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Specific saccade deficits in patients with Alzheimer’s disease at mild to moderate stage and in patients with amnestic mild cognitive impairment

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Abstract

Saccadic impairment in Alzheimer’s disease (AD) was found in horizontal saccades. The present study extends investigation to vertical saccades in a large number of subjects, including AD and amnestic mild cognitive impairment (aMCI). We examined both horizontal and vertical saccades in 30 healthy elderly, 18 aMCI, and 25 AD. Two tasks were used: gap (fixation target extinguishes prior to target onset) and overlap (fixation stays on after target onset). Eye movements were recorded with the Eyeseecam system. (1) Robust gap effect (shorter latencies in gap than in overlap) exists for AD and aMCI patients as for healthy elderly; (2) abnormal long latency of saccades in gap and overlap tasks for AD relative to healthy elderly and aMCI patients; (3) longer latency for aMCI patients than for healthy elderly for the overlap task; (4) significant correlation between scores of Mini-Mental State Examination (MMSE) and latencies of saccades considering the AD group only; (5) higher coefficient of variation in latency for AD patients than for healthy elderly and for aMCI patients; (6) variability of accuracy and speed is abnormally higher in AD patients than in aMCI and healthy elderly. Abnormalities of latency and latency–accuracy–speed variability reflect deficits of cerebral areas involved in the triggering and execution of saccades; latency of saccades can be used as follow-up test for aMCI and AD patients with its significant correlation with the changes of MMSE scores.

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References

  • Abel LA, Unverzagt F, Yee RD (2002) Effects of stimulus predictability and interstimulus gap on saccades in Alzheimer's disease. Dement Geriatr Cogn Disord 13(4):235–243

    Article  PubMed  Google Scholar 

  • Andersen RA, Mountcastle VB (1983) The influence of the angle of gaze upon the excitability of the light-sensitive neurons of the posterior parietal cortex. J Neurosci 3(3):532–548

    PubMed  CAS  Google Scholar 

  • Bizzi E (1968) Discharge of frontal eye field neurons during saccadic and following eye movements in unanesthetized monkeys. Exp Brain Res 6(1):69–80

    Article  PubMed  CAS  Google Scholar 

  • Boxer AL, Garbutt S, Rankin KP, Hellmuth J, Neuhaus J, Miller BL, Lisberger SG (2006a) Medial versus lateral frontal lobe contributions to voluntary saccade control as revealed by the study of patients with frontal lobe degeneration. J Neurosci 26(23):6354–6363. doi:10.1523/JNEUROSCI.0549-06.2006

    Article  PubMed  CAS  Google Scholar 

  • Boxer AL, Geschwind MD, Belfor N, Gorno-Tempini ML, Schauer GF, Miller BL, Weiner MW, Rosen HJ (2006b) Patterns of brain atrophy that differentiate corticobasal degeneration syndrome from progressive supranuclear palsy. Arch Neurol 63(1):81–86

    Article  PubMed  Google Scholar 

  • Brun A, Englund E (1981) Regional pattern of degeneration in Alzheimer's disease: neuronal loss and histopathological grading. Histopathology 5(5):549–564

    Article  PubMed  CAS  Google Scholar 

  • Bylsma FW, Rasmusson DX, Rebok GW, Keyl PM, Tune L, Brandt J (1995) Changes in visual fixation and saccadic eye movements in Alzheimer's disease. Int J Psychophysiol 19(1):33–40

    Article  PubMed  CAS  Google Scholar 

  • Crawford TJ, Higham S, Renvoize T, Patel J, Dale M, Suriya A, Tetley S (2005) Inhibitory control of saccadic eye movements and cognitive impairment in Alzheimer's disease. Biol Psychiatry 57(9):1052–1060

    Article  PubMed  Google Scholar 

  • Dorris MC, Pare M, Munoz DP (1997) Neuronal activity in monkey superior colliculus related to the initiation of saccadic eye movements. J Neurosci 17(21):8566–8579

    PubMed  CAS  Google Scholar 

  • Findlay JM, Walker R (1999) A model of saccade generation based on parallel processing and competitive inhibition. Behav Brain Sci 22(4):661–674, discussion 674–721

    PubMed  CAS  Google Scholar 

  • Fischer B, Breitmeyer B (1987) Mechanisms of visual attention revealed by saccadic eye movements. Neuropsychologia 25(1A):73–83

    Article  PubMed  CAS  Google Scholar 

  • Fischer B, Weber H (1993) Express saccades and visual attention. Behav Brain Sci 16:553–610

    Article  Google Scholar 

  • Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12(3):189–198

    Article  PubMed  CAS  Google Scholar 

  • Garbutt S, Matlin A, Hellmuth J, Schenk AK, Johnson JK, Rosen H, Dean D, Kramer J, Neuhaus J, Miller BL, Lisberger SG, Boxer AL (2008) Oculomotor function in frontotemporal lobar degeneration, related disorders and Alzheimer's disease. Brain 131(Pt 5):1268–1281

    PubMed  Google Scholar 

  • Goldberg ME, Bruce CJ (1981) Frontal eye fields in the monkey: eye movements remap the effective coordinates of visual stimuli. Society for Neuroscience 7:131

    Google Scholar 

  • Hershey LA, Whicker L Jr, Abel LA, Dell'Osso LF, Traccis S, Grossniklaus D (1983) Saccadic latency measurements in dementia. Arch Neurol 40(9):592–593

    Article  PubMed  CAS  Google Scholar 

  • Hoffman JE, Subramaniam B (1995) The role of visual attention in saccadic eye movements. Percept Psychophys 57(6):787–795

    Article  PubMed  CAS  Google Scholar 

  • Hutton JT, Nagel JA, Loewenson RB (1984) Eye tracking dysfunction in Alzheimer-type dementia. Neurology 34(1):99–102

    Article  PubMed  CAS  Google Scholar 

  • Isa T, Kobayashi Y (2004) Switching between cortical and subcortical sensorimotor pathways. Prog Brain Res 143:299–305

    Article  PubMed  Google Scholar 

  • Kapoula Z, Isotalo E, Muri RM, Bucci MP, Rivaud-Pechoux S (2001) Effects of transcranial magnetic stimulation of the posterior parietal cortex on saccades and vergence. Neuroreport 12(18):4041–4046

    Article  PubMed  CAS  Google Scholar 

  • Kapoula Z, Yang Q, Coubard O, Daunys G, Orssaud C (2004) Transcranial magnetic stimulation of the posterior parietal cortex delays the latency of both isolated and combined vergence-saccade movements in humans. Neurosci Lett 360(1–2):95–99

    Article  PubMed  CAS  Google Scholar 

  • Kapoula Z, Yang Q, Vernet M, Dieudonne B, Greffard S, Verny M (2010) Spread deficits in initiation, speed and accuracy of horizontal and vertical automatic saccades in dementia with Lewy bodies. Front Neurol 1:138

    Article  PubMed  Google Scholar 

  • Katzman R, Zhang MY, Ouang Ya Q, Wang ZY, Liu WT, Yu E, Wong SC, Salmon DP, Grant I (1988) A Chinese version of the Mini-Mental State Examination; impact of illiteracy in a Shanghai Dementia Survey. J Clin Epidemiol 41(10):971–978

    Article  PubMed  CAS  Google Scholar 

  • Kaufman LD, Pratt J, Levine B, Black SE (2010) Antisaccades: a probe into the dorsolateral prefrontal cortex in Alzheimer's disease. A critical review. J Alzheimers Dis 19(3):781–793. doi:10.3233/JAD-2010-1275

    PubMed  Google Scholar 

  • Kaufman LD, Pratt J, Levine B, Black SE (2012) Executive deficits detected in mild Alzheimer's disease using the antisaccade task. Brain and Behavior 2(1):15–21

    Article  PubMed  Google Scholar 

  • Kim EJ, Lee BH, Seo SW, Moon SY, Jung DS, Park KH, Heilman KM, Na DL (2007) Attentional distractibility by optokinetic stimulation in Alzheimer disease. Neurology 69(11):1105–1112

    Article  PubMed  CAS  Google Scholar 

  • Kurkin S, Takeichi N, Akao T, Sato F, Fukushima J, Kaneko CR, Fukushima K (2003) Neurons in the caudal frontal eye fields of monkeys signal three-dimensional tracking. Ann N Y Acad Sci 1004:262–270

    Article  PubMed  Google Scholar 

  • Leigh RJ, Zee DS (2006) The neurology of eye movement, 4th edn. Oxford University Press, New York

    Google Scholar 

  • Moser A, Kompf D, Olschinka J (1995) Eye movement dysfunction in dementia of the Alzheimer type. Dementia 6(5):264–268

    PubMed  CAS  Google Scholar 

  • Munoz DP, Broughton JR, Goldring JE, Armstrong IT (1998) Age-related performance of human subjects on saccadic eye movement tasks. Exp Brain Res 121(4):391–400

    Article  PubMed  CAS  Google Scholar 

  • Peltsch A, Hemraj A, Garcia A, Munoz DP (2009) Age-related trends in saccade characteristics among the elderly. Neurobiol Aging 32:669-79

    Google Scholar 

  • Petersen RC, Doody R, Kurz A, Mohs RC, Morris JC, Rabins PV, Ritchie K, Rossor M, Thal L, Winblad B (2001) Current concepts in mild cognitive impairment. Arch Neurol 58(12):1985–1992

    Article  PubMed  CAS  Google Scholar 

  • Pierrot-Deseilligny C, Rivaud S, Gaymard B, Agid Y (1991) Cortical control of reflexive visually-guided saccades. Brain 114(Pt 3):1473–1485

    Article  PubMed  Google Scholar 

  • Pierrot-Deseilligny C, Rivaud S, Gaymard B, Muri R, Vermersch AI (1995) Cortical control of saccades. Ann Neurol 37(5):557–567

    Article  PubMed  CAS  Google Scholar 

  • Pirozzolo FJ, Hansch EC (1981) Oculomotor reaction time in dementia reflects degree of cerebral dysfunction. Science 214(4518):349–351

    Article  PubMed  CAS  Google Scholar 

  • Pitt MC, Rawles JM (1988) The effect of ageing on saccadic latency and velocity. Neuro-ophthalmology 8:123–129

    Article  Google Scholar 

  • Reuter-Lorenz PA, Hughes HC, Fendrich R (1991) The reduction of saccadic latency by prior offset of the fixation point: an analysis of the gap effect. Percept Psychophys 49(2):167–175

    Article  PubMed  CAS  Google Scholar 

  • Rolfs M, Vitu F (2007) On the limited role of target onset in the gap task: support for the motor-preparation hypothesis. J Vis 7(10):1–20, 7

    Article  PubMed  Google Scholar 

  • Saslow MG (1967) Effects of components of displacement-step stimuli upon latency for saccadic eye movement. J Opt Soc Am 57(8):1024–1029

    Article  PubMed  CAS  Google Scholar 

  • Schlotterer G, Moscovitch M, Crapper-McLachlan D (1984) Visual processing deficits as assessed by spatial frequency contrast sensitivity and backward masking in normal ageing and Alzheimer's disease. Brain 107(Pt 1):309–325

    Article  PubMed  Google Scholar 

  • Shafiq-Antonacci R, Maruff P, Masters C, Currie J (2003) Spectrum of saccade system function in Alzheimer disease. Arch Neurol 60(9):1272–1278

    Article  PubMed  Google Scholar 

  • Sharpe JA, Zackon DH (1987) Senescent saccades. Effects of aging on their accuracy, latency and velocity. Acta Otolaryngol 104(5–6):422–428

    Article  PubMed  CAS  Google Scholar 

  • Shepherd M, Findlay JM, Hockey RJ (1986) The relationship between eye movements and spatial attention. Q J Exp Psychol A 38(3):475–491

    PubMed  CAS  Google Scholar 

  • van Beers RJ (2007) The sources of variability in saccadic eye movements. J Neurosci 27(33):8757–8770

    Article  PubMed  Google Scholar 

  • Van Gisbergen JA, Robinson DA, Gielen S (1981) A quantitative analysis of generation of saccadic eye movements by burst neurons. J Neurophysiol 45(3):417–442

    PubMed  Google Scholar 

  • Vernet M, Yang Q, Gruselle M, Trams M, Kapoula Z (2009) Switching between gap and overlap pro-saccades: cost or benefit? Exp Brain Res 197(1):49–58

    Article  PubMed  Google Scholar 

  • Warabi T, Kase M, Kato T (1984) Effect of aging on the accuracy of visually guided saccadic eye movement. Ann Neurol 16(4):449–454

    Article  PubMed  CAS  Google Scholar 

  • Whitwell JL, Jack CR Jr, Boeve BF, Parisi JE, Ahlskog JE, Drubach DA, Senjem ML, Knopman DS, Petersen RC, Dickson DW, Josephs KA (2010) Imaging correlates of pathology in corticobasal syndrome. Neurology 75(21):879–887

    Article  Google Scholar 

  • Wright CE, Harding GF, Orwin A (1984) Presenile dementia—the use of the flash and pattern VEP in diagnosis. Electroencephalogr Clin Neurophysiol 57(5):405–415

    Article  PubMed  CAS  Google Scholar 

  • Yang Q, Kapoula Z (2004) TMS over the left posterior parietal cortex prolongs latency of contralateral saccades and convergence. Invest Ophthalmol Vis Sci 45(7):2231–2239

    Article  PubMed  Google Scholar 

  • Yang Q, Kapoula Z (2008) Aging does not affect the accuracy of vertical saccades nor the quality of their binocular coordination: a study of a special elderly group. Neurobiol Aging 29(4):622–638

    Article  PubMed  Google Scholar 

  • Yang Q, Kapoula Z, Debay E, Coubard O, Orssaud C, Samson M (2006) Prolongation of latency of horizontal saccades in elderly is distance and task specific. Vision Res 46(5):751–759

    Article  PubMed  CAS  Google Scholar 

  • Yang Q, Wang T, Su N, Liu YY, **ao SF, Kapoula Z (2011) Long latency and high variability in accuracy-speed of prosaccades in Alzheimer's disease at mild to moderate stage. Dement Geriatr Cogn Disord Ext 1:318–329

    Article  Google Scholar 

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Acknowledgments

Experimental design and methods were conceived and developed by the IRIS group (Z Kapoula); support by the PICS CNRS (no: 4197). Case recruitment was supported by grant from China Ministry of Science and Technology (no: 2009BAI77B03).

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Authors and Affiliations

  1. IRIS group, UMR 8194, CNRS, Hôpital Européen Georges Pompidou, University Paris V, 20 rue Leblanc, 75015, Paris, France

    Qing Yang & Zoi Kapoula

  2. Department of Geriatric Psychiatry, Shanghai Mental Health Center, Shanghai Jiaotong University School of Medicine; Alzheimer’s Disease and Related Disorders Center,, Shanghai Jiaotong University, 600 Wan ** Nan Road, 200030, Shanghai, China

    Tao Wang, Ning Su & Shifu **ao

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  1. Qing Yang
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  2. Tao Wang
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  3. Ning Su
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  4. Shifu **ao
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  5. Zoi Kapoula
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Correspondence to Qing Yang, Shifu **ao or Zoi Kapoula.

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Yang, Q., Wang, T., Su, N. et al. Specific saccade deficits in patients with Alzheimer’s disease at mild to moderate stage and in patients with amnestic mild cognitive impairment. AGE 35, 1287–1298 (2013). https://doi.org/10.1007/s11357-012-9420-z

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  • DOI: https://doi.org/10.1007/s11357-012-9420-z

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