Hand preshaping in Parkinson’s disease: effects of visual feedback and medication state

Abstract

Previous studies in our laboratory examining pointing and reach-to-grasp movements of Parkinson's disease patients (PDPs) have found that PDPs exhibit specific deficits in movement coordination and in the sensorimotor transformations required to accurately guide movements. We have identified a particular difficulty in matching unseen limb position, sensed by proprioception, with a visible target. In the present work, we further explored aspects of complex sensorimotor transformation and motor coordination using a reach-to-grasp task in which object shape, visual feedback, and dopaminergic medication were varied. Normal performance in this task requires coordinated generation of appropriate reach, to bring the hand to the target, and differentiated grasp, to preshape the hand congruent with object form. In Experiment 1, we tested PDPs in the off-medication state. To examine the dependence of subjects on visual feedback and their ability to implement intermodal sensory integration, we required them to reach and grasp the target objects in three conditions: (1) Full Vision, (2) Object Vision with only the target object visible and, (3) No Vision with neither the moving arm nor the target object visible. PDPs exhibited two types of deficits. First, in all conditions, they demonstrated a generalized slowing of movement or bradykinesia. We consider this an intensive deficit, since it involves largely a modulation of the gain of specific task parameters: in this case, velocity of movement. Second, they were less able than controls to extract critical proprioceptive information and integrate it with vision in order to coordinate the reach and grasp components of movement. These deficits which involve the coordination of different inputs and motor components, we classify as coordinative deficits. As in our previous work, the PDPs' deficits were most marked when they were required to use proprioception to guide their hand to a visible target (Object Vision condition). But even in the full-vision condition, their performance only became fully accurate when both the target and effector (hand) were simultaneously visible. In Experiment 2, PDPs were tested on their dopaminergic replacement therapy. Dopaminergic treatment significantly ameliorated the bradykinesia of the PDPs, but produced no changes in the hand preshaping deficiencies of PDPs. These results suggest that adequate treatment of the PDPs may more readily compensate for intensive, than coordinative deficits, since the latter are likely to depend on specific and time-dependent neural interdependencies that are unlikely to be remediated simply by increasing the gain of a pathway.

Dopamine replacement therapy does not restore the ability of Parkinsonian patients to make rapid adjustments in motor strategies according to changing sensorimotor contexts

“…akinesia and bradykinesia [9][10][11], rigidity [12,13], and resting tremor [9,10,14], but has shown modest effects on restoring coordinated movements when demands on precision are high, such as for prehensile actions or reaching/ pointing toward a target. For example, dopamine replacement therapy failed to improve some aspects of reach-to-grasp actions [15,16] and reaching movements [17,18], and even led to increased spatial errors [11]. Disruptions in movement amplitude and velocity, which we have termed intensive aspects of movement, may be amendable to dopamine replenishment therapy [15] perhaps due to thalamo-cortical disinhibition resulting in an increase of BGthalamocortical signals to the primary and supplementary motor areas [19].…”

“…For example, dopamine replacement therapy failed to improve some aspects of reach-to-grasp actions [15,16] and reaching movements [17,18], and even led to increased spatial errors [11]. Disruptions in movement amplitude and velocity, which we have termed intensive aspects of movement, may be amendable to dopamine replenishment therapy [15] perhaps due to thalamo-cortical disinhibition resulting in an increase of BGthalamocortical signals to the primary and supplementary motor areas [19]. Conversely, other coordinative aspects of an action may be resistive to pharmacotherapy since these aspects may not be restored by a simple facilitation of the BG-thalamo-cortical pathways [15].…”

Finger tapping movements of Parkinson’s disease patients automatically rated using nonlinear delay differential equations

“…The impairment in voluntary movement in PD is characterized by a number of specific sensorimotor processing deficits, including a generalized slowness of movement; 3 a difficulty in carrying out sequential movements; 4 a reliance on sensory input, particularly visual input, to guide and correct movement; 5,6 and difficulties in timing, synchronizing, and coordinating movements. [7][8][9] Since Parkinson's disease is a degenerative disease, an effective tool is needed to track changes in its severity and the effectiveness of remedial treatments. Clinical evaluations can be costly and difficult to execute consistently over the long duration of the disease.…”

Hand Function in Parkinson’s Disease

“…Invasive procedures, such as DBS of the subthalamic nucleus show improvements of motor performance in many patients (for meta-analysis, see Boucai et al [ 123 ]). A recent study by Schettino et al [ 124 ] showed that STN DBS resulted in a more normal pattern of hand preshaping when reaching to grasp an object, a pattern not seen with dopaminergic therapy in a previous study [ 8 ]. Specifi cally, when reaching towards an object that was convex on one side (Fig.…”

“…Thus, when visual feedback of the object and/or the hand is removed during the reach, PD patients take signifi cantly longer to transport the hand to the object, especially at close range to the target, while producing a greater than normal grip aperture [ 64 ]. Removal of visual feedback of the hand during the reach also exacerbates inappropriate hand preshaping and results in signifi cantly more failed grasps [ 8 ].…”