Impaired proactive and reactive grip force control in chronic hemiparetic patients.

OBJECTIVES: The aim of the study was to test manipulative capacities of hemiparetic patients with partial recovery in a drawer task. The main objective was to assess adjustments of grip force in the face of load perturbations. METHODS: The task was to pull and to hold the drawer manipulandum during predictable or unpredictable perturbations with short (90 ms) load pulses (factor set). RESULTS: The following novel observations were made. (1) Load pulses elicited, at a latency of about 70 ms, a transient grip force response and a corresponding phasic EMG response. These reactive adjustments were larger during holding than during pulling (factor task). In patients, the reactive grip force adjustments and the EMG response in the grip muscles were reduced. (2) The above deficit was set-dependent. (3) With regular perturbations, grip force was scaled already before perturbation onset. This proactive adjustment was greatly reduced in the patient group. (4) Coordination between grip force and pull force before onset of the perturbation was also disturbed in the patients who generated less grip force per unit pull force than control subjects. CONCLUSIONS: It is concluded that the patients had difficulties in adapting proactively and reactively to external load disturbances, in addition to their hand weakness.     

Predictive and reactive finger force control during catching in cerebellar degeneration

We investigated how patients with cerebellar degeneration control fingertip forces to resist a perturbation imposed on a handheld load. Patients and healthy sex- and age-matched control subjects held an instrumented receptacle between the index finger and thumb. A weight was dropped into the receptacle either unexpectedly from the experimenter's hand with the subject being blindfolded or expectedly from the subject's opposite hand. This paradigm allowed us to study predictive and reactive modes of finger force control. Patients generated an overshoot of grip force, irrespective of whether the weight was dropped expectedly or unexpectedly. When the weight was dropped from the experimenter's hand, grip force lagged behind the load perturbation at impact in patients and controls. When the weight was dropped expectedly from the subject's opposite hand, healthy subjects started to increase grip force prior to the release of the weight. This observation is indicative for a predictive mode of force control. In contrast, the grip force profile of cerebellar patients was not processed in anticipation of the time of impact when the weight was dropped from the opposite hand. Our data suggest involvement of cerebellar circuits in a predictive, but less in a reactive, mode of fingertip force control during manipulative behavior.     

Prehension Kinematics,Grasping Forces,and Independent Finger Control in Mildly Affected Patients with Essential Tremor

Although the pathophysiology of essential tremor (ET), one of the most common movement disorders, is not fully understood, evidence increasingly points to cerebellar involvement. To confirm this connection, we assessed the everyday hand and finger movements of patients with ET, as these movements are known to be affected in cerebellar diseases. In 26 mildly affected patients with ET (compared to age- and gender-matched controls), kinematic and finger force parameters were assessed in a precision grip. In a second task, independent finger movements were recorded. The active finger had to press and release against a force-sensitive keypad while the other fingers stayed inactive. Finally, control of grip force to movement-induced, self-generated load changes was studied. Transport and shaping components during prehension were significantly impaired in patients with ET compared to controls. No significant group differences were observed in independent finger movements and grip force adjustments to self-generated load force changes. However, in the latter two tasks, more severely affected ET patients performed worse than less affected. Although observed deficits in hand and finger movement tasks were small, they are consistent with cerebellar dysfunction in ET. Findings need to be confirmed in future studies examining more severely affected ET patients.     

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.     

Impairments of prehension kinematics and grasping forces in patients with cerebellar degeneration and the relationship to cerebellar atrophy

OBJECTIVE: This study established the relationship between kinematic and grip force parameters in prehension tasks, disease severity and cerebellar atrophy in patients with cerebellar degeneration. METHODS: Prehension was tested in a condition during which the hand reached out, grasped, and lifted an object. Task complexity was modified by limiting the transport component to a single-joint movement, and introducing a bimanual condition. RESULTS: Compared to controls the cerebellar patients showed disturbances in hand transport, in hand shaping and the most pronounced in time to peak grip force and the grip/load force coupling. Task-dependent changes did not differ between groups. Ataxia scores revealed significant correlations with hand transport and shaping measures only. Ataxia subscores correlated with volume reduction of appropriate longitudinal cerebellar zones. Volume reduction of the intermediate zone was associated with grip force coordination deficits. CONCLUSIONS: Results indicate that the cerebellum may have a more general role in motor control of grasping independent of task complexity. Temporal and coordinative measures of grip force appear to be most useful to assess the severity of grasping deficits in patients with cerebellar degeneration not detectable by clinical ataxia scales. SIGNIFICANCE: To assess the severity and course of cerebellar disease grip force control in a standard prehension task is a sensitive quantitative measure.     

Different modes of grip force control: voluntary and externally guided arm movements with a hand-held load.

OBJECTIVE: When we move hand-held objects that exhibit stable physical properties grip force is regulated in anticipation of movement-induced inertial loads. In contrast, when the object's behaviour is unpredictable, grip force is adjusted in response to sensory feedback with the consequence that grip tends to lag behind load. Previous studies analysed reactive and predictive grip force behaviour by systematically varying the predictability of the physical object properties. METHODS: This study examines if anticipatory force control also depends on the predictability of the limb dynamics interfering with external objects. The coupling between grip and load force profiles was comparatively analysed during voluntary and externally guided vertical arm movements with an instrumented hand-held object. Voluntary and externally guided movements were performed with and without visual feedback. RESULTS: During voluntary arm movements grip force was precisely regulated in anticipation of movement-induced inertial load fluctuations with grip force increasing in parallel with load force without an obvious time delay. In contrast, during externally guided movements grip force was regulated in reaction to the imposed load fluctuations. However, the reflex-mediated grip force responses were still flexible to account for the differential loading requirements of movement direction. There was no difference of grip force performance between movements performed with and without visual feedback. CONCLUSIONS AND SIGNIFICANCE: The results suggest that predictability of both the external object and the dynamics of the own body is essential to establish an anticipatory mode of grip force regulation. Unpredictability of the own limb dynamics results in a reactive mode of grip force control. Reactive grip force control appears to be both highly automatised and flexible reflecting differential loading requirements of movement direction.     

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 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.     

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.     

Objective evaluation of manual performance deficits in neurological movement disorders

Impaired hand function is a frequent finding in movement disorders. The skilled control of prehensile finger forces is an essential feature of tool use in daily life. In healthy subjects, grip force is precisely adjusted to the mechanical object properties, such as weight and surface friction. Grip force is accurately scaled to be only a small amount higher than the minimum necessary to prevent a hand-held object from slipping. When an object is lifted and moved around in space, grip force is modulated in parallel with the movement-induced fluctuations in load. The absence of a temporal delay between grip and load force profiles implies that the central nervous system is able to predict the load variations before the intended manipulation. Sensory information is used to adjust the level of applied finger forces efficiently to the requirements of the mechanical object properties and the task at hand. The characteristics of impaired finger force control include inefficient grip force scaling and imprecision of the temporal coupling between grip and load force profiles. Here, we review the characteristics of deficient grip force behavior in movement disorders, e.g. Parkinson's disease, task-specific dystonia, Gille de la Tourette's syndrome and cerebellar disease. Grip force analysis is a highly sensitive method to document even subtle impairments of finger force control and may be used both as a diagnostic tool and for the objective evaluation of treatment in neurological movement disorders.     

BASIC CO-ORDINATION OF MANIPULATIVE FORCES OF CHILDREN WITH CEREBRAL PALSY

The coordination of manipulatory forces during prehension was studied in 12 children with cerebral palsy (CP) and compared with that of controls. The results indicated that coupling of grip force and load force does not develop in children with CP. These children's force development increased in stages, with an early onset of excessive grip force. They did not use anticipatory control of the isometric force development during the load phase. Prolonged delays between successive phases indicated inefficient sensory feedback during the movement. The early onset of grip force and the over-all high force employment may compensate for the lack of anticipatory control and inefficient sensorimotor integration.     

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.     

Grip force scaling and sequencing of events during a manipulative task in Huntington's disease

The aim of the study was to investigate force regulation and sequencing of events in Huntington's disease (HD) patients when performing a drawer opening task using the precision grip. Results revealed that HD patients used excessive grip force levels that were unrelated to the actual task demands. Also, they demonstrated a higher grip force value at load force onset in addition to an increased delay between initiation of grip force and load (pulling) force. These data indicate a deficit in the coordinated activation of both forces due to HD. Furthermore, the patients showed bradykinesia along with a prolonged interval between the movement phases underlying the task, denoting an impairment in encoding serially ordered events. Together, these results illustrate the deteriorating effect of striatal pathology on manual function. Accordingly, an amended control of grasping forces and serial encoding of movement-related events due to HD are likely to affect the proficiency of common manipulative skills.     

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.     

Role of the primary motor and sensory cortex in precision grasping: a transcranial magnetic stimulation study

Human precision grip requires precise scaling of the grip force to match the weight and frictional conditions of the object. The ability to produce an accurately scaled grip force prior to lifting an object is thought to be the result of an internal feedforward model. However, relatively little is known about the roles of various brain regions in the control of such precision grip-lift synergies. Here we investigate the role of the primary motor (M1) and sensory (S1) cortices during a grip-lift task using inhibitory transcranial magnetic theta-burst stimulation (TBS). Fifteen healthy individuals received 40 s of either (i) M1 TBS, (ii) S1 TBS or (iii) sham stimulation. Following a 5-min rest, subjects lifted a manipulandum five times using a precision grip or completed a simple reaction time task. Following S1 stimulation, the duration of the pre-load phase was significantly longer than following sham stimulation. Following M1 stimulation, the temporal relationship between changes in grip and load force was altered, with changes in grip force coming to lag behind changes in load force. This result contrasts with that seen in the sham condition where changes in grip force preceded changes in load force. No significant difference was observed in the simple reaction task following either M1 or S1 stimulation. These results further quantify the contribution of the M1 to anticipatory grip-force scaling. In addition, they provide the first evidence for the contribution of S1 to object manipulation, suggesting that sensory information is not necessary for optimal functioning of anticipatory control.     

The contribution of non-digital afferent signals to grip force adjustments evoked by brisk unloading of the arm or the held object.

OBJECTIVE: Earlier studies suggest that grip force adjustments evoked by mechanical perturbations result more from cutaneous signals from the fingertips, than from afferent signals from the supporting limb. Generally an increase in tangential load at the fingertips induces an increase in grip force, whereas a decrease in load induces the opposite reaction. Some data suggest that prior knowledge and experience influences the magnitude of grip force adjustments. METHODS: This study examines the relative contribution of digital and arm afferent signals in the context of brisk involuntary upward flexions obtained either by unloading the arm (ARM) or the held object (OBJECT). Following the perturbation, the tangential load at the fingertips increased in ARM, but decreased in OBJECT. A subsidiary goal was to compare the performance of naive subjects with the performance of trained and informed subjects. RESULTS: When the perturbation was completely unexpected, grip force increased sharply after OBJECT and ARM unloading. By contrast, when subjects had prior knowledge and experience with the upcoming perturbation, grip responses were clearly differentiated; grip force increased after ARM, but decreased after OBJECT. CONCLUSIONS: These results challenge the view that cutaneous signals of the fingertips are the driving signals of grip force responses. Instead, afferent signals from the flexed arm would account well for the lack of difference between grip force responses in ARM and OBJECT under unpredictable conditions. These data provide clear evidence that prior knowledge and experience influences reactive grip force control, since subjects became able to repress unnecessary grip force modulation in OBJECT. SIGNIFICANCE: These data have implications for understanding the initiation and the modulation of grip force adjustments.     

Impairments in precision grip correlate with functional measures in adult hemiplegia.

OBJECTIVE: Analysis of a precision grip-lift task provides measures to assess functional disability of the hand, but the correlation between these measures and accepted tests of motor function in stroke patients has not been established. METHODS: Seventeen subacute stroke patients were studied to compare parameters of a precision grip-lift task between the affected and unaffected side, and to correlate them with function. Functional impairment was assessed with the Action Research Arm Test and the Fugl-Meyer assessment, as well as grip strength and maximal finger-tapping speed. The grip force (GF) and load force (LF) were recorded as patients lifted a custom-built manipulandum. All measures were recorded on two separate occasions, at least 1 week apart. RESULTS: There was good reproducibility between testing sessions for the grip-lift and functional measures. The affected hand gripped the manipulandum for longer prior to lift-off than the unaffected hand, and the normal close temporal coupling between the rate of change of GF and LF during the lift was disrupted. These two measures correlated more highly with the ARAT than the FMA and, when combined with measures of grip strength and tapping speed, explained 71% of the variance of the ARAT. CONCLUSIONS: The grip-lift task is a sensitive measure of impaired dexterity following stroke and provides measures which correlate well with a commonly applied functional assessment scale. SIGNIFICANCE: This task may be used clinically to detect changes in the hemiplegic upper limb during rehabilitation and recovery.     

Disturbed sensorimotor processing during control of precision grip in patients with writer's cramp.

The aim of the study was to investigate force regulation in patients with writer's cramp when performing a drawer-opening task using the precision grip. Experimental conditions included intervening load pulses and vibratory manipulations for examining grip force responses to sensory disturbances. The data revealed that grip force was increased in patients with writer's cramp compared with normal subjects, with a stronger modulation in the symptomatic compared with the asymptomatic hand. This denotes a change in force scaling capabilities and most notably for the preferred hand used in manipulative activities. Vibratory stimulation of the extrinsic hand/finger muscles resulted in an increased grip force of both hands in the patients with writer's cramp. The latter was not observed in normal subjects and supports a bilateral dysfunction in sensorimotor integration resulting from focal dystonia. In conclusion, the disturbed regulation of the precision grip during a drawer-opening task is illustrative for the inability of patients with writer's cramp to efficiently control the force output during manipulative activities.     

Cutaneous afferent activity in the median nerve during grasping in the primate

Neural activity was recorded from the median nerve of a monkey during grasping and lifting, using a chronically implanted cuff electrode. At the onset of lifting, there was an initial dynamic response during which the intensity of the neural signal increased rapidly. This neural response attained its peak value well before the displacement, the load force or the grip force. The time course and peak of the rectified, integrated neurogram were best correlated with the rate of change of grip force. The neural activity declined exponentially to a steady value following the initial peak. During steady holding the mean amplitude of the neurogram was best correlated with the mean grip force. At the end of the holding phase there was a short burst of neural activity as the monkey relaxed the grip force and released the object. During some blocks of trials pulse perturbations were applied to the object. When the monkey did not increase the grip force in advance of the perturbation, the perturbation produced a relatively large displacement of the object and a burst of neural activity whose onset coincided with the onset of displacement. When the monkey anticipated the perturbation by increasing the grip force during the holding period preceding the perturbation, the perturbation produced a relatively small displacement and relatively little increase in neural activity.     

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.