Brain, Vol. 122, No. 6, 1157-1168,
June 1999
© 1999 Oxford University Press
Impaired grip–lift synergy in children with unilateral brain lesions
1 Department of Woman and Child Health, Karolinska Institute, Stockholm, Sweden, 2 Laboratoire de Neurobiologie Intégrative et Adaptative, Université de Provence/CNRS, Marseille, France and 3 Department of Paediatrics, Hammersmith Hospital, London, UK
Correspondence to:
Hans Forssberg, Motorik Laboratory, Astrid Lindgren Hospital, Karolinska Hospital, S-171 76 Stockholm, Sweden E-mail: hansf{at}child.ks.se
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Abstract |
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Children with spastic hemiplegia have impaired dexterity in the affected extremity. The purpose of the present study was to investigate whether the force co-ordination pattern during precision grip in 13 children between 4 and 10 years of age with predominant unilateral brain lesions is related to manual dexterity and to the location and size of the brain lesion. The force co-ordination pattern was investigated by means of a specially designed object that monitored the isometric fingertip forces applied to the contact surfaces during precision grip. Hand function was measured by means of neurological examination, functional hand-grips and dexterity. Brain lesions were identified by series of ultrasound and MRI scans. Normally, the fingertip forces are applied to the object in the initial phase of the lift in an invariant force co-ordination pattern (i.e. grip–lift synergy), in which the grip and load forces are initiated simultaneously and increase in parallel with unimodal force rate trajectories. A majority of children with unilateral brain lesions had not developed the force co-ordination pattern typical for their age, but produced an immature or a pathological pattern. The developmental level of the grip–lift synergy was determined and quantified according to criteria derived from earlier studies on normally developed children. There was a clear relationship between the developmental level of the grip–lift synergy and impaired dexterity, indicating that proper development of the force co-ordination pattern is important for skilled hand function. The grip–lift synergy correlated with the total extent of lesions in the contralateral cortex and white matter and with lesions in the thalamus/basal ganglia, while no correlation was found for isolated cortical lesions. The results suggest that the neural circuits involved in the control of the precision grip are organized in a parallel and distributed system in the hemispheres, and that the basal ganglia are important during the formation of these circuits. Perinatal lesions in specific cortical motor areas may be compensated for by circuits elsewhere in the grip–lift motor system, while large lesions exclude this possibility.
unilateral brain lesion; grip; dexterity; children; cerebral palsy
M1 = primary motor cortex; PM = premotor cortex; SMA = supplementary motor area
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Introduction |
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Children with cerebral palsy usually have impaired dexterity. The impairment is partly due to spasticity and secondary musculoskeletal malformations, but, more importantly, the neural control of the finger movements is disturbed. Several of the specific functions required for the delicate control of the fingertip forces during precision grip and manipulation are lacking in children with cerebral palsy (Eliasson et al., 1991
, 1992, 1995). During their first 4 years children normally develop an invariant co-ordination pattern of the load (tangential to the grip surface) and grip forces (normal force) (Forssberg et al., 1991). The pattern is characterized by a short delay between the contacts with the first and second fingers and onset of the grip and load forces (preload phase). There is a parallel increase in the forces during the loading phase and `unimodal' force rate trajectories, i.e. the first time derivative of the forces (Johansson, 1991). The unimodal force rate trajectories indicate an anticipatory strategy in which the entire force output is programmed prior to the execution of the movement (Brooks, 1984).
The development of an invariant force co-ordination pattern for grasping is indicative of the automation of movement control. According to Bernstein (Bernstein, 1967), the CNS solves the problem of many degrees of freedom by forming functional synergies or classes of movement patterns. Although the number of muscles involved in precision grip is high, the grouping of several muscles into a functional grip–lift synergy allows the movement to be controlled by a small number of independent parameters.
The normal development of the grip–lift synergy occurs over several years and parallels the development of manual skills (Forssberg et al., 1991; Pehoski, 1995). Since precision grip requires independent finger movements and these are controlled directly from the motor cortex via the corticomotoneuronal system (Lawrence and Kuypers, 1968; Bortoff and Strick, 1993), the increased skill may partly reflect the growth and maturation of the cortical representations and the descending pathways. Indeed, the postnatal development of the corticospinal system occurs during an extended period in non-human primates (Lawrence and Hopkins, 1976; Flament et al., 1992; Armand et al., 1997; Olivier et al., 1997) and in humans (Eyre et al., 1991; Muller et al., 1991, 1994). As the main course of congenital hemiplegia in children consists of hemispheric lesions involving the cortical motor areas, leading to degeneration of the neurones in the descending motor pathways (Uvebrant, 1988; Bouza et al., 1994a, b; Rutherford et al., 1996), the poor development of the grip–lift synergy is attributable to these lesions.
In our previous studies on precision grip in children with cerebral palsy (Eliasson et al., 1991), we discussed whether the large amount of variation of the force pattern among subjects was dependent on the location and size of the brain lesions, and whether lesions in certain areas were more critical than in others. In the present study, the development of the grip–lift synergy was investigated in children with predominantly unilateral brain lesions, in whom several series of MRI scans were performed. Impairment of the force pattern was correlated with the location and size of the brain lesions. The developmental level of the grip–lift synergy was also correlated with the children's manual dexterity.
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Methods |
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Subjects
The children who were recruited for this study were born at or referred to the Hammersmith Hospital, London. They were part of another ongoing prospective follow-up study designed to evaluate the functional outcome in children with brain lesions (Jongmans et al., 1997
). Informed consent was given by subjects or their parents and the study was approved by the Ethics Committee of the Karolinska Institute, Stockholm, Sweden. Seventeen children with brain lesions that were determined by neonatal ultrasound and MRI scanning to be predominantly unilateral were identified and investigated. Four of these 17 children had such severe impairment of their hand movements that they could not perform the tests accurately, e.g. they were unable to establish a proper grip position at the contact surfaces of the object. These four children were excluded from the study. The remaining 13 children were aged between 4 and 13 years (Table 2).
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MRI
The infants had had either one or several MRI scans in the 2 years preceding the present study. MRI was performed using a Picker Vista HPQ 1.0 T system in an axial plane, using T1- and T2-weighted SE (Inversion Recovery) sequences. The images were assessed for evidence of brain loss or damage, which is manifested as an alteration in the signal intensity. Special attention was paid to changes in the cortex, the deep white matter, the periventricular region, the basal ganglia, the internal and external capsule and the brainstem. The ventricles were assessed for generalized or localized enlargement and irregularity of their outlines. The severity of the hemispheric involvement was graded into three categories using an overall score obtained by adding the degree of involvement of cortical, deep white matter and periventricular changes. Involvement was scored as mild (denoted +) if the lesion was very small and well defined, severe (+++) if the lesion was large and involved >50% of the lobes, and moderate (++) if the lesion was of an intermediate pattern (Table 1
).
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Clinical evaluation of hand function
Neurological examination
A standard neurological examination was performed to identify (i) abnormalities in posture, muscle tone and power, (ii) reflexes and (iii) movements. Impairment of the hemiplegic hand was graded according to the criteria described by Claeys and colleagues (Claeys et al., 1983
) into categories termed mild (pincer grasp: isolated finger movements present), moderate (grasping with whole hand: no isolated finger movements) and severe (no grasping).
Functional hand-grips
The quality of the hand-grip was evaluated according to Uvebrant (Uvebrant, 1988). Eight different grips were each tested and scored on a 1–3 point scale, a high score indicating poor performance. The hand-grips were considered to be normal if the global score was 8. Scores between 9 and 12 were considered to be indicative of mild impairment; scores between 13 and 20 demonstrated moderate impairment and a score above 20 represented severe impairment. The two hands were tested separately.
Manual dexterity
The items evaluating accuracy and speed of unimanual performance were selected from the Movement Assessment Battery for Children (Henderson and Sugden, 1992). The test presents tasks that increase in difficulty with age. The results
can be normalized according to age-specific data. The range is 0–5 and a score of 0–2 is normal, 3–4 is borderline and 5 is regarded as being representative of impaired manual dexterity. In our study an additional score of 6 was used when the child was unable to perform the task. The two hands were tested separately.
Analysis of grip–lift synergy; measurements of isometric fingertip forces
The instrumented grip object was a modified version of an earlier object adjusted for children (Westling and Johansson, 1984; Forssberg et al., 1991). It had a wide base allowing it to be placed on an ordinary table. Parallel contact surfaces (35x35 mm, 20 mm apart) covered with sandpaper were located at the top of the object. The grip force (normal force) and the load force (tangential to the surface) from each contact surface were measured with strain gauge transducers (DC, 160 Hz). The signals from the test object were sampled at 400 Hz and digitized with 12-bit resolution into a flexible computer system (SC/ZOOM, Department of Physiology, University of Umeå). A graphics terminal was used interactively to define time events and amplitudes of the grip and load forces as well as corresponding time derivatives.
The children either sat in a chair (n = 11) or stood (n = 2) in front of a table with their forearms approximately horizontal to the table when the object was lifted. They were instructed to grasp the object between the thumb and the index finger and hold it in the air for 3–4 s. Several children used additional fingers to stabilize the grip. Children with moderate impairment often touched the top of the object and pressed it towards the table before lifting it. This `pretouching' was recorded as a negative load force, although the forces were not employed on the contact surfaces (Fig. 2C). They performed the lifting task with both hands. There were 10 trials with each hand; the trials started with the hand ipsilateral to the predominantly lesion. Having received instructions on how to proceed, including demonstration of lifting, the children performed five practice lifts prior to recording. The co-ordination of the isometric fingertip forces during the lift was defined in various developmental stages according to earlier studies (Johansson and Westling, 1984; Eliasson et al., 1991; Forssberg et al., 1991). Three measures were used: (i) the duration of the preload phase; (ii) the grip force at onset of positive load force; (iii) the time when the peak of the grip force rate (first time derivative) occurred during the loading phase in relative terms. The mean for each child was calculated and the performance was compared with that of a group of children of the same age (Forssberg et al., 1991). Each subject in this study got a score defined by the variation in the corresponding age group. A value below +1 SD was given a score of 0, the range between +1 SD and +2 SD was given score 1 and values above +2 SD of the group mean were graded score 2. The sum of the three parameters produced a global score, giving a rough estimate of the development of the grip–lift synergy. A global score of 0–2 was regarded as being representative of well developed grip–lift synergy, 3–4 of immature grip–lift synergy and 5–6 as highly underdeveloped grip–lift synergy.
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Statistics
Non-parametric statistical methods were used. The Spearman correlation rank test was used to test the correlation between the development of the grip–lift synergy and the neurological examination, the functional tests and the lesions on the MRI scans.
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Results |
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MRI
The predominantly unilateral signal alterations in the MRI scans of all children in this study indicate that they had infarctions located mainly in one hemisphere. In seven children the lesions involved both the frontal and the parietal lobes, including the primary sensory and motor cortex and more frontal motor areas. All children had pathological signal alterations in the parietal lobe. In one child the infarctions predominantly involved the cortical layer (grey matter), and in seven children only the white matter was involved. In the remaining five children both the grey matter and white matter were affected. The ventricles were dilated as a result of white matter atrophy in almost all children. In nine children the lesions also involved the pathways through the internal capsule. Signal alterations were also common in the basal ganglia, the thalamus and the brainstem. For details of the location and size of the lesions see Table 1
and Fig. 1.
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Clinical evaluation of hand function
Neurological examination
Three of the 13 children exhibited normal posture, muscle tone, muscle power and movement in both hands. Five children had mild spastic hemiplegia and five had moderate spastic hemiplegia, contralateral to the unilateral lesion (Table 2
). In all children the ipsilateral hand was considered normal.
Functional hand-grips
In the hand contralateral to the lesion, four children had a normal score (8), three exhibited mild impairment (score 9–12) and four had moderate impairment (score 13–20). The two youngest children were not able to complete this task. In the hand ipsilateral to the lesion, eight children were found to have normal and three mild impairment (Table 2).
Manual dexterity
In the hand contralateral to the lesion, one child had a normal score (0–2), two children were borderline (score 3–4) and six were found to have impaired manual dexterity (score 5). Four children were not able to perform this test (score 6). In the ipsilateral hand, eight children had a normal score, four children were borderline and one child was found to have impaired manual dexterity (Table 2).
Grip–lift synergy
Recordings of the isometric fingertip forces by means of the instrumented grip object revealed disturbed co-ordination of the grip and load forces during the initial phase similar to that described in earlier studies on children with cerebral palsy (Eliasson et al., 1991). Figure 2 shows the force trajectories for three children with different levels of grip–lift synergy. When the individual distributions of the three components of grip–lift synergy were plotted (Fig. 3), the preload phase, the grip force at load force onset and the relative time to peak grip force rate varied considerably. When the values were compared with normal development the following groups were obtained. In the contralateral hand six children had a high score (5–6), indicating the absence of synergy; one child had a medium score (3–4), indicating immature development; and six children fell within the normal range (0–2). In the ipsilateral hand, almost all children (11 of 13) had a well developed grip–lift synergy (i.e. score 0–2). The remaining two children belonged to the group with immature development (i.e. score 3–4) (Table 2).
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Correlation between clinical evaluation of hand function and the development of grip–lift synergy
There was a strong correlation between the neurological examination and the development of the grip–lift synergy in the hand contralateral to the lesion (Fig. 4A
; r = 0.83, P < 0.001). None of the five children with a moderately hemiplegic hand developed a grip–lift synergy. In the children with mild hemiplegic hands, the grip–lift synergy varied. Of the three children whose neurological examination of the hand resulted in a normal verdict, all had developed a well co-ordinated grip–lift synergy.
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The two children who exhibited an immature grip–lift synergy in the ipsilateral hand were classified as normal in that hand by neurological examination. In the contralateral hand, both were classified as having a moderate hemiplegia and a poor grip–lift synergy (Table 2
).
The results of the clinical assessment of the functional hand-grips correlated with the grip–lift synergy (Fig. 4B; r = 0.80, P < 0.01) in the contralateral hand. The four children with moderate impairment (score 13–20) had no grip–lift synergy. In the remaining children with a normal score or mild impairment, the stage of grip–lift synergy varied. There was no correlation in the ipsilateral hand (r = –0.34, P > 0.05) (Table 2).
Manual dexterity correlated with the development of the grip–lift synergy (Fig. 4C; r = 0.87, P < 0.001). Of the four children unable to perform the manual dexterity test (score 6), none developed grip–lift synergy. Children with mild or moderate impairment, as determined from their performance of the manual dexterity test, exhibited a varying degree of development of grip–lift synergy. The child with a normal result in the manual dexterity test had also developed a normal synergy. There was no correlation between manual dexterity and grip–lift synergy development in the ipsilateral hand (r = 0.12, P > 0.05) (Table 2).
Correlation between MRI and grip–lift synergy
The impairment of grip–lift synergy correlated well with the overall contralateral hemispheric changes as investigated by MRI, i.e. with the total extent of the lesions in both the cortex and the white matter (r = 0.81, P < 0.001). Neither the cortical changes nor the changes in the periventricular white matter correlated with grip–lift synergy when they were analysed separately. The correlation with the lesions in the deep white matter had a fairly good correlation (r = 0.54, P < 0.05) (Table 3). The frontal lesions seemed to have the most influence upon development. In seven of the 13 children the frontal lobe was involved, and five of these seven children belonged to the group of six who had highly underdeveloped grip–lift synergy (r = 0.60, P < 0.05) (Tables 2 and 3).
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In addition to the signal alterations in cortical areas and in the white matter, lesions in the basal ganglia/thalamus strongly correlated with the development of grip–lift synergy (r = 0.84, P < 0.001).
Correlation between MRI and clinical evaluation of hand function
There were strong correlations between the various clinical examinations and the overall contralateral hemisphere changes (Table 3). In addition, lesions of the basal ganglia and thalamus corresponded well with impaired performance in the clinical tests while changes in the other structures seemed to have less influence on performance.
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Discussion |
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Is poor manual skill in children with cerebral palsy due to underdeveloped grip–lift synergy?
Grasp stability during the initial phase of a precision grip–lift is obtained by a small increase in the grip force during the preload phase followed by a parallel increase in the grip and load forces during the loading phase (Johansson and Westling, 1984
). The sensory control that ensures adequate adaptation of force output even when the weight or friction of the object is unknown depends on this coupling of the generation of the grip and load forces (Johansson, 1991). For example, when the increase in grip force is too small in relation to the friction and weight of the object, slips in the finger–object interface can be detected and the grip force increase can be adjusted before the object is lifted from its support (Johansson and Westling, 1984). A disturbance of the parallel force increase would probably result in deficient sensorimotor control and impaired dexterity. Earlier studies have revealed that children with cerebral palsy have frequently not developed the coupling between the grip and load forces, but instead have a sequential onset beginning with the increase in grip force (Eliasson et al., 1991). The present study has confirmed the absence of the specific force co-ordination pattern. In addition, a strong correlation was found between the developmental level of the force pattern and the level of dexterity, as revealed by neurological examination and assessment of manual dexterity and functional hand-grips. The co-ordination of the grip and load forces in each child was compared with that in normally developed children (Forssberg et al., 1991). Some children with cerebral palsy had developed patterns that almost corresponded to the norm for their age, while others had immature patterns, similar to those of much younger children. A third group exhibited abnormal patterns, lacking the characteristics of well developed grip–lift synergy. These latter children performed very poorly in the clinical tests, while children with a more developed pattern of force co-ordination exhibited much better performance (Fig. 4). Hence, it seems that development of the force co-ordination pattern of grip–lift synergy is important for achieving skilled hand movements and that disturbed co-ordination of the grip and lift forces results in impaired manual skills. However, it is not obvious that there is a causal relationship between deficient grip–lift synergy and impaired dexterity, as the brain lesions will also interfere with the neural control circuits involved in other functions that are critical for dexterity. Indeed, it has been shown that the sensory control that adapts the fingertip forces to the physical properties of the object is also disturbed in children with cerebral palsy (Eliasson et al., 1992, 1995).
Spasticity and secondary musculoskeletal malformations have been given much attention in earlier discussions of the cause of impaired dexterity in cerebral palsy (Twitchell, 1965; Sahrmann and Norton, 1977; Carr and Shepherd, 1983). The present finding emphasizes that disturbed neural control is a critical factor in itself and that it underlies the impaired motor performance. Likewise, disturbed neural control functions have been reported for several kinds of impaired gross motor behaviour in children with cerebral palsy, including walking and postural adjustments (Nashner et al., 1983; Berger et al., 1984; Leonard et al., 1991; Brogren et al., 1996). This is important information for the development of new strategies for treatment other than just the reduction of spasticity and the prevention of contractures.
Neural representation of grip–lift synergy
The concept of synergy has a long history and is still subject to various interpretations. Basically it means that instead of controlling each individual muscle, the CNS combines muscles into groups (or synergies) and exerts control over the group as a whole (synergy). In contrast to Sherrington (Sherrington, 1947), who used the term from an anatomical–morphological viewpoint, taking the synergies as laid down in the spinal cord, Bernstein (Bernstein, 1967) proposed a functional, operational definition and stressed higher-level neural processes. According to this proposal, the CNS groups functional variables into functional synergies, each synergy being controlled by a single central command. The coupling of the grip and load forces during the precision grip has the characteristics of such a synergy. The behaviour is automatized and invariant; the same pattern of force co-ordination is used every time. The motor pattern is not innate: instead it develops from a sequential pattern built up over several years of practice at the same time as the sensory control of the forces is developed (Forssberg et al., 1991, 1992, 1995; Gordon et al., 1992).
Which parts of the brain are necessary for the functional synergy required to achieve the specific co-ordination pattern of the grip and load forces (i.e. the grip–lift synergy)? Earlier stimulation and lesion studies indicated that various motor tasks were localized in specific cortical motor areas. For example, lesion of the supplementary motor area (SMA) in monkeys interfered with bimanual tasks and induced clumsiness of the contralateral hand (Brinkman, 1984), although the latter effect was transient and therefore indicated the existence of other centres that could compensate for the lost function. In humans there are reports that SMA lesions in adults may result in a decline in spontaneous movement (Meador et al., 1986), release of the `grasp reflex' and motor preservation (Goldberg et al., 1981; Gelmers, 1983), and that lesions of the premotor cortex (PM) may result in poorly co-ordinated movements of the contralateral limb (Freund, 1987). In a recent study, Hoffman and Strick (Hoffman and Strick, 1995) lesioned the primary motor cortex (M1) in a monkey that had been trained to make rapid step-tracking movements of the wrist. In certain directions, wrist flexion and radial deviation were made simultaneously, coupled in the same way as the generation of grip and load forces. After the lesion the movement was decomposed and the two components were performed in sequence. The latter result indicates that the neural representation of the learned movement involved the primary motor cortex.
In the present study on the effect of perinatal lesions in human infants, lesions involving the frontal lobe tended to have the strongest impact on the development of the grip–lift synergy in children with cerebral palsy. It was only when all lesions in the contralateral hemisphere were added together that a strong correlation with the developmental level of the grip–lift synergy could be found. These results suggest that there is no strict cortical representation of the grip–lift synergy, but that the functional synergy is organized in a parallel distributed system. Early damage to neurones in one cortical area can, in a parallel distributed system, be compensated for by neurones in other parts of the system.
Recent studies on humans using functional neuroimaging technology, e.g. with PET or functional MRI, also suggest that the several motor cortices (i.e. the primary motor, supplementary motor, premotor and the cingulate motor cortices) are organized in distributed and parallel systems. In simple motor tasks involving the hand, the shoulder and the foot, all non-primary motor areas were active in concert with the M1 (Fink et al., 1997). Complex sequences of finger movements, which were previously believed to be controlled by the SMA (Roland et al., 1980; Wise, 1985; Halsband et al., 1993), activated the same motor areas as simple flexion–extension movements of one finger (Rao et al., 1993; Shibasaki et al., 1993). Several studies indicate that the SMA is active both when movements are triggered externally and when they are self-generated (Obeso et al., 1995), in contrast to the earlier idea that the SMA controlled self-generated and self-paced movements. An earlier hypothesis suggested that the PM is specifically activated by movements that are guided by sensory information (in contrast to those that are triggered, paced or cued). Again, recent neuroimaging studies contradict earlier concepts and show that the PM is active both during self-generated movements and when movements are guided by sensory information (Roland and Zilles, 1996). All the cortical motor areas also seem to be involved in the modulation of the intensity and frequency with which a motor task is performed. Furthermore, variation of the force in a simple finger flexion task was correlated with activity in the SMA, CMA and M1, but not in the PM (Dettmers et al., 1995). In yet another study, a correlation was found between movement frequency and activity in the SMA, PM and M1 (Leonardo et al., 1995). Hence, at present the data from functional brain imaging of the control of human hand movement suggests that multiple hand representations are working in concert to control various aspects of task. A recent neuroanatomical study in monkeys has also shown that there are direct pathways from the more frontal motor cortices to the lateral horn in the cervical spinal cord (Dum et al., 1996), which implies that motor commands generated in these areas can reach the motor units directly without passing through the M1 or any other subcortical relay centre.
The extent of the perinatal lesions in the deep white matter correlated well with the impairment of the grip–lift synergy. This correlation is compatible with a parallel distribution of the functional grip–lift synergy in several cortical areas. If the information is stored in a cortical network, lesions of the corticocortical pathways in the white matter will disconnect the various parts of the network and prevent the functional variables from forming and the motor command from being properly generated. The present study indicates that the basal ganglia were also part of the distributed system for the grip–lift synergy. Other studies have shown that the force co-ordination pattern in adult patients with cerebellar lesions is disturbed during precision lifts in a similar way to that in children with cerebral palsy (Muller and Dichgans, 1994a, b). These findings enlarge the parallel distributed system to involve these subcortical structures also. White matter lesions will destroy the connections between the cortical areas, the basal ganglia and the cerebellum as well as disintegrating the network. In human fetuses and infants, the white matter is particularly vulnerable during the last trimester (Volpe, 1995). White matter lesion (periventricular leucomalacia) is also the most common cause of cerebral palsy in preterm infants, resulting in spastic diplegia. This emphasizes the importance of the neural pathways in the white matter for the development of motor skills in children, and suggests that several of the complex motor sequences that are normally learned depend upon distributed parallel systems involving both cortical and subcortical motor centres.
Remarkably, not all children with perinatal lesions in the frontal lobe demonstrated an impaired grip–lift synergy of the contralateral hand (e.g. subject 12; Tables 1 and 2). One explanation for this could be that lesions that occur in the immature CNS allow neural circuits to develop in other parts of the distributed network instead. Results from transcranial magnetic stimulation of the undamaged motor cortex in children with hemiplegic cerebral palsy support the idea that compensatory development may occur in the non-damaged hemisphere (Carr et al., 1993). In some children, connections had been established from the undamaged motor cortex to the ipsilateral arm and hand muscles of the hemiplegic side. Recent neuroimaging studies have also shown bilateral activation of the MI, SMA and PM in adults during unimanual finger movements (Kawashima et al., 1993, 1994; Kim et al., 1993), indicating that cortical areas of the ipsilateral hemisphere are involved in the fine motor control of the adult hand. The well-developed grip–lift synergy in some of the children with large lesions in one hemisphere could be a result of compensatory development of cortical circuits in the undamaged hemisphere controlling the ipsilateral hand. This corresponds well with the clinical outcome, as perinatal lesions in a single hemisphere may result in relatively small functional deficits while bilateral lesions are more deleterious (Bouza et al., 1994b).
The involvement of several cortical areas in the control of the grip–lift synergy is in good agreement with lesion studies in monkeys showing that the corticomotoneuronal system plays a critical role in skilled hand movements, particularly for independent finger movements and precision grip (Lawrence and Kuypers, 1968; Muir and Lemon, 1983; Palmer and Ashby, 1992; Bortoff and Strick, 1993; Bennet and Lemon, 1996). Independent finger movements first develop in the macaque monkey at 6–8 months, at the same age as cortical neurones establish contact with the distal finger motor units (Lawrence and Hopkins, 1976; Galea and Darian-Smith, 1995; Armand et al., 1997). Transcranial magnetic stimulation of the motor cortex in human infants indicates gradual development of the corticospinal system with increased conduction velocity and increasing amplitude of the response with increasing age (Eyre et al., 1991; Muller et al., 1991, 1994). The maturation of the corticospinal system takes place in parallel with the development of grip–lift synergy and manual dexterity (Forssberg et al., 1991, 1992, 1995).
A final strong correlation was found between lesions of the basal ganglia and thalamus and a poorly developed grip–lift synergy. This corresponds well with the central role of the basal ganglia in motor control, but not to earlier studies on precision lift in which patients with Parkinson's disease or focal dystonia exhibited normal force co-ordination patterns (Odergren et al., 1996; Ingvarsson et al., 1997). Instead, a strong action tremor and problems integrating the grip–lift synergy with the preceding reaching and subsequent lift-off phases contributed to the impaired dexterity in Parkinson's disease patients (Gordon et al., 1997; Ingvarsson et al., 1997), while patients with focal dystonia exhibited deficient sensory control of the force output. The apparently paradoxical results can be explained by the critical role of the basal ganglia during motor learning, but not after the motor behaviour has been established (Graybiel, 1995). Neuroimaging studies in humans indicate that the striatum is active during motor learning, as part of a distributed forebrain system (Seitz and Roland, 1992; Jenkins et al., 1994). In one study, when new tasks were being learned the striatum was active in a different way from when familiar or repetitive sequences of button presses were being carried out (Jueptner et al., 1997). The grip–lift synergy is acquired over several years of practice (Forssberg et al., 1991) and is probably the result of a long-lasting motor learning process. During this period the basal ganglia are required for the learning process and to store the functional variables in the distributed cortical network. Early lesion of the striatum and other basal ganglia circuits prior to this learning process would, therefore, affect the development of the grip–lift synergy. Destruction of functional circuits of the basal ganglia after the grip–lift synergy has been formed should, however, not be as deleterious since the functional variables are already stored in a network outside the basal ganglia.
Concluding remarks
Cerebral palsy comprises a heterogeneous group of movement disorders caused by damage to the immature brain. In each subject there is an individual blend of impaired motor functions, including spasticity, musculoskeletal deformations, dyskinesia, dystonia, ataxia and sustained developmental reactions. We have focused on another aspect of the movement disorder, which has so far drawn little attention for therapeutic intervention, namely impaired neural control. Children with spastic hemiplegia have impaired dexterity due to damage predominantly to the contralateral hemisphere. In the present study we found a clear relationship between impaired dexterity and deficiencies in the basic motor pattern underlying precision grip–lifts, these being used as a model of various aspects of grasping and manipulation. By comparing the degree of impairment with the brain lesions recorded in a series of MRI scans, our intention was to determine where in the brain the lesions affected the pattern most. In particular, we were interested to discover whether certain cortical structures had a special importance. Our results, supported by recent neuroimaging studies in humans, indicate that no specific cortical motor area is especially important. Instead, the functional synergy, or the procedural memory, for the basic force co-ordination pattern of the precision lift seems to be stored in parallel and distributed systems involving several cortical and subcortical structures. The basal ganglia might be particularly important whilst learning the basic pattern, and perinatal lesions severely hamper the capacity of children to learn the proper motor pattern. These new ideas will set the clinical focus on motor learning, and on new strategies to improve the learning procedure in children with cerebral palsy.
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Acknowledgments |
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This study was supported by the Swedish Medical Research Council, Stiftelsen Sven Jerrings fond and Karolinska Institute. The informed consent of all subjects was obtained according to the declaration of Helsinki.
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Received September 18, 1998. Revised January 15, 1999. Accepted January 25, 1999.
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