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Erschienen in: Journal of Neurology 9/2009

01.09.2009 | Original Communication

Comparison of smooth pursuit eye movement deficits in multiple system atrophy and Parkinson’s disease

verfasst von: Elmar H. Pinkhardt, Jan Kassubek, Sigurd Süssmuth, Albert C. Ludolph, Wolfgang Becker, Reinhart Jürgens

Erschienen in: Journal of Neurology | Ausgabe 9/2009

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Abstract

Because of the large overlap and quantitative similarity of eye movement alterations in Parkinson’s disease (PD) and multiple system atrophy (MSA), a measurement of eye movement is generally not considered helpful for the differential diagnosis. However, in view of the pathophysiological differences between MSA and PD as well as between the cerebellar (MSA-C) and Parkinsonian (MSA-P) subtypes of MSA, we wondered whether a detailed investigation of oculomotor performance would unravel parameters that could help to differentiate between these entities. We recorded eye movements during sinusoidal pursuit tracking by means of video-oculography in 11 cases of MSA-P, 8 cases of MSA-C and 27 cases of PD and compared them to 23 healthy controls (CTL). The gain of the smooth pursuit eye movement (SPEM) component exhibited significant group differences between each of the three subject groups (MSA, PD, controls) but not between MSA-P and MSA-C. The similarity of pursuit impairment in MSA-P and in MSA-C suggests a commencement of cerebellar pathology in MSA-P despite the lack of clinical signs. Otherwise, SPEM gain was of little use for differential diagnosis between MSA and PD because of wide overlap. However, inspection of the saccadic component of pursuit tracking revealed that in MSA saccades typically correct for position errors accumulated during SPEM epochs (“catch-up saccades”), whereas in PD, saccades were often directed toward future target positions (“anticipatory saccades”). The differences in pursuit tracking between PD and MSA were large enough to warrant their use as ancillary diagnostic criteria for the distinction between these disorders.
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Literatur
1.
Zurück zum Zitat Anderson T, Luxon L, Quinn N, Daniel S, Marsden CD, Bronstein A (2008) Oculomotor function in multiple system atrophy: clinical and laboratory features in 30 patients. Mov Disord 23:977–984PubMedCrossRef Anderson T, Luxon L, Quinn N, Daniel S, Marsden CD, Bronstein A (2008) Oculomotor function in multiple system atrophy: clinical and laboratory features in 30 patients. Mov Disord 23:977–984PubMedCrossRef
2.
Zurück zum Zitat Bensimon G, Ludolph A, Agid Y, Vidailhet M, Payan C, Leigh PN (2009) Riluzole treatment, survival and diagnostic criteria in Parkinson plus disorders: the NNIPPS study. Brain 132:156–171PubMedCrossRef Bensimon G, Ludolph A, Agid Y, Vidailhet M, Payan C, Leigh PN (2009) Riluzole treatment, survival and diagnostic criteria in Parkinson plus disorders: the NNIPPS study. Brain 132:156–171PubMedCrossRef
3.
Zurück zum Zitat Brand M, Labudda K, Kalbe E, Hilker R, Emmans D, Fuchs G, Kessler J, Markowitsch HJ (2004) Decision-making impairments in patients with Parkinson’s disease. Behav Neurol 15:77–85PubMed Brand M, Labudda K, Kalbe E, Hilker R, Emmans D, Fuchs G, Kessler J, Markowitsch HJ (2004) Decision-making impairments in patients with Parkinson’s disease. Behav Neurol 15:77–85PubMed
4.
Zurück zum Zitat Briand KA, Strallow D, Hening W, Poizner H, Sereno AB (1999) Control of voluntary and reflexive saccades in Parkinson’s disease. Exp Brain Res 129:38–48PubMedCrossRef Briand KA, Strallow D, Hening W, Poizner H, Sereno AB (1999) Control of voluntary and reflexive saccades in Parkinson’s disease. Exp Brain Res 129:38–48PubMedCrossRef
5.
Zurück zum Zitat Cegalis JA, Sweeney JA (1981) The effect of attention on smooth pursuit eye movements of schizophrenics. J Psychiatr Res 16:145–161PubMedCrossRef Cegalis JA, Sweeney JA (1981) The effect of attention on smooth pursuit eye movements of schizophrenics. J Psychiatr Res 16:145–161PubMedCrossRef
6.
Zurück zum Zitat Chan F, Armstrong IT, Pari G, Riopelle RJ, Munoz DP (2005) Deficits in saccadic eye-movement control in Parkinson’s disease. Neuropsychologia 43:784–796PubMedCrossRef Chan F, Armstrong IT, Pari G, Riopelle RJ, Munoz DP (2005) Deficits in saccadic eye-movement control in Parkinson’s disease. Neuropsychologia 43:784–796PubMedCrossRef
7.
Zurück zum Zitat Crevits L, Vandierendonck A, Stuyven E, Verschaete S, Wildenbeest J (2004) Effect of intention and visual fixation disengagement on prosaccades in Parkinson’s disease patients. Neuropsychologia 42:624–632PubMedCrossRef Crevits L, Vandierendonck A, Stuyven E, Verschaete S, Wildenbeest J (2004) Effect of intention and visual fixation disengagement on prosaccades in Parkinson’s disease patients. Neuropsychologia 42:624–632PubMedCrossRef
8.
Zurück zum Zitat Drago V, Foster PS, Skidmore FM, Kluger B, Antoniello D, Heilman KM (2008) Attentional grasp in Parkinson disease. Cogn Behav Neurol 21:138–142PubMedCrossRef Drago V, Foster PS, Skidmore FM, Kluger B, Antoniello D, Heilman KM (2008) Attentional grasp in Parkinson disease. Cogn Behav Neurol 21:138–142PubMedCrossRef
9.
Zurück zum Zitat Gibb WR, Lees AJ (1988) The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson’s disease. J Neurol Neurosurg Psychiatr 51:745–752PubMedCrossRef Gibb WR, Lees AJ (1988) The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson’s disease. J Neurol Neurosurg Psychiatr 51:745–752PubMedCrossRef
10.
Zurück zum Zitat Gilman S, Wenning GK, Low PA, Brooks DJ, Mathias CJ, Trojanowski JQ, Wood NW, Colosimo C, Durr A, Fowler CJ, Kaufmann H, Klockgether T, Lees A, Poewe W, Quinn N, Revesz T, Robertson D, Sandroni P, Seppi K, Vidailhet M (2008) Second consensus statement on the diagnosis of multiple system atrophy. Neurology 71:670–676PubMedCrossRef Gilman S, Wenning GK, Low PA, Brooks DJ, Mathias CJ, Trojanowski JQ, Wood NW, Colosimo C, Durr A, Fowler CJ, Kaufmann H, Klockgether T, Lees A, Poewe W, Quinn N, Revesz T, Robertson D, Sandroni P, Seppi K, Vidailhet M (2008) Second consensus statement on the diagnosis of multiple system atrophy. Neurology 71:670–676PubMedCrossRef
11.
Zurück zum Zitat Hikosaka O, Takikawa Y, Kawagoe R (2000) Role of the basal ganglia in the control of purposive saccadic eye movements. Physiol Rev 80:953–978PubMed Hikosaka O, Takikawa Y, Kawagoe R (2000) Role of the basal ganglia in the control of purposive saccadic eye movements. Physiol Rev 80:953–978PubMed
12.
Zurück zum Zitat Hsu JL, Jung TP, Hsu CY, Hsu WC, Chen YK, Duann JR, Wang HC, Makeig S (2007) Regional CBF changes in Parkinson’s disease: a correlation with motor dysfunction. Eur J Nucl Med Mol Imaging 34:1458–1466PubMedCrossRef Hsu JL, Jung TP, Hsu CY, Hsu WC, Chen YK, Duann JR, Wang HC, Makeig S (2007) Regional CBF changes in Parkinson’s disease: a correlation with motor dysfunction. Eur J Nucl Med Mol Imaging 34:1458–1466PubMedCrossRef
13.
Zurück zum Zitat Hutton SB, Tegally D (2005) The effects of dividing attention on smooth pursuit eye tracking. Exp Brain Res 163:306–313PubMedCrossRef Hutton SB, Tegally D (2005) The effects of dividing attention on smooth pursuit eye tracking. Exp Brain Res 163:306–313PubMedCrossRef
14.
Zurück zum Zitat Iacono WG, Lykken DT (1979) Comments on “smooth-pursuit eye movements: a comparison of two measurement techniques” by Lindsey, Holzman, Haberman, and Yasillo. J Abnorm Psychol 88:678–680PubMedCrossRef Iacono WG, Lykken DT (1979) Comments on “smooth-pursuit eye movements: a comparison of two measurement techniques” by Lindsey, Holzman, Haberman, and Yasillo. J Abnorm Psychol 88:678–680PubMedCrossRef
15.
Zurück zum Zitat Kitagawa M, Fukushima J, Tashiro K (1994) Relationship between antisaccades and the clinical symptoms in Parkinson’s disease. Neurology 44:2285–2289PubMed Kitagawa M, Fukushima J, Tashiro K (1994) Relationship between antisaccades and the clinical symptoms in Parkinson’s disease. Neurology 44:2285–2289PubMed
16.
Zurück zum Zitat Kollensperger M, Geser F, Seppi K, Stampfer-Kountchev M, Sawires M, Scherfler C, Boesch S, Mueller J, Koukouni V, Quinn N, Pellecchia MT, Barone P, Schimke N, Dodel R, Oertel W, Dupont E, Ostergaard K, Daniels C, Deuschl G, Gurevich T, Giladi N, Coelho M, Sampaio C, Nilsson C, Widner H, Sorbo FD, Albanese A, Cardozo A, Tolosa E, Abele M, Klockgether T, Kamm C, Gasser T, Djaldetti R, Colosimo C, Meco G, Schrag A, Poewe W, Wenning GK (2008) Red flags for multiple system atrophy. Mov Disord 23:1093–1099PubMedCrossRef Kollensperger M, Geser F, Seppi K, Stampfer-Kountchev M, Sawires M, Scherfler C, Boesch S, Mueller J, Koukouni V, Quinn N, Pellecchia MT, Barone P, Schimke N, Dodel R, Oertel W, Dupont E, Ostergaard K, Daniels C, Deuschl G, Gurevich T, Giladi N, Coelho M, Sampaio C, Nilsson C, Widner H, Sorbo FD, Albanese A, Cardozo A, Tolosa E, Abele M, Klockgether T, Kamm C, Gasser T, Djaldetti R, Colosimo C, Meco G, Schrag A, Poewe W, Wenning GK (2008) Red flags for multiple system atrophy. Mov Disord 23:1093–1099PubMedCrossRef
17.
Zurück zum Zitat Konishi S, Nakajima K, Uchida I, Kikyo H, Kameyama M, Miyashita Y (1999) Common inhibitory mechanism in human inferior prefrontal cortex revealed by event-related functional MRI. Brain 122(Pt 5):981–991PubMedCrossRef Konishi S, Nakajima K, Uchida I, Kikyo H, Kameyama M, Miyashita Y (1999) Common inhibitory mechanism in human inferior prefrontal cortex revealed by event-related functional MRI. Brain 122(Pt 5):981–991PubMedCrossRef
18.
Zurück zum Zitat Leigh RJ, Zee DS (2006) The neurology of eye movements. Oxford University Press, Oxford Leigh RJ, Zee DS (2006) The neurology of eye movements. Oxford University Press, Oxford
19.
Zurück zum Zitat Lueck CJ, Tanyeri S, Crawford TJ, Henderson L, Kennard C (1990) Antisaccades and remembered saccades in Parkinson’s disease. J Neurol Neurosurg Psychiatr 53:284–288PubMedCrossRef Lueck CJ, Tanyeri S, Crawford TJ, Henderson L, Kennard C (1990) Antisaccades and remembered saccades in Parkinson’s disease. J Neurol Neurosurg Psychiatr 53:284–288PubMedCrossRef
20.
Zurück zum Zitat Mari-Beffa P, Hayes AE, Machado L, Hindle JV (2005) Lack of inhibition in Parkinson’s disease: evidence from a lexical decision task. Neuropsychologia 43:638–646PubMedCrossRef Mari-Beffa P, Hayes AE, Machado L, Hindle JV (2005) Lack of inhibition in Parkinson’s disease: evidence from a lexical decision task. Neuropsychologia 43:638–646PubMedCrossRef
21.
Zurück zum Zitat Marino S, Sessa E, Di Lorenzo G, Lanzafame P, Scullica G, Bramanti A, La Rosa F, Iannizzotto G, Bramanti P, Di Bella P (2007) Quantitative analysis of pursuit ocular movements in Parkinson’s disease by using a video-based eye tracking system. Eur Neurol 58:193–197PubMedCrossRef Marino S, Sessa E, Di Lorenzo G, Lanzafame P, Scullica G, Bramanti A, La Rosa F, Iannizzotto G, Bramanti P, Di Bella P (2007) Quantitative analysis of pursuit ocular movements in Parkinson’s disease by using a video-based eye tracking system. Eur Neurol 58:193–197PubMedCrossRef
22.
Zurück zum Zitat Mosimann UP, Muri RM, Burn DJ, Felblinger J, O’Brien JT, McKeith IG (2005) Saccadic eye movement changes in Parkinson’s disease dementia and dementia with Lewy bodies. Brain 128:1267–1276PubMedCrossRef Mosimann UP, Muri RM, Burn DJ, Felblinger J, O’Brien JT, McKeith IG (2005) Saccadic eye movement changes in Parkinson’s disease dementia and dementia with Lewy bodies. Brain 128:1267–1276PubMedCrossRef
23.
Zurück zum Zitat Nagano-Saito A, Washimi Y, Arahata Y, Kachi T, Lerch JP, Evans AC, Dagher A, Ito K (2005) Cerebral atrophy and its relation to cognitive impairment in Parkinson disease. Neurology 64:224–229PubMed Nagano-Saito A, Washimi Y, Arahata Y, Kachi T, Lerch JP, Evans AC, Dagher A, Ito K (2005) Cerebral atrophy and its relation to cognitive impairment in Parkinson disease. Neurology 64:224–229PubMed
24.
Zurück zum Zitat Nakamura T, Kanayama R, Sano R, Ohki M, Kimura Y, Aoyagi M, Koike Y (1991) Quantitative analysis of ocular movements in Parkinson’s disease. Acta Otolaryngol Suppl 481:559–562PubMedCrossRef Nakamura T, Kanayama R, Sano R, Ohki M, Kimura Y, Aoyagi M, Koike Y (1991) Quantitative analysis of ocular movements in Parkinson’s disease. Acta Otolaryngol Suppl 481:559–562PubMedCrossRef
25.
Zurück zum Zitat Ozawa T, Paviour D, Quinn NP, Josephs KA, Sangha H, Kilford L, Healy DG, Wood NW, Lees AJ, Holton JL, Revesz T (2004) The spectrum of pathological involvement of the striatonigral and olivopontocerebellar systems in multiple system atrophy: clinicopathological correlations. Brain 127:2657–2671PubMedCrossRef Ozawa T, Paviour D, Quinn NP, Josephs KA, Sangha H, Kilford L, Healy DG, Wood NW, Lees AJ, Holton JL, Revesz T (2004) The spectrum of pathological involvement of the striatonigral and olivopontocerebellar systems in multiple system atrophy: clinicopathological correlations. Brain 127:2657–2671PubMedCrossRef
26.
Zurück zum Zitat Pierrot-Deseilligny C, Muri RM, Nyffeler T, Milea D (2005) The role of the human dorsolateral prefrontal cortex in ocular motor behavior. Ann N Y Acad Sci 1039:239–251PubMedCrossRef Pierrot-Deseilligny C, Muri RM, Nyffeler T, Milea D (2005) The role of the human dorsolateral prefrontal cortex in ocular motor behavior. Ann N Y Acad Sci 1039:239–251PubMedCrossRef
27.
Zurück zum Zitat Pierrot-Deseilligny C, Muri RM, Ploner CJ, Gaymard B, Demeret S, Rivaud-Pechoux S (2003) Decisional role of the dorsolateral prefrontal cortex in ocular motor behaviour. Brain 126:1460–1473PubMedCrossRef Pierrot-Deseilligny C, Muri RM, Ploner CJ, Gaymard B, Demeret S, Rivaud-Pechoux S (2003) Decisional role of the dorsolateral prefrontal cortex in ocular motor behaviour. Brain 126:1460–1473PubMedCrossRef
28.
Zurück zum Zitat Rascol O, Clanet M, Montastruc JL, Simonetta M, Soulier-Esteve MJ, Doyon B, Rascol A (1989) Abnormal ocular movements in Parkinson’s disease. Evidence for involvement of dopaminergic systems. Brain 112(Pt 5):1193–1214PubMedCrossRef Rascol O, Clanet M, Montastruc JL, Simonetta M, Soulier-Esteve MJ, Doyon B, Rascol A (1989) Abnormal ocular movements in Parkinson’s disease. Evidence for involvement of dopaminergic systems. Brain 112(Pt 5):1193–1214PubMedCrossRef
29.
Zurück zum Zitat Rivaud-Pechoux S, Vidailhet M, Brandel JP, Gaymard B (2007) Mixing pro- and antisaccades in patients with parkinsonian syndromes. Brain 130:256–264PubMedCrossRef Rivaud-Pechoux S, Vidailhet M, Brandel JP, Gaymard B (2007) Mixing pro- and antisaccades in patients with parkinsonian syndromes. Brain 130:256–264PubMedCrossRef
30.
Zurück zum Zitat Ross RG, Olincy A, Harris JG, Sullivan B, Radant A (2000) Smooth pursuit eye movements in schizophrenia and attentional dysfunction: adults with schizophrenia, ADHD, and a normal comparison group. Biol Psychiatry 48:197–203PubMedCrossRef Ross RG, Olincy A, Harris JG, Sullivan B, Radant A (2000) Smooth pursuit eye movements in schizophrenia and attentional dysfunction: adults with schizophrenia, ADHD, and a normal comparison group. Biol Psychiatry 48:197–203PubMedCrossRef
31.
Zurück zum Zitat Rottach KG, Riley DE, DiScenna AO, Zivotofsky AZ, Leigh RJ (1996) Dynamic properties of horizontal and vertical eye movements in parkinsonian syndromes. Ann Neurol 39:368–377PubMedCrossRef Rottach KG, Riley DE, DiScenna AO, Zivotofsky AZ, Leigh RJ (1996) Dynamic properties of horizontal and vertical eye movements in parkinsonian syndromes. Ann Neurol 39:368–377PubMedCrossRef
32.
Zurück zum Zitat Sasaki K, Gemba H, Nambu A, Matsuzaki R (1993) No-go activity in the frontal association cortex of human subjects. Neurosci Res 18:249–252PubMedCrossRef Sasaki K, Gemba H, Nambu A, Matsuzaki R (1993) No-go activity in the frontal association cortex of human subjects. Neurosci Res 18:249–252PubMedCrossRef
33.
Zurück zum Zitat Schlenker R, Cohen R, Berg P, Hubman W, Mohr F, Watzl H, Werther P (1994) Smooth-pursuit eye movement dysfunction in schizophrenia: the role of attention and general psychomotor dysfunctions. Eur Arch Psychiatry Clin Neurosci 244:153–160PubMedCrossRef Schlenker R, Cohen R, Berg P, Hubman W, Mohr F, Watzl H, Werther P (1994) Smooth-pursuit eye movement dysfunction in schizophrenia: the role of attention and general psychomotor dysfunctions. Eur Arch Psychiatry Clin Neurosci 244:153–160PubMedCrossRef
34.
Zurück zum Zitat Spengler D, Trillenberg P, Sprenger A, Nagel M, Kordon A, Junghanns K, Heide W, Arolt V, Hohagen F, Lencer R (2006) Evidence from increased anticipation of predictive saccades for a dysfunction of fronto-striatal circuits in obsessive–compulsive disorder. Psychiatry Res 143:77–88PubMedCrossRef Spengler D, Trillenberg P, Sprenger A, Nagel M, Kordon A, Junghanns K, Heide W, Arolt V, Hohagen F, Lencer R (2006) Evidence from increased anticipation of predictive saccades for a dysfunction of fronto-striatal circuits in obsessive–compulsive disorder. Psychiatry Res 143:77–88PubMedCrossRef
35.
Zurück zum Zitat Van Gelder P, Lebedev S, Liu PM, Tsui WH (1995) Anticipatory saccades in smooth pursuit: task effects and pursuit vector after saccades. Vision Res 35:667–678PubMedCrossRef Van Gelder P, Lebedev S, Liu PM, Tsui WH (1995) Anticipatory saccades in smooth pursuit: task effects and pursuit vector after saccades. Vision Res 35:667–678PubMedCrossRef
36.
Zurück zum Zitat Vidailhet M, Rivaud S, Gouider-Khouja N, Pillon B, Bonnet AM, Gaymard B, Agid Y, Pierrot-Deseilligny C (1994) Eye movements in parkinsonian syndromes. Ann Neurol 35:420–426PubMedCrossRef Vidailhet M, Rivaud S, Gouider-Khouja N, Pillon B, Bonnet AM, Gaymard B, Agid Y, Pierrot-Deseilligny C (1994) Eye movements in parkinsonian syndromes. Ann Neurol 35:420–426PubMedCrossRef
37.
Zurück zum Zitat Vingerhoets G, Vermeule E, Santens P (2005) Impaired intentional content learning but spared incidental retention of contextual information in non-demented patients with Parkinson’s disease. Neuropsychologia 43:675–681PubMedCrossRef Vingerhoets G, Vermeule E, Santens P (2005) Impaired intentional content learning but spared incidental retention of contextual information in non-demented patients with Parkinson’s disease. Neuropsychologia 43:675–681PubMedCrossRef
38.
Zurück zum Zitat Waterston JA, Barnes GR, Grealy MA, Collins S (1996) Abnormalities of smooth eye and head movement control in Parkinson’s disease. Ann Neurol 39:749–760PubMedCrossRef Waterston JA, Barnes GR, Grealy MA, Collins S (1996) Abnormalities of smooth eye and head movement control in Parkinson’s disease. Ann Neurol 39:749–760PubMedCrossRef
39.
Zurück zum Zitat White OB, Saint-Cyr JA, Tomlinson RD, Sharpe JA (1983) Ocular motor deficits in Parkinson’s disease. II. Control of the saccadic and smooth pursuit systems. Brain 106(Pt 3):571–587PubMedCrossRef White OB, Saint-Cyr JA, Tomlinson RD, Sharpe JA (1983) Ocular motor deficits in Parkinson’s disease. II. Control of the saccadic and smooth pursuit systems. Brain 106(Pt 3):571–587PubMedCrossRef
40.
Zurück zum Zitat Zee DS, Leigh RJ (1983) Disorders of eye movements. Neurol Clin 1:909–928PubMed Zee DS, Leigh RJ (1983) Disorders of eye movements. Neurol Clin 1:909–928PubMed
41.
Zurück zum Zitat Zgaljardic DJ, Borod JC, Foldi NS, Mattis PJ, Gordon MF, Feigin A, Eidelberg D (2006) An examination of executive dysfunction associated with frontostriatal circuitry in Parkinson’s disease. J Clin Exp Neuropsychol 28:1127–1144PubMedCrossRef Zgaljardic DJ, Borod JC, Foldi NS, Mattis PJ, Gordon MF, Feigin A, Eidelberg D (2006) An examination of executive dysfunction associated with frontostriatal circuitry in Parkinson’s disease. J Clin Exp Neuropsychol 28:1127–1144PubMedCrossRef
Metadaten
Titel
Comparison of smooth pursuit eye movement deficits in multiple system atrophy and Parkinson’s disease
verfasst von
Elmar H. Pinkhardt
Jan Kassubek
Sigurd Süssmuth
Albert C. Ludolph
Wolfgang Becker
Reinhart Jürgens
Publikationsdatum
01.09.2009
Verlag
D. Steinkopff-Verlag
Erschienen in
Journal of Neurology / Ausgabe 9/2009
Print ISSN: 0340-5354
Elektronische ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-009-5131-5

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