Attention and reach-to-grasp movements in Parkinson’s disease

The role of attention in grasping movements directed at common objects has not been examined in Parkinson’s disease (PD), though these movements are critical to activities of daily living. Our primary objective was to determine whether patients with PD demonstrate automaticity in grasping movements directed toward common objects. Automaticity is assumed when tasks can be performed with little or no interference from concurrent tasks. Grasping performance in three patient groups (newly diagnosed, moderate, and advanced/surgically treated PD) on and off of their medication or deep brain stimulation was compared to performance in an age-matched control group. Automaticity was demonstrated by the absence of a decrement in grasping performance when attention was consumed by a concurrent spatial-visualization task. Only the control group and newly diagnosed PD group demonstrated automaticity in their grasping movements. The moderate and advanced PD groups did not demonstrate automaticity. Furthermore, the well-known effects of pharmacotherapy and surgical intervention on movement speed and muscle activation patterns did not appear to reduce the impact of attention-demanding tasks on grasping movements in those with moderate to advanced PD. By the moderate stage of PD, grasping is an attention-demanding process; this change is not ameliorated by dopaminergic or surgical treatments. These findings have important implications for activities of daily living, as devoting attention to the simplest of daily tasks would interfere with complex activities and potentially exacerbate fatigue.

[1]  John C Marshall,et al.  Micrographia in Parkinson’s disease: the effect of providing external cues , 1997, Journal of neurology, neurosurgery, and psychiatry.

[2]  D. Rosenbaum,et al.  Planning for manual positioning: the end-state comfort effect for manual abduction–adduction , 2007, Experimental Brain Research.

[3]  Luca Turella,et al.  An object for an action, the same object for other actions: effects on hand shaping , 2008, Experimental Brain Research.

[4]  R. Iansek,et al.  Movement‐related potentials in Parkinson's disease: External cues and attentional strategies , 1999, Movement disorders : official journal of the Movement Disorder Society.

[5]  Janneke Koerts,et al.  Cognitive dysfunction in non-demented Parkinson's disease patients: Controlled and automatic behavior , 2009, Cortex.

[6]  J. Roulin,et al.  Working memory functioning in medicated Parkinson's disease patients and the effect of withdrawal of dopaminergic medication. , 2000, Neuropsychology.

[7]  T. Robbins,et al.  Dopaminergic basis for deficits in working memory but not attentional set-shifting in Parkinson's disease , 2005, Neuropsychologia.

[8]  B. Bloem,et al.  The “posture second” strategy: A review of wrong priorities in Parkinson's disease , 2006, Journal of the Neurological Sciences.

[9]  M. Gentilucci,et al.  Effects of disease progression and L-dopa therapy on the control of reaching-grasping in Parkinson's disease , 2005, Neuropsychologia.

[10]  Michael J. Frank,et al.  A dopaminergic basis for working memory, learning and attentional shifting in Parkinsonism , 2008, Neuropsychologia.

[11]  J. R. Bloedel,et al.  Control of aperture closure during reach-to-grasp movements in parkinson’s disease , 2005, Experimental Brain Research.

[12]  Sabrina M. Tom,et al.  The Neural Correlates of Motor Skill Automaticity , 2005, The Journal of Neuroscience.

[13]  Charles Adler,et al.  Disruptions in the reach-to-grasp actions of Parkinson's patients , 2001, Experimental Brain Research.

[14]  L. Brooks Spatial and verbal components of the act of recall. , 1968 .

[15]  A. Nieuwboer,et al.  The immediate effect of attentional, auditory, and a combined cue strategy on gait during single and dual tasks in Parkinson's disease. , 2007, Archives of physical medicine and rehabilitation.

[16]  M. Brin,et al.  Effects of levodopa on cognitive functioning in moderate-to-severe Parkinson’s disease (MSPD) , 2004, Journal of Neural Transmission.

[17]  R. Bakay,et al.  Cognitive impairments in advanced PD without dementia , 2002, Neurology.

[18]  M. Hallett,et al.  Neural correlates of dual task performance in patients with Parkinson’s disease , 2007, Journal of Neurology, Neurosurgery, and Psychiatry.

[19]  J. Phillips,et al.  Automatic behaviour: Efficient not mindless , 2007, Brain Research Bulletin.

[20]  T. Goldberg,et al.  Dopaminergic modulation of cortical function in patients with Parkinson's disease , 2002, Annals of neurology.

[21]  John D. E. Gabrieli,et al.  Reduced working memory span in Parkinson's disease: Evidence for the role of frontostriatal system in working and strategic memory. , 1996 .

[22]  M. Hallett,et al.  Pathophysiology of bradykinesia in Parkinson's disease. , 2001, Brain : a journal of neurology.

[23]  Maurizio Gentilucci Object familiarity affects finger shaping during grasping of fruit stalks , 2003, Experimental Brain Research.

[24]  Heather Gage,et al.  Rehabilitation for Parkinson's disease: a systematic review of available evidence , 2004, Clinical rehabilitation.

[25]  Alice Nieuwboer,et al.  Cueing for freezing of gait in patients with Parkinson's disease: A rehabilitation perspective , 2008, Movement disorders : official journal of the Movement Disorder Society.

[26]  D. V. Cramon,et al.  Manipulation of working memory information is impaired in Parkinson's disease and related to working memory capacity. , 2002, Neuropsychology.

[27]  U. Castiello,et al.  The reach-to-grasp movement in Parkinson’s disease before and after dopaminergic medication , 2000, Neuropsychologia.

[28]  C. Marsden,et al.  Dual task performance and processing resources in normal subjects and patients with Parkinson's disease. , 1991, Brain : a journal of neurology.

[29]  J. Soucy,et al.  Cognitive Deficits and Striatal Dopaminergic Denervation in Parkinson's Disease: A Single Photon Emission Computed Tomography Study Using 123Iodine-&bgr;-CIT in Patients ON and OFF Levodopa , 2002, Clinical neuropharmacology.

[30]  M. Hallett,et al.  A functional MRI study of automatic movements in patients with Parkinson's disease. , 2005, Brain : a journal of neurology.

[31]  Luis F. Schettino,et al.  Deficits in the evolution of hand preshaping in Parkinson’s disease , 2004, Neuropsychologia.

[32]  J. P. Martin The basal ganglia and posture. , 1967 .

[33]  M. Gentilucci,et al.  The control of an action in Parkinson’s disease , 1999, Experimental Brain Research.

[34]  Murray Grossman,et al.  Cognition following bilateral deep brain stimulation surgery of the subthalamic nucleus for Parkinson's disease , 2009, International journal of geriatric psychiatry.

[35]  M. Santello,et al.  Effects of end-goal on hand shaping. , 2006, Journal of neurophysiology.

[36]  Jean-Philippe Azulay,et al.  Influence of visual cues on gait in Parkinson's disease: Contribution to attention or sensory dependence? , 2006, Journal of the Neurological Sciences.

[37]  M. Weatherall,et al.  A meta-analysis of performance on simple span and more complex working memory tasks in Parkinson's disease. , 2008, Neuropsychology.

[38]  Robert Iansek,et al.  Characteristics of motor disturbance in Parkinson's disease and strategies for movement rehabilitation , 1996 .

[39]  G. Fink,et al.  The impact of subthalamic deep brain stimulation on bradykinesia of proximal and distal upper limb muscles in Parkinson's disease , 2008, Journal of Neurology.

[40]  R. Bastiaanse,et al.  The impact of executive functions on verb production in patients with Parkinson's disease , 2009, Cortex.

[41]  Sarah H. Creem,et al.  Grasping objects by their handles: a necessary interaction between cognition and action. , 2001, Journal of experimental psychology. Human perception and performance.

[42]  R. Shiffrin,et al.  Controlled and automatic human information processing: I , 1977 .

[43]  J. Hermsdörfer,et al.  Grasping tools: Effects of task and apraxia , 2009, Neuropsychologia.

[44]  Janey Prodoehl,et al.  Effects of deep brain stimulation and medication on bradykinesia and muscle activation in Parkinson's disease. , 2003, Brain : a journal of neurology.