Chapter 37 on rehabilitation in spinal cord injury).

Only recently a score has been developed which relates to function. Locomotor ability has been classified into 19 items (Ditunno et al., 2000). A current study indicates that a close relationship between motor scores and locomotor ability exists only in patients with moderately impaired motor function. Patients with a low motor score undergoing a locomotor training can achieve an improved locomotor function without a change in motor score (Dietz, 2002a; Maegele et al., 2002). In these cases, relatively little voluntary force in the leg muscles (reflected in the ASIA score) is required to achieve the ability to walk (cf. Fig. 19.4).

For the future, the effectiveness of any new inter-ventional therapy should be assessed by functional scores in combination with motor scores of selected limb muscles. Motor and sensory scores are most likely to reflect the spontaneous recovery of function, as they depend on the integrity of cortico-spinal connections. In contrast, improvement of locomotor function after SCI also reflects the plasticity of neuronal circuits below the level of lesion. With the combined assessment of voluntary force and automatic

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