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.     

Anticipatory Control of Manipulative Forces in Parkinson''s Disease

In a previous study we found that subjects with Parkinson's disease (PD) had an impaired capability to initiate and sequence successive movement phases during lifts of small objects using the precision grip, and that they had regular oscillations in the force rates. The present study examined whether these subjects could use anticipatory control, in which the force output is scaled prior to liftoff, based on the object's physical properties. Subjects lifted an instrumented test object between the tips of the thumb and index finger while the employed grip force, load force (vertical lifting force), and corresponding time derivatives were recorded. In the first experiment, the object's weight was varied to assess its influence on the isometric force output. Subjects with PD scaled the isometric force increase according to the object's weight. In another experiment, the weight changed in proportion to the volume to determine whether subjects could make associative transformations between visual size information and the weight of the object. Subjects with PD still scaled the forces toward the expected weight, proportional to the volume of the object. Finally, programmed adjustments in force to sudden self-induced load changes were examined while subjects dropped a disk with one hand into a plate attached to the bottom of the grip instrument, held with the other hand. Subjects with PD had preparatory increases in the grip force prior to the disk contact, which matched the change in load, though may have been more dependent on visual feedback. We conclude that subjects with PD are capable of using anticipatory control to parameterize the isometric force output during a familiar lifting task.     

Action tremor during object manipulation in Parkinson's disease.

In previous studies of fingertip forces during precision grip in subjects with Parkinson's disease (PD), we observed regular oscillations in isometric force. The present study characterizes the nature of these oscillations. Fingertip forces were recorded from the index finger and thumb during precision grip-lifts with a 300 g and 900 g object in 10 subjects with PD and 20 healthy control subjects. Fourier analysis confirmed that all subjects with PD exhibited force oscillations with a clearly definable frequency (approximately 7-11 Hz). Five of these subjects also exhibited a second lower frequency peak (approximately 5 Hz). Approximately half of the 20 control subjects displayed a single frequency peak (approximately 8-12 Hz), which was generally lower in amplitude than in the subjects with PD (representing enhanced physiological tremor), whereas the remaining control subjects had low-amplitude, broad-based spectra (representing physiological tremor). The amplitude of the force oscillations was higher for lifts with the heavier object in both the control subjects and subjects with PD. L-Dopa resulted in a decreased tremor amplitude but did not influence the frequency. The force oscillations of the two opposing digits normal to the grip surfaces were in phase, whereas the oscillations tangential to the grip surfaces were often out of phase. The results suggest that the multipeaked force rate trajectories reported previously are caused by action tremor. The similarity of force oscillations in subjects with PD and healthy control subjects suggests common tremor-generating mechanisms and supports the notion that the parkinsonian action tremor (AT) is an exaggerated form of physiological tremor. These findings provide insight into the impaired hand function observed in individuals with PD.     

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.     

Precision grip deficits in cerebellar disorders in man.

OBJECTIVE: To investigate the effect of a variety of cerebellar pathologies on a functional motor task (lifting an object in a precision grip). METHODS: The study involved 8 patients with unilateral damage in the region of the posterior inferior cerebellar artery (PICA), 6 with damage in the region of the superior cerebellar artery (SUPCA), 12 patients with familiar or idiopathic cortical cerebellar degeneration, and 45 age-matched normal subjects. Subjects lifted an object of unpredictable load (internally guided task) or responded to a sudden load increase while holding the object steadily (externally guided task). RESULTS: Damage to the dentate nucleus (SUPCA) or its afferent input (cerebellar atrophy) resulted in disruption of the close coordination normally seen between proximal muscles (lifting the object) and the fingers (gripping the object) during a self-paced lift. Both the SUPCA group and, more markedly, the atrophy group, showed exaggerated levels of grip force. All patients showed a normal rate of grip force development. Damage in the PICA region had no significant effect on any of the measured lifting parameters. All patient groups retained the ability to scale grip force to different object loads. The automatic grip force response to unexpected load increase of a hand held object showed normal latency and time course in all patient groups. The response was modulated by the rate of the load change. Response magnitude was exaggerated in the atrophy patients at all 3 rates tested. CONCLUSIONS: Disturbances associated with cerebellar disorders differed from those seen following damage to the basal ganglia, with no evidence of slowed rates of grip force development. Disruption of temporal coordination between the proximal muscles (lifting) and the fingers (gripping) in a lift was apparent, supporting the role of the cerebellum in coordinating the timing of multi-joint movement sequences. Exaggeration of grip force levels was found in association with damage to the dentate nucleus or, in particular, to its afferent input. This could support a role or the cerebellum in sensorimotor processing, but might also represent a failure to time correctly the duration of grip force generation.     

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 abnormalities in de novo Parkinson's disease.

In recent years it has been shown that a variety of movement disorders are associated with abnormalities of the fine motor control of the hand. In Parkinson's disease (PD), these changes consist of a slowing of the rate of grip force development and the use of abnormally large grip forces both during lifting and static holding of an object. It has been suggested, however, that these changes are a direct effect of the patient's levodopa medication or associated with levodopa induced dyskinesias. Accordingly, we examined the performance of de novo Parkinson patients in a precision lifting task. All patients (n = 6) were newly diagnosed and showed rigidity, bradykinesia, or both, but were unaffected by tremor or dyskinesia. None of the patients had received antiparkinson medication. Grip force was abnormally high in both the lifting and hold phases. This exaggeration was equal in magnitude to that observed previously in medicated patients. Thus we conclude that the abnormalities in grip force observed here are intrinsic features of PD and not the result of dopamine medication or its side effects.     

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.     

The effects of digital anaesthesia on predictive grip force adjustments during vertical movements of a grasped object

Grip force adjustments to fluctuations of inertial loads induced by vertical arm movements with a grasped object were analysed during normal and impaired finger sensibility. Normally grip force is modulated in a highly economical way in parallel with fluctuations of load force. Two subjects performed vertical up and down movements of a grasped object, both with normal finger sensibility and then cutaneously anaesthetized finger sensibility. Short breaks were taken in between single movements, during which the object was held stationary. After digital anaesthesia was applied to the grasping fingers, both subjects substantially increased the grip force. The grip force amplitude and timing still anticipated changes in load force, although the established grip force had already overcome movement-induced load force peaks. This implies that the increase of grip force and consequently the elevated force ratio between maximum grip and maximum load force are not processed to alter the feedforward system of grip force control. Cutaneous afferent information from the grasping digits appears to be necessary for economic scaling of the grip force level, but it plays a subordinate role in the precise anticipatory temporal coupling of grip and load forces during voluntary object manipulation.     

Grip force behavior in Gilles de la Tourette syndrome.

We analyzed predictive and reactive grip force behavior in 15 patients with Gilles de la Tourette syndrome (GTS) and 15 sex- and age-matched healthy control subjects. Nine patients were without medication; six patients were on medication. In a first experiment, participants lifted and held instrumented objects of different weight. In a second experiment, participants performed vertical point-to-point and continuous arm movements at different frequencies with a hand-held object. In a third experiment, preparatory and reactive grip force responses to sudden load perturbations were analyzed when a weight was dropped into a hand-held cup either by the subject or unexpectedly by the experimenter. Compared to the healthy subjects, GTS patients had increased grip forces relative to the load force in all tasks. Despite this finding, they adjusted the grip force to changes in load force (due to either a change in the mass lifted or accelerating the mass during continuous movements) in the same way as healthy subjects. The temporal coupling between grip and load force profiles was also similar in patients and healthy controls, and they displayed normal anticipation of impact forces when they dropped a weight into a hand-held cup. We found no significant effect of medication on the performance of GTS patients, regardless of the task performed. These results are consistent with deficient sensory-motor processing in Gilles de la Tourette syndrome.     

Disturbances of grip force behaviour in focal hand dystonia: evidence for a generalised impairment of sensory-motor integration?

BACKGROUND: Focal task specific dystonia occurs preferentially during performance of a specific task. There may be an inefficiently high grip force when doing manipulative tasks other than the trigger task, possibly reflecting a generalised impairment of sensory-motor integration. OBJECTIVE: To examine how well subjects with writer's cramp (n = 4) or musician's cramp (n = 5) adapted their grip force when lifting a new object or catching a weight. METHODS: Nine patients with focal hand dystonia and 10 controls were studied. Experiments addressed different motor behaviours: (A) lifting and holding an object; (B) adjusting grip force in anticipation of or in reaction to a change in load force by catching a small weight dropped expectedly or unexpectedly into a hand held receptacle. RESULTS: In (A), patients produced a grip force overshoot during the initial lifts; force overflow was most pronounced in those with writer's cramp. Patients and controls adjusted their grip force to object weight within one or two lifts, though patients settled to a steady force level above normal. In (B), patients with focal hand dystonia and normal controls showed similar predictive grip force adjustments to expected changes in object load, suggesting that this aspect of sensory-motor integration was normal. Patients had a shorter latency of grip force response than controls after an unexpected load increase, reflecting either a greater level of preparatory motor activity or a disinhibited spinal reflex response. CONCLUSIONS: The overall increased grip force in patients with focal hand dystonia is likely to be a prelearned phenomenon rather than a primary disorder of sensory-motor integration.     

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.     

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.     

Parametric control of fingertip forces during precision grip lifts in children with DCD (developmental coordination disorder) and DAMP (deficits in attention motor control and perception)

Twenty boys with developmental coordination disorder (DCD), 11 of whom had associated attention deficit disorder (ADD), were compared with an age-matched control group of 12 boys to examine mechanisms that adapt the grip force at the digit-object interface in a precision grip task. An experimental grip object equipped with pressure transducers registered the grip forces (normal to the surface) and the load force (tangential to the surface) generated by the fingertips. The surface of the object was changed to vary the frictional properties. Both study groups exhibited disturbances of the basic coordination of forces in the initial phase of the movement, manifested by longer time latencies and higher force levels than the control group. All subjects were able to adapt the force output in response to the friction at the digit-object interface. Higher grip forces and safety margins were documented for the DCD group in comparison to the controls. Furthermore, there was greater variation in the parametric control of the grip force in the DCD group. The results suggest that the control of the grip force is similar in children with DCD, regardless of whether they have associated ADD or not, but it is impaired in comparison to that of controls.     

Impaired grip force modulation in the ipsilesional hand after unilateral middle cerebral artery stroke

Understanding grasping control after stroke is important for relearning motor skills. The authors examined 10 individuals (5 males; 5 females; ages 32-86) with chronic unilateral middle cerebral artery (MCA) stroke (4 right lesions; 6 left lesions) when lifting a novel test object using skilled precision grip with their ipsilesional ("unaffected") hand compared to healthy controls (n = 14; 6 males; 8 females; ages 19-86). All subjects possessed normal range of motion, cutaneous sensation, and proprioception in the hand tested and had no apraxia or cognitive deficits. Subjects lifted the object 10 times at each object weight (260 g, 500 g, 780 g) using a moderately paced self-selected lifting speed. The normal horizontal ("grip") force and vertical tangential ("lift") force were separately measured at the thumb and index finger. Regardless of the object weight or stroke location, the stroke group generated greater grip forces at liftoff of the object (> or =39%; P < or = 0.05) and across the dynamic (P < or = 0.05) and static portions (P < or = 0.05) of the lifts compared to the healthy group. Peak lift forces were equivalent between groups, suggesting accurate load force information processing occurred. These results warrant further investigation of altered sensorimotor processing or compensatory biomechanical strategies that may lead to inaccurate grip force execution after strokes.     

Distal and proximal prehension is differentially affected by Parkinson‘s disease

Prehension movements consist of distal (grasp) and proximal (reach, lift) components. The proximal lifting movements (achieved at the wrist) of patients with Parkinson’s disease (PD) are characterized by bradykinesia. With respect to the distal component, PD patients show pathologically high grip forces (generated by the fingers) and slowing of force development indicative of disturbed sensorimotor adjustments during prehension. Combining kinematic and force analyses of prehension movements, we investigated whether PD differentially affects the adjustments of the distal or proximal prehension components to current load conditions. First, PD patients (n = 12) and healthy, age-matched control subjects grasped and lifted light and heavy objects without any load cues. Then, they were presented with cues that indicated changes in object load. These load cues were either consciously perceived or rendered subconscious through use of the technique of metacontrast masking. Consistent with the functional organization of the basal ganglia, patients with PD could adapt distal prehension components (grip force) to current load conditions using both types of cues. However, they were impaired in adjusting proximal prehension components (lift velocity). While controls were able to normalize lift velocity with the help of both conscious and subconscious load cues, the PD patients could use neither form of cue, and retained a pathological overshoot in lift velocity. Our results demonstrate that visuomotor integration during prehension movements differs at distal and more proximal joints and that deficits in this integration are pronounced for the latter in Parkinson’s disease.     

The beneficial effects of subthalamic nucleus stimulation on manipulative finger force control in Parkinson's disease

We investigated the differential effects of levodopa medication and STN stimulation on finger force control in Parkinson subjects grasping to lift an object and performing vertical point-to-point movements of a hand-held object. The experiments were conducted in four treatment conditions: off-drug/off-stimulation, off-drug/on-stimulation, on-drug/off-stimulation and on-drug/on-stimulation. We found that the bradykinesia in Parkinsonian subjects improved by both levodopa medication and STN stimulation. As compared to healthy subjects, excessive grip force was observed in all Parkinson subjects, regardless of the treatment condition. This force excess was most pronounced in the on-drug condition and ameliorated by STN stimulation. We observed reliable correlations between the amount of force overflow and the severity of levodopa-induced dyskinesias in the on-drug condition. Despite some similarities regarding therapeutic effects on bradykinesia, our findings contrast with earlier observations with respect to the differential effects of levodopa and STN stimulation on the scaling of fingertip forces in Parkinson's disease. While levodopa causes an overshoot of fingertip forces, STN stimulation appears to be sufficient to alleviate, but not normalise the force excess. STN stimulation enables Parkinson subjects to scale grip force more accurately to the loads arising from voluntary manipulation of hand-held objects.     

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.     

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 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.