Music Attenuates Excessive Visual Guidance of Skilled Reaching in Advanced but Not Mild Parkinson's Disease

Whishaw IQ (2009) Music Attenuates Excessive Visual Guidance of Skilled Reaching in Advanced but Not Mild Parkinson's Disease. PLoS ONE 4(8): e6841. doi:10.1371/journal.pone.0006841 Music Attenuates Excessive Visual Guidance of Skilled Reaching in Advanced but Not Mild Parkinson's Disease Lori-Ann R. Sacrey 0 Callie A. M. Clark 0 Ian Q. Whishaw 0 Jun Yan, Hotchkiss Brain Institute, University of Calgary, Canada 0 Canadian Centre for Behavioural Neuroscience, University of Lethbridge , Lethbridge, Alberta Parkinson's disease (PD) results in movement and sensory impairments that can be reduced by familiar music. At present, it is unclear whether the beneficial effects of music are limited to lessening the bradykinesia of whole body movement or whether beneficial effects also extend to skilled movements of PD subjects. This question was addressed in the present study in which control and PD subjects were given a skilled reaching task that was performed with and without accompanying preferred musical pieces. Eye movements and limb use were monitored with biomechanical measures and limb movements were additionally assessed using a previously described movement element scoring system. Preferred musical pieces did not lessen limb and hand movement impairments as assessed with either the biomechanical measures or movement element scoring. Nevertheless, the PD patients with more severe motor symptoms as assessed by Hoehn and Yahr (HY) scores displayed enhanced visual engagement of the target and this impairment was reduced during trials performed in association with accompanying preferred musical pieces. The results are discussed in relation to the idea that preferred musical pieces, although not generally beneficial in lessening skilled reaching impairments, may normalize the balance between visual and proprioceptive guidance of skilled reaching. - Funding: This work was supported by Canadian Institute of Health Research (CIHR) grant to IQW and Natural Sciences and Engineering Research Council (NSERC) grants to IQW and LRS. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Parkinsons disease (PD) is characterized by motor, sensory, and attentional impairments [12], and is related to a progressive degeneration of dopamine producing neurons in the substantia nigra pars compacta [3]. Motor symptoms are manifest in many laboratory-based motor tasks [45] and analogues of real-world tasks [68]. Impairments in movement are often accompanied by impairments in sensation [912]. For example, studies on walking suggest that PD subjects are more dependent on visual guidance than are control subjects [910] and studies on memory-guided pointing demonstrate that PD subjects are less accurate than control subjects in the absence of vision [1112]. It should therefore not be surprising that movement impairment has been shown to improve under sensory cueing [1316]. For example, when pointing to remembered targets, PD subjects make errors, but when given an external visual cue to point at, errors are reduced [17]. Similarly, providing PD subjects with verbal instructions (i.e., take long steps) versus self-selected gait patterns [14,18], or placing lines on the floor to serve as sensory cues [19] can improve cadence, stride length, and velocity of gait. Consequently, it is not always clear the extent to which a given impairment relates to motor, sensory, or attentional deficits. A number of lines of research have examined the effects of music as a sensory cue to assist in overcoming PD deficits [1,15,2022]. Music is shown to lessen whole body bradykinesia to the point that otherwise immobile PD patients can dance and it has also be reported to improve utensil usage [20]. These results suggest a very general beneficial effect of music on whole body movement and skilled movements. At present, it is unclear what aspects of skilled movement are improved under the effects of music. One form of skilled movement, the reach-to-eat task, in which a subject reaches for a small food item, grasps it, and transports it to the mouth for eating, provides a sensitive assay of PD effects on skilled limb movement [2325]. PD subjects are slow to complete the movement [8], are impaired in rotatory movements of the limb, and are impaired in shaping the hand to grasp [23,26]. The impairments persist with medication [24]. The fact that limb movements in reaching are sensitive to the effects of PD and are resistant to improvement with drug medication provides an opportunity for evaluating whether accompanying preferred musical pieces lessens the impairments in sensory and motor control. In the present study, young adult control subjects, age-matched control subjects, and adults with mild and advanced PD were instructed to reach for and eat a small food item. Subjects were fitted with light reflective markers to measure arm and hand movement, wore an eyetracking system to monitor eye movements, and were fitted with goggles that could be manipulated to occlude visual feedback during the reach. On some trials, subjects listened to preferred musical pieces. Synchronized data from the light reflective markers and the eyetracking system were compiled to determine the contribution of visual guidance to skilled reaching, and the effects of preferred musical pieces on skilled reaching, movement element scoring, and visual guidance of skilled reaching. Materials and Methods Subjects On the basis of Hoehn and Yahr (HY) scores [27], PD subjects were divided into two groups, mild PD (HY,2.5; 6 females and 2 males; ages 63.8868.32 years; HY = 1.9360.56) and advanced PD (HY.2.5; 3 females and 4 males; ages 75.0066.68 years; HY = 3.0760.67). Because skilled reaching is not affected by medication [24], the subjects were ON regular medication at the time of testing. For PD subject characteristics, see Table 1. Agematched old adult control (OAC) subjects were recruited from the city of Lethbridge (8 females and 7 males; ages 62.8067.52 to 81.7165.02 years). Eleven young adult control (YAC) subjects (4 females and 7 males; ages 22.2763.85 years) were recruited from the University of Lethbridge campus. All control subjects were selfreported to be of good health with no history of neurological disorder, and had normal or corrected to normal (contact lens) vision. Ethics Statement The University of Lethbridge Human Subject Research Committee approved the study. Rationale for the experiments and testing information were listed on a written consent form that each subject was required to read and sign prior to initiation of testing. The study was conducted in accordance with the Declaration of Helsinki. Reaching Task Subjects performed a seated skilled reaching task in which they reached toward the top of a pedestal for a small food item that was grasped and transported to (...truncated)