Deficient coordination of associated postural adjustments during a lifting task in children with neurodevelopmental disorders

Precision grip and concomitant anticipatory postural adjustments were investigated in 11 children (three females, eight males; mean age 9 years 1 month, SD 11 months) with attention-deficit-hyperactivity disorder (ADHD); 12 children (three females, nine males; mean age 9 years, SD 7 months) with developmental coordination disorder (DCD), and 13 children (two females, 11 males; mean age 9 years 9 months, SD 11 months) with a combination of ADHD and DCD (ADHD+). There were two comparison groups: an age-matched group (four females, 11 males; mean age 9 years 1 month, SD 14 months) and a younger age group (five females, six males; mean age 6 years 5 months, SD 8 months). Adaptation to different weights was evaluated by lifting a specialized grip instrument monitoring grip force, load force, and centre of foot pressure displacements. Children with ADHD+ showed: (1) excessive grip forces, (2) decreased amplitude and prolonged onset of postural adjustments, and (3) reduced ability to adapt the motor output. Children with ADHD and DCD did not scale manual and postural forces in amplitude and time domains. Children with DCD also differed in delayed timing of postural adjustments. Results indicate that children with ADHD and DCD show a spectrum of neural dysfunctions underlying poor motor coordination, which are not specific to the clinical disorder.     

Neurocase,Volume 18, Guest reviewers

Abstract

In adults, moving an object using precision grip involves anticipatory adjustment of grip force for fluctuations in inertial load force. These adjustments suggest that motion planning is based on an internal model of the effect or system and the environment. In the current study, we evaluate the coordination of grip force with load force in a child with developmental coordination disorder (DCD) and a matched, normally developing, control child. The children completed five tasks: (i) lifting an object; (ii) moving an object upwards; (iii) moving an object downwards; (iv) holding an object subject to unpredictable perturbation; (v) a time production (tapping) task. A number of differences were observed between the children. In particular, compared to the control, the child with DCD showed an earlier rise in grip force when making both upward and downward movements. We discuss this result in relation to the greater variability in explicit timing and longer reflex delays observed in the child with DCD. We conclude that this paradigm offers insight into the motion planning difficulties seen in DCD, providing a useful new methodology for the investigation of the observed coordination difficulties.     

Moving objects with clumsy fingers: how predictive is grip force control in patients with impaired manual sensibility?

OBJECTIVE: Anticipatory grip force adjustments to movement-induced load fluctuations of a hand-held object suggest that motion planning is based on an internal forward model of both the external object properties and the dynamics of the own motor apparatus. However, the central nervous system also refers to real time sensory feedback from the grasping digits in order to achieve a highly economical coupling between grip force and the actual loading requirements. METHODS: We analyzed grip force control during vertical point-to-point arm movements with a hand-held instrumented object in 9 patients with moderately impaired tactile sensibility of the grasping digits due to chronic median nerve compression (n = 3), axonal (n = 3) and demyelinating sensory polyneuropathy (n = 3) in comparison to 9 healthy age- and sex-matched control subjects. Point-to-point arm movements started and ended with the object being held stationary at rest. Load force changes arose from inertial loads related to the movement. A maximum of load force occurred early in upward and near the end of downward movements. RESULTS: Compared to healthy controls, patients with impaired manual sensibility generated similar static grip forces during stationary holding of the object and similar force ratios between maximum grip and load force. These findings reflect effective grip force scaling in relation to the movement-induced loads despite reduced afferent feedback from the grasping digits. For both groups the maxima of grip and load force coincided very closely in time, indicating that the temporal regulation of the grip force profile with the load profile was processed with a similar high precision. In addition, linear regression analyses between grip and load forces during movement-related load increase and load decrease phases revealed a similar precise temporo-spatial coupling between grip and load forces for patients and controls. CONCLUSIONS: Our results suggest that the precise and anticipatory adjustment of the grip force profile to the load force profile arising from voluntary arm movements with a hand-held object is centrally mediated and less under sensory feedback control. As suggested by previous investigations, the efficient scaling of the grip force magnitude in relation to the movement-induced loads may be intact when deficits of tactile sensibility from the grasping fingers are moderate.     

Grip force control in patients with neck and upper extremity pain and healthy controls

OBJECTIVE: To investigate whether sensory and motor problems in patients with non-specific neck and upper extremity pain can be ascribed to a deficit of sensory-motor integration. METHODS: Grip force control and adaptation were measured in 81 cases, 32 former cases and 39 healthy controls, during repetitive lifting and holding of an object. The object (300 g) was lifted vertically over 20 cm and held for 5s, using the dominant arm (the affected arm in all cases). The object was novel to the subjects when lifted for the first time, and was lifted five times consecutively. Grip forces orthogonal to the object's surface and its vertical acceleration were measured. RESULTS: Cases used significantly higher grip forces than both other groups, while vertical acceleration was not different. After the initial lift, all groups significantly reduced the maximum grip force. CONCLUSIONS: Subjects with neck and upper extremity pain consistently use higher grip forces than controls, but adjust grip forces by a similar amount after the first lift. Compensation of impaired sensory information rather than a general deficit in sensory-motor integration seems to account for these findings. SIGNIFICANCE: Non-specific neck and upper extremity pain coincides with objectifiable changes in control of grip force.     

Coordination of Manipulative Forces in Parkinson''s Disease

The coordination of manipulative forces was examined in 10 subjects with Parkinson's disease (PD) both OFF and ON medication while they grasped and lifted a small object using the precision grip. The development of grip (squeeze) force and load (vertical lifting) force was recorded and compared to a group of age-matched control subjects. Subjects with PD often exhibited a prolonged delay between the first digit contact with the object and initiation of the lifting drive. These subjects also exhibited stepwise increases in force, with regular oscillations in the force rates. However, once the vertical drive began, the main increase in grip and load force generally was in parallel and most other temporal aspects of the force coordination were similar to those of the control subjects. The extent to which the movement initiation was delayed was related to the stage of the disease, and most subjects improved ON medication. When the object was held in the air, subjects with PD used a grip force level which was similar to that of the control subjects, and all subjects adjusted their grip force according to the surface texture. Furthermore, they exhibited proper reflexive corrections to sudden changes in load (object perturbations), suggesting intact sensorimotor integration. We conclude that the most obvious impairments in the coordination of this task were delayed initiation of the grip–lift sequence and tremor-like oscillations superimposed on otherwise normal force.     

Effects of carpal tunnel syndrome on adaptation of multi-digit forces to object texture

Objective

The ability to adapt digit forces to object properties requires both anticipatory and feedback-driven control mechanisms which can be disrupted in individuals with a compromised sensorimotor system. Carpal tunnel syndrome (CTS) is a median nerve compression neuropathy affecting sensory and motor function in a subset of digits in the hand. Our objective was to examine how CTS patients coordinate anticipatory and feedback-driven control for multi-digit grip force adaptation.

Methods

We asked CTS patients and healthy controls to grasp, lift, and hold an object with different textures.

Results

CTS patients effectively adapted their digit forces to changes in object texture, but produced excessive grip forces. CTS patients also produced larger peak force rate profiles with fewer modulations of normal force prior to lift onset than did controls and continued to increase grip force throughout the lift whereas forces were set at lift onset for the controls.

Conclusions

These findings suggest that CTS patients use less online sensory feedback for fine-tuning their grip forces, relying more on anticipatory control than do healthy controls.

Significance

These characteristics in force adaptation in CTS patients indicate impaired sensorimotor control which leads to excessive grip forces with the potential to further exacerbate their median nerve compression.     

Deficits of predictive grip force control during object manipulation in acute stroke

Anticipatory grip force adjustments when lifting, holding and performing vertical point-to-point movements with a hand-held object were analysed in 11 patients with deficits of fine manual motor performance due to acute ischemic stroke. All patients had mild to moderate paresis and sensory deficits of the affected hand. Grip forces used to stabilise the object in the hand, accelerations of the object and movement-induced loads were measured. Compared with controls, patients produced markedly increased grip forces when lifting, holding and moving the hand-held object. The ratio between grip force and the actual load,which is considered to be a sensitive measure of force efficiency, was significantly elevated in stroke patients indicating a strategic generalisation of grip force increase when cerebral sensorimotor areas are functionally impaired. The temporal coupling between grip and load force profiles revealed only selective impairments during the lifting and movement tasks of stroke patients. The time to reach maximum grip force was prolonged and there were greater time lags between grip and load force maxima during the lifting movements. When healthy controls performed vertical movements with the hand-held object grip force increased early in upward and late in downward movements and grip and load force maxima coincided closely in time. The time lags between maximum grip and load forces were similar for vertical movements performed by patients and controls. However, the time lags between grip force and acceleration onset were larger for upward and smaller for downward movements performed by stroke patients. These findings indicate impaired prediction of the inertial load profiles arising from voluntary arm movements with a hand-held object in acute stroke.     

Effect of object transport on grasp coordination in multiple system atrophy.

We examined the effects of the parkinsonian variant of multiple-system atrophy (MSA-P) on grasp and forward transport and release of an object. Twelve patients with MSA-P and 10 age-matched control subjects performed the task with each of three object weights (200, 400, 800 gm). Subjects moved at a self-selected pace using a precision grip. The grip (normal) and load (tangential) forces and the object position were recorded. Results indicate subjects with MSA-P have temporal and force coordination deficits. Temporal delays were seen in all subjects with MSA-P, leading to prolonged overall movement times compared to control subjects. These delays occurred throughout the task, with significantly longer transport phases and delays releasing the object. Despite demonstrating an appropriate anticipatory scaling of forces, with increasing grip and load forces for heavier weights, force coordination was compromised in subjects with MSA-P. These subjects generated significant negative load forces prior to transporting the object. In addition, during the transport phase, subjects with MSA-P generated highly variable grip forces. Overall, the results indicate that subjects with MSA-P demonstrate bradykinesia and difficulty coordinating components of an object transport task.     

Altered movement trajectories and force control during object transport in Huntington's disease.

Individuals with Huntington's Disease (HD) have difficulty grasping and transporting objects, however, the extent to which specific impairments affect their performance is unknown. The present study examined the kinematics and force coordination during transport of an object in 12 subjects with HD and 12 age-matched controls. Subjects grasped an object between their thumb and index finger, transported it 25 cm forward, replaced and released it while their fingertip forces and the object's position were recorded. Five trials were performed with each of three weights (200 g, 400 g, and 800 g). While bradykinesia was evident in subjects with HD, this slowness was not consistently observed in all phases of the movement. The slowness of movement seen during the task appears to be due to impairments in sequencing and the movement strategies selected by the subjects. Compared to control subjects, subjects with HD produced highly curvilinear hand paths and more variable grip forces that were dependent on the weight of the object. Isometric force development and movement speed during transport were unaffected by the disease. The results suggest that prolonged task durations in subjects with HD are not necessarily due to slowness of movement, per se. These findings have clinical implications for understanding the task-specific nature of movement impairments in HD and developing effective intervention strategies.     

Coordination of fingertip forces during precision grasping in multiple system atrophy

While the pathology and autonomic nervous system components of multiple system atrophy (MSA) have been well described, little is known about the associated motor dysfunction. One prominent feature of MSA is parkinsonism, although ataxias and pyramidal tract signs are frequently present. To investigate the nature of motor deficits in MSA, a natural grip-lift movement requiring a precision grasp was used to examine force coordination. Subjects were asked to grasp an instrumented object using the fingertips of the thumb and index finger and lift it 10 cm above the table surface. Subjects with MSA demonstrated a prolonged duration between object contact and initiation of the lifting drive that increased with the weight of the object. During this period these subjects produced large grasping forces generating a significant portion of the eventual grip force employed to hold the object. In contrast, control subjects generated grip and load forces in parallel after establishing contact with the object. Therefore, subjects with MSA showed a disrupted performance on both the sequential (grasp, then lift) and simultaneous (grip and load force development) portions of this task. Only after initiation of the vertical lifting drive did subjects with MSA generate forces in a similar manner to control subjects. These findings demonstrate that subjects with MSA exhibit a disrupted coordination of grasp and could suggest a general deficit in motor control resulting from multi-focal neural degeneration.     

Coordination of fingertip forces during precision grip in premanifest Huntington's disease

Precision grip control is important for accurate object manipulation and requires coordination between horizontal (grip) and vertical (load) fingertip forces. Manifest Huntington's disease (HD) subjects demonstrate excessive and highly variable grip force and delayed coordination between grip and load forces. Because the onset of these impairments is unknown, we examined precision grip control in premanifest HD (pre‐HD) subjects. Fifteen pre‐HD and 15 age‐ and sex‐matched controls performed the precision grip task in a seated position. Subjects grasped and lifted an object instrumented with a force transducer that measured horizontal grip and vertical load forces. Outcomes were preload time, loading time, maximum grip force, mean static grip force, and variability for all measures. We compared outcomes across groups and correlated grip measures with the Unified Huntington's Disease Rating Scale and predicted age of onset. Variability of maximum grip force (P < .0001) and variability of static grip force (P < .00001) were higher for pre‐HD subjects. Preload time (P < .007) and variability of preload time (P < .006) were higher in pre‐HD subjects. No differences were seen in loading time across groups. Variability of static grip force (r² = 0.23) and variability of preload time (r² = 0.59) increased with predicted onset and were correlated with tests of cognitive function. Our results indicate that pre‐HD patients have poor regulation of the transition between reach and grasp and higher variability in force application and temporal coordination during the precision grip task. Force and temporal variability may be good markers of disease severity because they were correlated with predicted onset of disease. © 2011 Movement Disorder Society     

Grip force control during object manipulation in cerebral stroke.

OBJECTIVE: To analyze impairments of manipulative grip force control in patients with chronic cerebral stroke and relate deficits to more elementary aspects of force and grip control. METHODS: Nineteen chronic stroke patients with fine motor deficits after unilateral cerebral lesions were examined when performing 3 manipulative tasks consisting of stationary holding, transport, and vertical cyclic movements of an instrumented object. Technical sensors measured the grip force used to stabilize the object in the hand and the object accelerations, from which the dynamic loads were calculated. RESULTS: Many patients produced exaggerated grip forces with their affected hand in all types of manipulations. The amount of finger displacement in a grip perturbation task emerged as a highly sensitive measure for predicting the force increases. Measures of grip strength and maximum speed of force changes could not account for the impairments with comparable accuracy. In addition to force economy, the precision of the coupling between grip and load forces was impaired. However, no temporal delays were typically observed between the grip and load force profiles during cyclic movements. CONCLUSIONS: Impaired sensibility and sensorimotor processing, evident by delayed reactions in the perturbation task, lead to an excessive increase of the safety margin between the actual grip force and the minimum force necessary to prevent object slipping. In addition to grip force scaling, cortical sensorimotor areas are responsible for smoothly and precisely adjusting grip forces to loads according to predictions about movement-induced loads and sensory experiences. However, the basic feedforward mechanism of grip force control by internal models appears to be preserved, and thus may not be a cortical but rather a subcortical or cerebellar function, as has been suggested previously.     

Unilateral basal ganglia damage causes contralesional force control deficits: a case study

When grasping to lift an object, the grip force is usually scaled to the mass of the object. However, it has been shown that lifting objects of different sizes but equal masses results in the generation of higher forces for larger compared to smaller objects. The objective of this study was to investigate whether a similar effect is present in an individual (RI) with a unilateral lesion to the basal ganglia (BG). It was hypothesized that if the BG have an influence on the use of visual information in updating of the internal model used to anticipate the forces required for grasping, damage to these structures should result in the inability of RI's contralesional hand to anticipate object mass based on size cues. To test this hypothesis three objects of equal mass but different sizes were grasped and lifted by RI and six control individuals. The forces that were generated during these lifts were quantified. The controls showed the expected increases in peak grip force as object size increased. RI showed no effect of object size for his contralesional hand, but did show force scaling with his ipsilesional hand. In conclusion, RI's BG damage affected the on-line control of grip forces and the inability to integrate visual and tactile information in the programming of finger forces.     

Obesity and motor coordination ability in Taiwanese children with and without developmental coordination disorder

The purpose of this study was to investigate the associations between obesity and motor coordination ability in Taiwanese children with and without developmental coordination disorder (DCD). 2029 children (1078 boys, 951 girls) aged nine to ten years were chosen randomly from 14 elementary schools across Taiwan. We used bioelectrical impedance analysis to measure percentage of body fat (PBF) and the Movement Assessment Battery for Children test (MABC test) to evaluate the motor coordination ability. Using cut-off points based on PBF from past studies, boys and girls were divided into obese, overweight and normal-weight groups, respectively. In boys, total impairment scores and scores on balance subtest in the MABC were significantly higher in the obese and overweight groups when compared against the normal-weight group. Girls in the obese and the overweight groups had higher balance impairment scores than those of the normal-weight group. Among boys, the prevalence of obesity was highest in the DCD group, when compared to the borderline DCD and TD boys. A higher percentage of DCD girls were overweight and obese than TD girls. Obesity may be associated with poor motor coordination ability among boys and girls, and particularly in relation to balance ability. Children with DCD may have a higher risk to be overweight or obese in Taiwan.     

Detrimental neural control of precision grip lifts in children with ADHD

The aim was to investigate the performance of children with attention-deficit-hyperactivity disorder (ADHD) in tasks involving motor-memory representations. A special grip object recorded forces generated by the fingertips during a precision grip-lift task. Common objects were lifted from a linear scale. Twenty-five boys with ADHD were evaluated and grouped according to the presence (ADHD+) or absence (ADHD) of movement dysfunction using the Movement Assessment Battery for Children (Henderson and Sugden 1992). Mean group ages were 11.4 years (range 9.0 to 11.0 years) and 11.7 years (9.0 to 15.6 years), respectively. They were compared to a control group of 25 age-matched boys, mean group age 11.8 years (range 9.0 to 13.0 years). Variability of motor performance was predominant in the ADHD+ group. Several of these participants presented a higher grip-force output during the gripping movement. They also had difficulties in adapting the motor output to target different weights, suggesting deficient anticipatory parameter control based on memory representations. The results suggest that in some children motor problems are due to detrimental neural control functions rather than core symptoms of ADHD.     

Coordination of prehensile forces during precision grip in Huntington's disease

The present study examined the coordination of prehensile forces during precision grip in subjects with Huntington's disease (HD). Fingertip forces were measured in 12 subjects with HD and 12 age-matched controls during the lifting of an instrumented object whose weight and surface texture were varied. The results indicate that subjects with HD have impaired initiation and delayed transitions between movement sequences and produce excessive and variable forces. However, subjects with HD demonstrated anticipatory scaling of force development based on the object's expected physical properties (planning) and adjustment of the force to the object's actual physical properties (sensorimotor integration). The observed findings generally were unrelated to the overall disease severity. However, the variability in forces was correlated with functional capacity and motor performance suggesting that variability is a key feature of the motor deficit. These results provide insights into the impaired hand function observed in individuals with HD.     

Impaired generalization of weight-related information during grasping in cerebellar degeneration

When we repetitively lift an object, the balance between grip force normal to the object's surface and load force tangential to the object's surface is accurately programmed to match the physical object properties within a few lifts. Here, we ask if the accuracy of grip force scaling to object weight and the transfer of weight-related information from one hand to the other is impaired in cerebellar degeneration. Subjects with generalized cerebellar degenerative disorders were tested. Subjects first repeatedly lifted a constant weight with the dominant hand, followed by a series of lifts of the same weight with the opposite hand. The experiments were performed with a light and a heavy weight. Patients and controls scaled the grip force output differentially to different weight. The comparison of grip force scaling for the first and last lifts with a constant weight demonstrated that healthy subjects and cerebellar patients adjusted grip forces more accurately to a specific weight with increasing number of lifts performed at each hand. The ability to transfer weight-related information from one hand to the other was analyzed by comparing the last lift with a constant weight of the dominant hand with the first lift of the same weight performed by the opposite hand. Healthy subjects scaled the grip force output precisely to a given weight immediately after a change in hand, suggesting that they succeeded to transfer weight-related information in between both hemispheres. In contrast, cerebellar patients produced an inaccurate grip force overshoot when lifting a given weight with the opposite hand. Our data suggest that the cerebellum plays a major role for the generalization of weight-related information during object manipulation.     

Human brain activity in the control of fine static precision grip forces: an fMRI study

Dexterous manipulation of delicate objects requires exquisite control of fingertip forces. We have used functional magnetic resonance imaging to identify brain regions involved in the skillful scaling of these forces when normal human subjects (n = 8) held with precision grip a small object (weight 200 g) in the dominant right hand. In one condition, they used their normal, automatically scaled grip force. The object was held gently in a second condition; the isometric grip force was maintained just above the critical level at which the object would have slipped. In a third condition, the force was increased to hold the object with a more firm grip. The supplementary and cingulate motor areas were significantly more active during the gentle force condition than during either of the other conditions in all subjects, despite weaker contractions of the hand muscles. In addition, the left primary sensorimotor cortex, the ventral premotor cortex and the left posterior parietal cortex were more strongly activated during gentle than during normal grasping. These novel results suggest that these regions are specifically involved in dexterous scaling of fingertip forces during object manipulation.     

Adaptive force generation for precision-grip lifting by a spectral timing model of the cerebellum.

We modeled adaptive generation of precision grip forces during object lifting. The model presented adjusts reactive and anticipatory grip forces to a level just above that needed to stabilize lifted objects in the hand. The model obeys principles of cerebellar structure and function by using slip sensations as error signals to adapt phasic motor commands to tonic force generators associated with output synergies controlling grip aperture. The learned phasic commands are weight- and texture-dependent. Simulations of the new circuit model reproduce key aspects of experimental observations of force application. Over learning trials, the onset of grip force buildup comes to lead the load force buildup, and the rate-of-rise of grip force, but not load force, scales inversely with the friction of the object.     

Grip force behavior during object manipulation in neurological disorders: toward an objective evaluation of manual performance deficits.

The control of prehensile finger forces is an essential feature of skilled manual performance. The basic aspects of healthy grip force behavior have been well documented. In healthy subjects, grip force is precisely adjusted to the mechanical object properties. Grip force is always slightly higher than the minimum necessary to prevent the object from slipping. When we move a hand-held object, grip force is modulated in parallel with movements-induced load fluctuations without an obvious delay. The absence of a temporal delay between grip and load force profiles suggests that the central nervous system is able to predict the load variations before the intended manipulation and consequently regulates grip force in anticipation. Feedback from the grasping fingertips is used to adjust the level of applied fingertip force efficiently to the actual loading requirements. Pathologic grip force control affects the efficiency of produced force and the precision of the temporal coupling between grip and load force profiles. Here, we review the characteristics of pathologic grip force behavior in various neurological disorders. Detailed examination of grip force control is simple and well suited for the objective evaluation of impaired motor function of the hand and its rehabilitation.