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.     

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.     

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.     

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.     

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.     

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.     

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.     

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 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.     

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.     

Predictive and reactive co-ordination of grip and load forces in bimanual lifting in man

We investigated the intra- and inter-manual coordination of grip force (GF) and load force (LF) during bimanual lifting and holding of a single object. In a voluntary task involving lifting a predictable load (Experiment 1), we showed scaling of GF to LF generated by either hand, similar to effects seen in previous unimanual studies. Moreover, the GF rates generated by the two hands were correlated. In part this correlation was due to the correlation between the LF rates. However, the GF rates remained correlated when the effects of the correlation in LF rates were partialled out. This novel finding suggests an additional co-ordinative constraint at the level of specification of GFs. As a contrast to the predictable loading in the first experiment, in the second experiment loading was temporally unpredictable and elicited reactive increases in GF. In Experiment 2, the intermanual correlation of GF rates was stronger than in Experiment 1. We speculate that this result reflects greater degrees of co-ordinative constraint at lower levels in the motor control hierarchy.     

Role of the cerebellum in tuning anticipatory and reactive grip force responses

The aim of our study was to determine if load perturbations that could destabilize grasp control are adequately controlled by cerebellar patients. We examined patients with unilateral cerebellar lesions who had largely recovered from their initial symptoms and compared grip force regulation for the affected and unaffected hand during a drawer-opening task. Two experimental paradigms were included: (1) a brief load perturbation during a self-stopped drawer pull and (2) a loading impact when the drawer was pulled out to the mechanical stop. The results showed that when a self-stopped movement was perturbed during its trajectory, anticipatory grip force increase was smaller for the affected than for the unaffected hand, illustrating a disturbed gain control due to cerebellar dysfunction. When the mechanical stop arrested the movement, the amount of grip force did not differ significantly between the affected and unaffected side; however, both hands used different control strategies. Whereas the unaffected hand anticipated the load perturbation by a ramp-like increase of grip force toward the impending impact, the affected hand increased grip force at movement onset to a default level and maintained this value until the task was ended. In addition, the latency between impact and reactive peak in grip force was prolonged for the affected hand, suggesting a delayed cerebellar transmission of reactive responses. In conclusion, these findings demonstrate that the cerebellum is involved in anticipatory and reactive mechanisms dealing with load perturbations during goal-directed behavior.     

Object properties and cognitive load in the formation of associative memory during precision lifting

When we manipulate familiar objects in our daily life, our grip force anticipates the physical demands right from the moment of contact with the object, indicating the existence of a memory for relevant object properties. This study explores the formation and consolidation of the memory processes that associate either familiar (size) or arbitrary object features (color) with object weight. In the general task, participants repetitively lifted two differently weighted objects (580 and 280 g) in a pseudo-random order. Forty young healthy adults participated in this study and were randomly distributed into four groups: Color Cue Single task (CCS, blue and red, 9.8(3)cm(3)), Color Cue Dual task (CCD), No Cue (NC) and Size Cue (SC, 9.8(3) and 6(3)cm(3)) group. All groups performed a repetitive precision grasp-lift task and were retested with the same protocol after a 5-min pause. The CCD group was also required to simultaneously perform a memory task during each lift of differently weighted objects coded by color. The results show that groups lifting objects with arbitrary or familiar features successfully formed the association between object weight and manipulated object features and incorporated this into grip force programming, as observed in the different scaling of grip force and grip force rate for different object weights. An arbitrary feature, i.e., color, can be sufficiently associated with object weight, however with less strength than the familiar feature of size. The simultaneous memory task impaired anticipatory force scaling during repetitive object lifting but did not jeopardize the learning process and the consolidation of the associative memory.     

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.     

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     

Deficits in sensorimotor control during precise hand movements in Huntington's disease.

OBJECTIVES: To investigate the performance of patients with Huntington's disease (HD) while manipulating objects using a precision grip. METHODS: The grip forces developed by the fingers were studied while subjects lifted an object of unpredictable weight in the hand. The ability to stabilize grip force after externally imposed weight change was also studied. RESULTS: Patients used higher grip forces than the normal subjects in both the lifting and holding phases, particularly with a lighter weight. Lift timing was slowed in the patients, most markedly with a lighter weight. Increased levels of inter-trial variation were observed only with a light weight. This indicates that the slowing in HD differs from that in Parkinson's disease, which remains constant regardless of object load, and that the slowing in HD is not due to involuntary antagonist muscle activity resulting from an underlying chorea. The grip force response to sudden weight change was normal, but appeared after a delay which increased at lower rates of weight change. CONCLUSIONS: Disturbances in precision grip timing and magnitude in HD may result from a reduced ability to process relevant tactile afferent input. The delay in the adaptive response suggests an increased threshold for detection of weight change in HD. Alternatively, this delay may arise from mediation of the response over an additional cerebellar pathway to compensate for damage to the basal ganglia.     

Evidence for both reaching and grasping activity in the medial parieto-occipital cortex of the macaque

In humans, the caudal pole of the superior parietal lobule is involved in the control of both reaching and grasping movements, whereas in monkey it is reported to be involved only in the control of reaching. Using single-unit recordings from trained macaque monkeys, we investigated whether area V6A, a visuomotor area located in the caudal part of the posterior parietal cortex, is involved in both components of prehension, the hand transport towards the visual target and the grip formation to secure the grasp. In Experiment 1, neural activity was recorded in V6A while two monkeys performed two instructed-delay reaching tasks (reach-to-point and reach-to-grasp) under controlled conditions in darkness. Fourty-five of 93 tested neurons (48%) were modulated during reach-to-point and 62% (52/84) during reach-to-grasp. In 63% of cells (51/81) neural activity was significantly different between reach-to-point and reach-to-grasp tasks, suggesting that grip formation could influence neural activity. In Experiment 2, two monkeys performed natural reach-to-grasp movements in fully lit environment; V6A neural activity and arm-hand movements were recorded by a digital camcorder and analysed frame-by-frame using a digital video technique. Thirty of the 58 tested neurons (52%) were modulated during natural prehension; about 30% of these neurons (8/30) were modulated only during the last phase of prehension, i.e. during finger flexion around the object to be grasped. This is the first direct demonstration that both reaching and grasping modulate neural activity in the caudal part of the posterior parietal cortex of the macaque. Our work suggests a strict functional homology between human and monkey superior parietal lobule.     

Force requirements of observed object lifting are encoded by the observer’s motor system: a TMS study

Several transcranial magnetic stimulation (TMS) studies have reported facilitation of the primary motor cortex (M1) during the mere observation of actions. This facilitation was shown to be highly congruent, in terms of somatotopy, with the observed action, even at the level of single muscles. With the present study, we investigated whether this muscle‐specific facilitation of the observer’s motor system reflects the degree of muscular force that is exerted in an observed action. Two separate TMS experiments are reported in which corticospinal excitability was measured in the hand area of M1 while subjects observed the lifting of objects of different weights. The type of action ‘grasping‐and‐lifting‐the‐object’ was always identical, but the grip force varied according to the object’s weight. In accordance to previous findings, excitability of M1 was shown to modulate in a muscle‐specific way, such that only the cortical representation areas in M1 that control the specific muscles used in the observed lifting action became increasingly facilitated. Moreover, muscle‐specific M1 facilitation was shown to modulate to the force requirements of the observed actions, such that M1 excitability was considerably higher when observing heavy object lifting compared with light object lifting. Overall, these results indicate that different levels of observed grip force are mirrored onto the observer’s motor system in a highly muscle‐specific manner. The measured force‐dependent modulations of corticospinal excitability in M1 are hypothesized to be functionally relevant for scaling the observed grip force in the observer’s own motor system. In turn, this mechanism may contribute, at least partly, to the observer’s ability to infer the weight of the lifted object.     

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.     

Parkinsonian action tremor: interference with object manipulation and lacking levodopa response

It has been postulated that Parkinsonian action tremor is distinct from classical resting tremor and that it may contribute to a loss of manual dexterity in Parkinson's disease. We analyzed pinch grip coordination in 20 patients with Parkinson's disease. An object with and without an additional 500 g weight was grasped, lifted and held for a short time with opposed thumb and index finger. Force sensors recorded the force exerted by both fingers. Spectral analysis of the force traces was performed. Transition times between grasping and lifting the object were measured. 18 age matched normal volunteers served as a control group. While holding the object, there were force oscillations in the 3.5-6.5 Hz band indicating (reemerging) classical Parkinsonian tremor in 65% of the patients. This was reduced to 15-20% under levodopa. Oscillations in the 6-15 Hz band were found in 30% (50% with weight) of the patients, remaining unchanged under levodopa, and in 10% (20% with weight) of the normal controls. During lift initiation, 6-15 Hz oscillations were found in all patients and the majority of controls. The band power was positively correlated with the movement transition times in the severely akinetic patients and was significantly higher than in controls. It remained unchanged under levodopa. Our data confirm that Parkinsonian action tremor activated during complex voluntary movements is distinct from classical resting tremor. It does not show a clear levodopa response but affects dextrous movement coordination when associated with clinically severe overall akinesia.