Parkinsonian patients show impaired predictive smooth pursuit

To determine if patients with Parkinson’s disease (PD) are able to use a visual contextual cue to induce a predictive change in smooth pursuit direction and if this ability depends on the state of the dopaminergic system, we measured predictive smooth pursuit in nine patients with mild to moderate PD during OFF and ON medication. These values were compared with those of nine agematched and sex-matched healthy controls.Our focus was on the horizontal smooth pursuit when subjects pursued a downward moving target entering a ± 90 deg curve. The target moved on a homogeneous background or on a static “street” that indicated the future trajectory of the target. Our main result is that PD patients were impaired in eliciting predictive smooth pursuit using the context information of the street compared to healthy subjects. The control group elicited predictive pursuit 250 ms before target onset. In contrast, PD patients showed significantly longer latency (100–120 ms) and reduced maximal pursuit velocity. However, without the street guiding pursuit, a delay of about 250 ms was seen in both groups. There was no significant difference in the smooth pursuit performance between OFF and ON medication in the patient group.These results show that earlystage PD patients are impaired in the use of static visual information as a cue for predictive pursuit compared to controls and that this deficit does not depend on dopaminergic medication. In the context of predictive eye movement, the involvement of the striatal-frontal pathway and the spatial working memory is discussed.

[1]  C. Kennard,et al.  Quantitative study of "on-off" fluctuations in the ocular motor system in Parkinson's disease. , 1987, Advances in neurology.

[2]  M. Simonetta,et al.  Abnormal ocular movements in Parkinson's disease. Evidence for involvement of dopaminergic systems. , 1989, Brain : a journal of neurology.

[3]  A. Owen Cognitive Dysfunction in Parkinson’s Disease: The Role of Frontostriatal Circuitry , 2004, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[4]  G R Barnes,et al.  Progressive bradykinesia and hypokinesia of ocular pursuit in Parkinson’s disease , 1999, Journal of neurology, neurosurgery, and psychiatry.

[5]  C H Lücking,et al.  Abnormalities of tracking behavior in Parkinson's disease , 1995, Movement disorders : official journal of the Movement Disorder Society.

[6]  Eileen Kowler Cognitive expectations, not habits, control anticipatory smooth oculomotor pursuit , 1989, Vision Research.

[7]  O. Lindvall,et al.  Use and interpretation of on/off diaries in Parkinson’s disease , 2004, Journal of Neurology, Neurosurgery & Psychiatry.

[8]  S. Heinen Single neuron activity in the dorsomedial frontal cortex during smooth pursuit eye movements , 2004, Experimental Brain Research.

[9]  Erich Schneider,et al.  Low-latency video tracking of horizontal, vertical, and torsional eye movements as a basis for 3dof realtime motion control of a head-mounted camera , 2006, 2006 IEEE International Conference on Systems, Man and Cybernetics.

[10]  Howard Poizner,et al.  Control of voluntary and reflexive saccades in Parkinson’s disease , 1999, Experimental Brain Research.

[11]  E. G. Keating,et al.  Frontal eye field lesions impair predictive and visually-guided pursuit eye movements , 2004, Experimental Brain Research.

[12]  T. Robbins,et al.  Cognitive Impairments in Early Parkinson's Disease Are Accompanied by Reductions in Activity in Frontostriatal Neural Circuitry , 2003, The Journal of Neuroscience.

[13]  Stefan Glasauer,et al.  Velocity scaling of cue-induced smooth pursuit acceleration obeys constraints of natural motion , 2007, Experimental Brain Research.

[14]  B. Gaymard,et al.  Eye movement disorders after frontal eye field lesions in humans , 2004, Experimental Brain Research.

[15]  J. Jankovic,et al.  Variable expression of Parkinson's disease , 1990, Neurology.

[16]  Jennifer J. Pokorny,et al.  Activity of substantia nigra pars reticulata neurons during smooth pursuit eye movements in monkeys , 2005, The European journal of neuroscience.

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

[18]  U. Ilg Visual-tracking neurons in area MST are activated during anticipatory pursuit eye movements , 2003, Neuroreport.

[19]  Peter Thier,et al.  The influence of structured visual backgrounds on smooth-pursuit initiation, steady-state pursuit and smooth-pursuit termination , 1995, Biological Cybernetics.

[20]  Klaus Bartl,et al.  Eye movement driven head-mounted camera: it looks where the eyes look , 2005, 2005 IEEE International Conference on Systems, Man and Cybernetics.

[21]  K. Fukushima,et al.  Predictive responses of periarcuate pursuit neurons to visual target motion , 2002, Experimental Brain Research.

[22]  S. Fahn Members of the UPDRS Development Committee. Unified Parkinson's Disease Rating Scale , 1987 .

[23]  G. R. Barnes,et al.  The remembered pursuit task: evidence for segregation of timing and velocity storage in predictive oculomotor control , 1999, Experimental Brain Research.

[24]  R. Tomlinson,et al.  Ocular motor deficits in Parkinson's disease. III. Coordination of eye and head movements. , 1988, Brain : a journal of neurology.

[25]  J. Hughes,et al.  Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. , 1992, Journal of neurology, neurosurgery, and psychiatry.

[26]  C. Marsden,et al.  Fronto-striatal cognitive deficits at different stages of Parkinson's disease. , 1992, Brain : a journal of neurology.

[27]  R. Tomlinson,et al.  Ocular motor deficits in Parkinson's disease. II. Control of the saccadic and smooth pursuit systems. , 1983, Brain : a journal of neurology.

[28]  M. Grealy,et al.  Abnormalities of smooth eye and head movement control in parhson's disease , 1996, Annals of neurology.

[29]  C. Frith,et al.  Initiation and execution of predictable and unpredictable movements in Parkinson's disease. , 1984, Brain : a journal of neurology.

[30]  H. Collewijn,et al.  Human smooth and saccadic eye movements during voluntary pursuit of different target motions on different backgrounds. , 1984, The Journal of physiology.

[31]  M. Missal,et al.  Supplementary eye fields stimulation facilitates anticipatory pursuit. , 2004, Journal of neurophysiology.

[32]  G. Barnes,et al.  The mechanism of prediction in human smooth pursuit eye movements. , 1991, The Journal of physiology.

[33]  S. Pollmann,et al.  D1- Versus D2-Receptor Modulation of Visuospatial Working Memory in Humans , 1998, The Journal of Neuroscience.

[34]  P. Goldman-Rakic The cortical dopamine system: role in memory and cognition. , 1998, Advances in pharmacology.

[35]  J. Sharpe,et al.  Smooth pursuit during dose‐related on‐off fluctuations in Parkinson's disease , 1987, Neurology.

[36]  L. Henderson,et al.  Abnormalities of nonvisually-guided eye movements in Parkinson's disease. , 1989, Brain : a journal of neurology.

[37]  PhD K. A. Flowers,et al.  Predictive control of eye movements in parkinson disease , 1978, Annals of neurology.

[38]  S. Fahn Unified Parkinson's Disease Rating Scale , 1987 .