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

doi:10.1016/j.neuropsychologia.2005.04.003

Neuropsychologia

Volume 43, Issue 9, 2005, Pages 1379-1384

https://doi.org/10.1016/j.neuropsychologia.2005.04.003 Get rights and content

Abstract

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

Introduction

Wolpert and colleagues have proposed a general computational model that explains the formation of memorial representations of movement (Wolpert & Ghahramani, 2000; Wolpert & Kawato, 1998). With respect to lifting tasks, the basic concept of this model is that as the movement unfolds, multiple forward models are run that mimic the motor outputs used to pick up the object. Each forward model generates a predicted sensory feedback that should be received from the digits. Furthermore, each of the forward models is coupled with an inverse model, which, if the sensory feedback matches the predicted feedback, will be selected, stored and used to determine appropriate motor commands for subsequent interactions with similar objects. Johansson and Cole (1994) have proposed a comparable feed-forward model for grasp control. In their view, the forward model contains a set of correction commands in addition to the principal motor command that could be accessed quickly if the predicted and actual sensory feedback does not match.

Based on work with patients with cerebellar dysfunction, the cerebellum was the proposed site for the forward model (Miall, Weir, & Stein, 1993). The basal ganglia (BG) have also been shown to be involved in higher order aspects of motor control such as planning a movement, the initiation of internally generated movements, and the execution of complex motor synergies (Stelmach & Phillips, 1991). Furthermore, the BG is thought to be involved in the comparison of the peripheral feedback with the efferent motor program copy generated in the frontal fields (Hikosaka & Wurtz, 1983). Jueptner and Weiller (1998) who investigated the roles of the BG and the cerebellum in the processing of afferent information have challenged this view. The authors concluded that the cerebellum, and not the BG is involved in the on-line control of evolving movement. In addition (Weiller et al., 1996) have demonstrated that the BG did not show any increases in activation during passive elbow flexion (afferent sensory information only) in contrast to active flexion (afferent sensory and efferent motor information), and instead only the cerebellum was activated. This was taken as evidence that the BG were not the site for feedback information processing. Together these studies suggest that the BG are not used to control movement based on sensory feedback, but rather they are concerned with the selection of appropriate movement synergies (Jueptner & Weiller, 1998). Thus, based on the study by Jueptner and Weiller (1998), it could be hypothesized that the cerebellum is the major site of feedback information processing for optimizing the internal forward model. However, since the BG are mainly concerned with the selection of movement and complex muscle synergies (Kandel, Schwartz, & Jessell, 1991), it is possible that they play a key role in releasing corrective responses in the feed-forward control of grasp (Johansson & Cole, 1994) for on-line corrections.

Gordon, Forssberg, Johansson, and Westling (1991) have shown that when lifting objects of varying dimensions, the size of the object influences the peak grip force exerted on it, such that large objects are lifted with higher peak grip forces than small ones. This finding suggests that programming of grip forces is dependent on the integration of visual and tactile information. In the present study, both healthy control individuals and an individual with unilateral BG damage (RI), lifted objects of various sizes that had the same mass (Flanagan & Beltzner, 2000; Mon-Williams & Murray, 2000). Based on the findings of Gordon et al. (1991) and on the suggested roles of the BG and cerebellum in the control of grip forces, we hypothesized that if BG damage affects the integration of vision and the sense of touch, RI's contralesional hand should show no scaling of peak grip force to object size, and possibly over-gripping that would be related to increased safety margins.

Section snippets

Participants

RI was a 28 year old, right-handed, health professional who had suffered a left subcortical ischemic stroke more than a year prior to testing. The infarct was centered on the left putamen, but extended anteriorally through the anterior internal capsule into the head of the ventral caudate and medially into the external segment of the globus pallidus (refer to Fig. 1). He made a very good recovery and was neurologically intact except for mild decreased finger dexterity in the right hand and

Controls

For the analysis of peak grip force for the controls there was only a significant main effect for object size, F(2,94) = 34.6, p < 0.01. The least amount of grip force was produced when lifting the small object (M = 5.6 N, S.E. = 0.41), an intermediate amount was produced when lifting the medium object (M = 6.2 N, S.E. = 0.44), and the most force was produced when lifting the large object (M = 7.4 N, S.E. = 0.51). There were no main effects or interactions with hand (refer to Fig. 3, Fig. 4). This pattern is

Acknowledgement

Financial support: Natural Science and Engineering Council of Canada research grant awarded to Heather Carnahan.

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Cited by (7)

Functional lateralization in cingulate cortex predicts motor recovery after basal ganglia stroke
2016, Neuroscience Letters
Citation Excerpt :
An altered balance of facilitatory and inhibitory influence on the function of frontal cortex was conceived as effects of basal ganglia dysfunction [4]. Dubrowski et al. reported a single chronic stroke patient with a failure to integrate sensory information in motor programming after a unilateral BG damage [5]. However, functional neuroimaging studies are rare on patients with BG stroke, which would reveal the isolated effects of BG damage on motor control.
The basal ganglia (BG) is involved in higher order motor control such as movement planning and execution of complex motor synergies. Neuroimaging study on stroke patients specifically with BG lesions would help to clarify the consequence of BG damage on motor control. In this paper, we performed a longitudinal study in the stroke patients with lesions in BG regions across three motor recovery stages, i.e., less than 2week (Session 1), 1–3 m (Session 2) and more than 3 m (Session 3). The patients showed an activation shift from bilateral hemispheres during early sessions (<3 m) to the ipsilesional cortex in late session (>3m), suggesting a compensation effect from the contralesional hemisphere during motor recovery. We found that the lateralization of cerebellum(CB) for affected hand task correlated with patients' concurrent Fugl-Meyer index (FMI) in Session 2. Moreover, the cingulate cortex lateralization index in Session 2 was shown to significantly correlate with subsequent FMI change between Session 3 and Session 2, which serves as a prognostic marker for motor recovery. Our findings consolidated the close interactions between BG and CB during the motor recovery after stroke. The dominance of activation in contralateral cingulate cortex was associated with a better motor recovery, suggesting the important role of ipsilesional attention modulation in the early stage after BG stroke.
The impact of unilateral brain damage on anticipatory grip force scaling when lifting everyday objects
2014, Neuropsychologia
Citation Excerpt :
A trend for prolonged loading times in LBD patients may be indicative of mild general hesitations, it did however not correlate with deficits in anticipation (see Section 3.2). Also an increased average grip force level could not be a confound leading to imprecise force scaling since the average force level was similar in control subjects and patients groups (Dubrowski et al., 2005). The finding of normal average grip force levels is in contrast with reports of increased ipsilesional grip forces in stroke patients during comparable lifting task with the ipsilesional hand (Nowak et al., 2007; Quaney, Perera, Maletsky, Luchies, & Nudo, 2005).
The scaling of our finger forces according to the properties of manipulated objects is an elementary prerequisite of skilled motor behavior. Lesions of the motor-dominant left brain may impair several aspects of motor planning. For example, limb-apraxia, a tool-use disorder after left brain damage is thought to be caused by deficient recall or integration of tool-use knowledge into an action plan. The aim of the present study was to investigate whether left brain damage affects anticipatory force scaling when lifting everyday objects. We examined 26 stroke patients with unilateral brain damage (16 with left brain damage, ten with right brain damage) and 21 healthy control subjects. Limb apraxia was assessed by testing pantomime of familiar tool-use and imitation of meaningless hand postures.
Participants grasped and lifted twelve randomly presented everyday objects. Grip force was measured with help of sensors fixed on thumb, index and middle-finger. The maximum rate of grip force was determined to quantify the precision of anticipation of object properties.
Regression analysis yielded clear deficits of anticipation in the group of patients with left brain damage, while the comparison of patient with right brain damage with their respective control group did not reveal comparable deficits. Lesion-analyses indicate that brain structures typically associated with a tool-use network in the left hemisphere play an essential role for anticipatory grip force scaling, especially the left inferior frontal gyrus (IFG) and the premotor cortex (PMC). Furthermore, significant correlations of impaired anticipation with limb apraxia scores suggest shared representations. However, the presence of dissociations, implicates also independent processes.
Overall, our findings suggest that the left hemisphere is engaged in anticipatory grip force scaling for lifting everyday objects. The underlying neural substrate is not restricted to a single region or stream; instead it may rely on the intact functioning of a left hemisphere network that may overlap with the left hemisphere dominant tool-use network.
Size-weight illusion and anticipatory grip force scaling following unilateral cortical brain lesion
2011, Neuropsychologia
Citation Excerpt :
Against the authors’ expectation, the size–weight illusion as well as the anticipatory scaling of the grip force was preserved in the cerebellar patients (Rabe et al., 2009). A single case study of a patient with unilateral basal ganglia damage reported grip forces of the contra-lesional hand that did not anticipate the different object sizes in a SWI paradigm, suggesting a role of the basal ganglia in force scaling (Dubrowski, Roy, Black, & Carnahan, 2005). However, the first lift was not reported and overall exaggerated force may have been a confounding factor.
The prediction of object weight from its size is an important prerequisite of skillful object manipulation. Grip and load forces anticipate object size during early phases of lifting an object. A mismatch between predicted and actual weight when two different sized objects have the same weight results in the size–weight illusion (SWI), the small object feeling heavier. This study explores whether lateralized brain lesions in patients with or without apraxia alter the size–weight illusion and impair anticipatory finger force scaling.
Twenty patients with left brain damage (LBD, 10 with apraxia, 10 without apraxia), ten patients with right brain damage (RBD), and matched control subjects lifted two different-sized boxes in alternation. All subjects experienced a similar size–weight illusion. The anticipatory force scaling of all groups was in correspondence with the size cue: higher forces and force rates were applied to the big box and lower forces and force rates to the small box during the first lifts. Within few lifts, forces were scaled to actual object weight. Despite the lack of significant differences at group level, 5 out of 20 LBD patients showed abnormal predictive scaling of grip forces. They differed from the LBD patients with normal predictive scaling by a greater incidence of posterior occipito-parietal lesions but not by a greater incidence of apraxia.
The findings do not support a more general role for the motor-dominant left hemisphere, or an influence of apraxia per se, in the scaling of finger force according to object properties. However, damage in the vicinity of the parietal–occipital junction may be critical for deriving predictions of weight from size.
Basal ganglia mechanisms underlying precision grip force control
2009, Neuroscience and Biobehavioral Reviews
The classic grasping network has been well studied but thus far the focus has been on cortical regions in the control of grasping. Sub-cortically, specific nuclei of the basal ganglia have been shown to be important in different aspects of precision grip force control but these findings have not been well integrated. In this review, we outline the evidence to support the hypothesis that key basal ganglia nuclei are involved in parameterizing specific properties of precision grip force. We review literature from different areas of human and animal work that converges to build a case for basal ganglia involvement in the control of precision gripping. Following on from literature showing anatomical connectivity between the basal ganglia nuclei and key nodes in the cortical grasping network, we suggest a conceptual framework for how the basal ganglia could function within the grasping network, particularly as it relates to the control of precision grip force.
Grip forces isolated from knowledge about object properties following a left parietal lesion
2007, Neuroscience Letters
When lifting two objects with equal weight but different size, we judge the smaller object to be heavier. This size–weight illusion has been intensively tested by the recruitment of fingertip grip forces during precision lifting. Previous findings have suggested that perceptual (object size) prediction can influence sensorimotor prediction (anticipatory grip force scaling to the object size) but these predictions could be processed independently. This study investigates whether the anticipatory scaling of the grip forces according to object properties critically depends on the integrity of the posterior parietal cortex (PPC) and how a deficit may affect the perceptual size–weight illusion. Here, we report the case of a patient, F.S., with a large left temporal parietal lesion intruding into the temporal cortex and limb apraxia, who did not show anticipatory scaling of fingertip grip force to object size whereas matched controls did. However, the patient's perception of the size–weight illusion was only impaired during his ipsi-lesional hand lifting. Our findings suggest that left parietal cortex may be particularly responsible for the anticipatory grip force scaling of both hands and the perceptual process of size–weight illusion involving ipsi-lesional hand motion.
The nature of the sense of effort and its neural substrate
2006, Revue Neurologique
Quels sont la nature et le substratum neural de la perception de la force musculaire volontaire ? État des connaissances. Les données expérimentales démontrent que des signaux efférents dérivés de la commande motrice jouent un rôle dominant dans le processus par lequel la force volontaire est perçue. Ceci signifie que la perception de la force volontaire est réalisée, avant tout, par l’intermédiaire d’un sens de l’effort, et non pas par l’intermédiaire d’un sens de la tension intramusculaire. De nombreuses études montrent néanmoins que les informations en provenance des capteurs sensoriels participent au sens de l’effort. Leur rôle ne consiste pas à engendrer un signal d’effort, mais plutôt à moduler et à calibrer l’intensité de celui-ci. Les études de neuro-imagerie et de neuropsychologie révèlent par ailleurs que de nombreuses structures corticales participent à la perception de la force musculaire volontaire. Perspectives et conclusion Dans ce type de tâche, les ganglions de la base pourraient assurer la mise en cohérence de l’activité corticale.
What are the nature and the neural substrate of voluntary force perception? State of art. Experimental findings demonstrate that efferent signals related to motor command play a dominant role in perceiving voluntary muscular force. This suggests that voluntary force perception is provided through a sense of effort and not through a sense of intramuscular tension. Nevertheless, experimental data show that the contribution of sensory input to effort awareness must not be dismissed. Sensory signals are not involved in generating a signal of effort but rather in calibrating and modulating its magnitude. Neuroimaging and neuropsychological studies revealed that many cortical structures are activated during tasks of voluntary muscular force perception. Perspectives and conclusion. In such tasks, the basal ganglia might support the coherence of cortical activity.

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NoteUnilateral basal ganglia damage causes contralesional force control deficits: A case study

Abstract

Introduction

Section snippets

Participants

Controls

Acknowledgement

Experimental Neurology

Brain Research

Neuropsychologia

Neuropsychologia

Neuroimage

Neural Networks

Precision grip and Parkinson's disease

Brain

Independence of perceptual and sensorimotor predictions in the size-weight illusion

Nature Neuroscience

Visual size cues in the programming of manipulative forces during precision grip

Experimental Brain Research

Visual and somatosensory information about object shape control manipulative fingertip forces

Journal of Neuroscience

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