title: Impaired smooth-pursuit in Parkinson's disease: normal cue-information memory, but dysfunction of extra-retinal mechanisms for pursuit preparation and execution.
abstract: While retinal image motion is the primary input for smooth-pursuit, its efficiency depends on cognitive processes including prediction. Reports are conflicting on impaired prediction during pursuit in Parkinson's disease. By separating two major components of prediction (image motion direction memory and movement preparation) using a memory-based pursuit task, and by comparing tracking eye movements with those during a simple ramp-pursuit task that did not require visual memory, we examined smooth-pursuit in 25 patients with Parkinson's disease and compared the results with 14 age-matched controls. In the memory-based pursuit task, cue 1 indicated visual motion direction, whereas cue 2 instructed the subjects to prepare to pursue or not to pursue. Based on the cue-information memory, subjects were asked to pursue the correct spot from two oppositely moving spots or not to pursue. In 24/25 patients, the cue-information memory was normal, but movement preparation and execution were impaired. Specifically, unlike controls, most of the patients (18/24 = 75%) lacked initial pursuit during the memory task and started tracking the correct spot by saccades. Conversely, during simple ramp-pursuit, most patients (83%) exhibited initial pursuit. Popping-out of the correct spot motion during memory-based pursuit was ineffective for enhancing initial pursuit. The results were similar irrespective of levodopa/dopamine agonist medication. Our results indicate that the extra-retinal mechanisms of most patients are dysfunctional in initiating memory-based (not simple ramp) pursuit. A dysfunctional pursuit loop between frontal eye fields (FEF) and basal ganglia may contribute to the impairment of extra-retinal mechanisms, resulting in deficient pursuit commands from the FEF to brainstem.
authors.affiliation: Department of Neurology, Sapporo Yamanoue Hospital, Sapporo, Japan kf001@pop.sys.hokudai.ac.jp.
authors.forename: Kikuro
authors.initials: K
authors.lastname: Fukushima
authors.affiliation: Department of Neurology, Sapporo Yamanoue Hospital, Sapporo, Japan.
authors.forename: Norie
authors.initials: N
authors.lastname: Ito
authors.affiliation: Faculty of Life Sciences, University of Manchester, Manchester, UK.
authors.forename: Graham R
authors.initials: GR
authors.lastname: Barnes
authors.affiliation: Department of Neurology, Sapporo Yamanoue Hospital, Sapporo, Japan.
authors.forename: Sachiyo
authors.initials: S
authors.lastname: Onishi
authors.affiliation: Department of Neurology, Sapporo Yamanoue Hospital, Sapporo, Japan.
authors.forename: Nobuyoshi
authors.initials: N
authors.lastname: Kobayashi
authors.affiliation: Department of Radiology, Sapporo Yamanoue Hospital, Sapporo, Japan.
authors.forename: Hidetoshi
authors.initials: H
authors.lastname: Takei
authors.affiliation: Department of Neurology, Sapporo Yamanoue Hospital, Sapporo, Japan.
authors.forename: Peter M
authors.initials: PM
authors.lastname: Olley
authors.affiliation: Department of Neurology, Sapporo Yamanoue Hospital, Sapporo, Japan.
authors.forename: Susumu
authors.initials: S
authors.lastname: Chiba
authors.affiliation: Department of Neurology, Sapporo Yamanoue Hospital, Sapporo, Japan.
authors.forename: Kiyoharu
authors.initials: K
authors.lastname: Inoue
authors.affiliation: Department of Neurology, Sapporo Yamanoue Hospital, Sapporo, Japan.
authors.forename: Tateo
authors.initials: T
authors.lastname: Warabi
keywords: Extra‐retinal mechanisms; Parkinson's disease; memory; priming effects; smooth‐pursuit
references.citation: Neurology. 1982 May;32(5):514-39
references.pmid: 7200209
references.citation: J Neurosci. 1992 Nov;12(11):4468-88
references.pmid: 1279139
references.citation: J Neurol Neurosurg Psychiatry. 1992 Mar;55(3):181-4
references.pmid: 1564476
references.citation: Neurology. 1967 May;17(5):427-42
references.pmid: 6067254
references.citation: Neurosci Lett. 2011 Jun 1;496(2):84-9
references.pmid: 21507339
references.citation: Brain. 1989 Dec;112 ( Pt 6):1573-86
references.pmid: 2597998
references.citation: J Neurosci. 2005 Jun 22;25(25):5866-76
references.pmid: 15976075
references.citation: Ann Neurol. 1978 Jul;4(1):63-6
references.pmid: 697327
references.citation: J Neurophysiol. 1998 Apr;79(4):1918-30
references.pmid: 9535958
references.citation: Brain. 1989 Oct;112 ( Pt 5):1193-214
references.pmid: 2804611
references.citation: J Neurophysiol. 2014 Jun 15;111(12):2644-55
references.pmid: 24671543
references.citation: Science. 2003 May 2;300(5620):812-5
references.pmid: 12730605
references.citation: J Neurophysiol. 1987 May;57(5):1446-63
references.pmid: 3585475
references.citation: Ann N Y Acad Sci. 2011 Sep;1233:168-76
references.pmid: 21950990
references.citation: J Neurophysiol. 2008 Feb;99(2):831-42
references.pmid: 18057108
references.citation: J Neurosci. 2006 Nov 29;26(48):12479-86
references.pmid: 17135410
references.citation: J Neurophysiol. 1998 Jul;80(1):28-47
references.pmid: 9658026
references.citation: Neurology. 2000 Dec 12;55(11):1621-6
references.pmid: 11113214
references.citation: J Neurophysiol. 2003 May;89(5):2678-84
references.pmid: 12612013
references.citation: Prog Brain Res. 2008;171:433-40
references.pmid: 18718338
references.citation: Neuropsychologia. 2010 Jun;48(7):1948-57
references.pmid: 20303998
references.citation: Brain. 1985 Dec;108 ( Pt 4):925-40
references.pmid: 4075079
references.citation: Cereb Cortex. 2011 Aug;21(8):1910-24
references.pmid: 21209120
references.citation: Front Syst Neurosci. 2013 Mar 19;7:4
references.pmid: 23515488
references.citation: J Neurol Neurosurg Psychiatry. 1999 Jun;66(6):746-53
references.pmid: 10329748
references.citation: Exp Brain Res. 2013 Aug;229(1):23-35
references.pmid: 23736523
references.citation: Brain. 1983 Sep;106 (Pt 3):571-87
references.pmid: 6640270
references.citation: Ann Neurol. 1996 Jun;39(6):749-60
references.pmid: 8651647
references.citation: J Neurosci. 1997 Oct 1;17(19):7490-502
references.pmid: 9295395
references.citation: Mov Disord. 2012 Jul;27(8):1012-8
references.pmid: 22693071
references.citation: J Clin Exp Neuropsychol. 1990 Mar;12(2):323-39
references.pmid: 2341560
references.citation: J Neurophysiol. 2000 Jan;83(1):563-87
references.pmid: 10634896
references.citation: Ann Neurol. 1996 Mar;39(3):368-77
references.pmid: 8602756
references.citation: J Psychiatr Res. 1975 Nov;12(3):189-98
references.pmid: 1202204
references.citation: J Neurosci. 2002 Jun 1;22(11):4675-85
references.pmid: 12040074
references.citation: Neuroreport. 2009 Jan 28;20(2):103-4
references.pmid: 19151594
references.citation: Nat Neurosci. 2003 Jan;6(1):66-74
references.pmid: 12483216
references.citation: Brain. 1988 Jun;111 ( Pt 3):497-505
references.pmid: 3382909
references.citation: Exp Brain Res. 2002 Jul;145(1):104-20
references.pmid: 12070750
references.citation: Neurology. 1987 Aug;37(8):1389-92
references.pmid: 3614666
references.citation: Brain Cogn. 2008 Dec;68(3):309-26
references.pmid: 18848744
references.citation: J Neurophysiol. 2008 Aug;100(2):1135-46
references.pmid: 18596183
references.citation: Front Neurol. 2011 Dec 14;2:78
references.pmid: 22174706
references.citation: J Neurol Neurosurg Psychiatry. 1987 Jul;50(7):853-60
references.pmid: 3625208
references.citation: Neurosci Res. 1994 May;19(3):251-68
references.pmid: 8058203
references.citation: J Neurol. 2008 Dec;255(12):1916-25
references.pmid: 19224319
references.citation: Prog Brain Res. 2006;151:461-501
references.pmid: 16221598
references.citation: Ann Neurol. 1994 Apr;35(4):420-6
references.pmid: 8154868
references.citation: Exp Brain Res. 2014 Jul;232(7):2369-79
references.pmid: 24736861
references.citation: Arch Neurol. 1979 Jun;36(6):360-4
references.pmid: 454234
references.citation: J Neurol. 2009 Sep;256(9):1438-46
references.pmid: 19363627
references.citation: J Gerontol. 1994 Sep;49(5):M235-8
references.pmid: 8056943
references.citation: Nat Rev Neurosci. 2010 Nov;11(11):760-72
references.pmid: 20944662
references.citation: J Neurophysiol. 2011 Jul;106(1):347-60
references.pmid: 21525365
references.citation: Neuroreport. 2009 Jan 28;20(2):121-5
references.pmid: 19151596
references.citation: Exp Brain Res. 1985;57(3):562-75
references.pmid: 3979498
references.citation: Brain. 1984 Jun;107 ( Pt 2):371-84
references.pmid: 6722509
references.citation: Neuropsychology. 2008 Sep;22(5):585-95
references.pmid: 18763878
references.citation: J Neurophysiol. 1994 Dec;72(6):2714-28
references.pmid: 7897484
references.citation: Exp Brain Res. 2011 Oct;214(2):293-301
references.pmid: 21837438
references.citation: J Neurol. 2008 Jul;255(7):1071-8
references.pmid: 18438696
references.citation: BMC Neurol. 2012 Feb 29;12:5
references.pmid: 22375860
references.citation: Brain. 2010 Sep;133(9):2677-89
references.pmid: 20688815
references.citation: Parkinsonism Relat Disord. 2003 Jan;9(3):139-44
references.pmid: 12573868
references.citation: Neuron. 2009 Jun 11;62(5):717-32
references.pmid: 19524530
references.citation: Exp Brain Res. 2014 Jan;232(1):191-210
references.pmid: 24129645
references.citation: Ann N Y Acad Sci. 2011 Sep;1233:117-26
references.pmid: 21950984