Generic placeholder image

Current Alzheimer Research


ISSN (Print): 1567-2050
ISSN (Online): 1875-5828

Research Article

Oculomotor Abnormalities during Reading in the Offspring of Late-Onset Alzheimer’s Disease

Author(s): Gerardo Fernández*, Ana Paula González, Carolina Abulafia, Leticia Fiorentini, Osvaldo Agamennoni and Salvador M. Guinjoan

Volume 19, Issue 3, 2022

Published on: 23 May, 2022

Page: [212 - 222] Pages: 11

DOI: 10.2174/1567205019666220413075840

Price: $65


Introduction: Eye movement patterns during reading are well defined and documented. Each eye movement ends up in a fixation point, which allows the brain to process the incoming information and program the following saccade. In this work, we investigated whether eye movement alterations during a reading task might be already present in middle-aged, cognitively normal offspring of late-onset Alzheimer’s disease (O-LOAD).

Methods: 18 O-LOAD and 18 age-matched healthy individuals with no family history of LOAD participated in the study. Participants were seated in front of a 20-inch LCD monitor, and single sentences were presented on it. Eye movements were recorded with an eye tracker with a sampling rate of 1000 Hz.

Results: Analysis of eye movements during reading revealed that O-LOAD displayed more fixations, shorter saccades, and shorter fixation durations than controls.

Conclusion: The present study shows that O-LOAD experienced alterations in their eye movements during reading. O-LOAD eye movement behavior could be considered an initial sign of oculomotor impairment. Hence, the evaluation of eye movement during reading might be a useful tool for monitoring well-defined cognitive resources.

Keywords: Offspring of late-onset, Alzheimer’s disease, reading performance, oculomotor behavior, cognitive impairments, O-LOAD

Rayner K. Eye movements in reading and information processing: 20 years of research. Psychol Bull 1998; 124(3): 372-422.
[] [PMID: 9849112]
Kennedy A, Pynte J. Parafoveal-on-foveal effects in normal reading. Vision Res 2005; 45(2): 153-68.
[] [PMID: 15581917]
Kennedy A, Pynte J, Murray WS, Paul SA. Frequency and predictability effects in the Dundee Corpus: An eye movement analysis. Q J Exp Psychol 2013; 66(3): 601-18.
[] [PMID: 22643118]
Kliegl R. Toward a perceptual-span theory of distributed processing in reading: A reply to Rayner, Pollatsek, Drieghe, Slattery, and Reichle. J Exp Psychol Gen 2007; 136: 530-7.
Kliegl R, Nuthmann A, Engbert R. Tracking the mind during reading: The influence of past, present, and future words on fixation durations. J Exp Psychol Gen 2006; 135(1): 12-35.
[] [PMID: 16478314]
Vitu F, Brysbaert M, Lancelin D. A test of parafoveal on-foveal effects with pairs of orthographically related words. J Cogn Psychol 2004; 16: 154-77.
Fernández G, Shalom D, Kliegl R, Sigman M. Eye movements during reading proverbs and regular sentences: The incoming word predictability effect. Lang Cogn 2014; 29(3): 260-73.
Fernández G, Orozco D, Agamennoni O, et al. Visual Processing during short-term memory binding in mild Alzheimer’s Disease. J Alzheimers Dis 2018; 63(1): 185-94.
[] [PMID: 29614644]
Rayner K, Ashby J, Pollatsek A, Reichle ED. The effects of frequency and predictability on eye fixations in reading: Implications for the E-Z Reader model. J Exp Psychol Hum Percept Perform 2004; 30(4): 720-32.
[] [PMID: 15301620]
Fernández G, Manes F, Rotstein NP, et al. Lack of contextual-word predictability during reading in patients with mild Alzheimer disease. Neuropsycholy 2014; 62: 143-51.
[] [PMID: 25080188]
Yan M, Kliegl R, Richter EM, Nuthmann A, Shu H. Flexible saccade-target selection in Chinese reading. Q J Exp Psychol 2010; 63(4): 705-25.
[] [PMID: 19742387]
Li X, Liu P, Rayner K. Eye movement guidance in Chinese reading: Is there a preferred viewing location? Vision Res 2011; 51(10): 1146-56.
[] [PMID: 21402094]
Wei W, Li X, Pollatsek A. Word properties of a fixated region affect outgoing saccade length in Chinese reading. Vision Res 2013; 80: 1-6.
[] [PMID: 23231957]
Just MA, Carpenter PA, Woolley JD. Paradigms and processes in reading comprehension. J Exp Psychol Gen 1982; 111(2): 228-38.
[] [PMID: 6213735]
Fernández G, Castro LR, Schumacher M, Agamennoni OE. Diagnosis of mild Alzheimer disease through the analysis of eye movements during reading. J Integr Neurosci 2015; 14(1): 121-33.
[] [PMID: 25728469]
Schotter ER, Berry RW, McKenzie CRM, Rayner K. Gaze bias: Selective encoding and liking effects. Vis Cogn 2010; 18: 1113-32.
Moreno J, León J, Botella J. Age differences in eye movements during reading: Degenerative problems or compensatory strategy? A meta-analysis. In: Eur Psychol. 2018; pp. 1-15.
Cabeza R, Anderson ND, Locantore JK, McIntosh AR. Aging gracefully: Compensatory brain activity in high-performing older adults. Neuroimage 2002; 17(3): 1394-402.
[] [PMID: 12414279]
Mosimann UP, Felblinger J, Ballinari P, Hess CW, Müri RM. Visual exploration behaviour during clock reading in Alzheimer’s disease. Brain 2004; 127(Pt 2): 431-8.
[] [PMID: 14691059]
Mendez MF, Mendez MA, Martin R, Smyth KA, Whitehouse PJ. Complex visual disturbances in Alzheimer’s disease. Neurology 1990; 40(3 Pt 1): 439-43.
[] [PMID: 2314585]
Lueck KL, Mendez MF, Perryman KM. Eye movement abnormalities during reading in patients with Alzheimer disease. Neuropsychiatry Neuropsychol Behav Neurol 2000; 13(2): 77-82.
[PMID: 10780625]
Frank EM. Effect of Alzheimer’s disease on communication function. J S C Med Assoc 1994; 90(9): 417-23.
[PMID: 7967534]
Taler V, Phillips NA. Language performance in Alzheimer’s disease and mild cognitive impairment: A comparative review. J Clin Exp Neuropsychol 2008; 30(5): 501-56.
[] [PMID: 18569251]
Fielding J, Kilpatrick T, Millist L, White O. Multiple sclerosis: Cognition and saccadic eye movements. J Neurol Sci 2009; 277(1-2): 32-6.
[] [PMID: 18977003]
Posner MI. Orienting of attention. Q J Exp Psychol 1980; 32(1): 3-25.
[] [PMID: 7367577]
Hoffman JV. In search of the “simple view” of reading comprehension. In: Susan E. I, Gerald GD, (eds.), Handbook of research on reading comprehension. Madison Ave, New York 2009; pp. 54-66.
Itoh N, Fukuda T. Comparative study of eye movements in extent of central and peripheral vision and use by young and elderly walkers. Percept Mot Skills 2002; 94(3 Pt 2): 1283-91.
[] [PMID: 12186250]
Arnáiz E, Almkvist O. Neuropsychological features of mild cognitive impairment and preclinical Alzheimer’s disease. Acta Neurol Scand Suppl 2003; 179: 34-41.
[] [PMID: 12603249]
Bäckman L, Jones S, Berger AK, Laukka EJ, Small BJ. Multiple cognitive deficits during the transition to Alzheimer’s disease. J Intern Med 2004; 256(3): 195-204.
[] [PMID: 15324363]
Abulafia C, Fiorentini L, Loewenstein DA, et al. Executive functioning in cognitively normal middle-aged offspring of late-onset Alzheimer’s disease patients. J Psychiatr Res 2019; 112: 23-9.a.
[] [PMID: 30836202]
Mosconi L, Berti V, Swerdlow RH, Pupi A, Duara R, de Leon M. Maternal transmission of Alzheimer’s disease: Prodromal metabolic phenotype and the search for genes. Hum Genomics 2010; 4(3): 170-93.
[] [PMID: 20368139]
Sánchez SM, Abulafia C, Duarte-Abritta B, et al. Failure to recover from proactive semantic interference and abnormal limbic connectivity in asymptomatic, middle-aged offspring of patients with late-onset Alzheimer’s disease. J Alzheimers Dis 2017; 60(3): 1183-93.
[] [PMID: 28984601]
Sheng C, Xia M, Yu H, et al. Abnormal global functional network connectivity and its relationship to medial temporal atrophy in patients with amnestic mild cognitive impairment. PLoS One 2017; 12(6): e0179823.
[] [PMID: 28650994]
Abulafia C, Loewenstein D, Curiel-Cid R, et al. Brain structural and amyloid correlates of recovery from semantic interference in cognitively normal individuals with or without family history of late-onset Alzheimer’s Disease. J Neuropsych Clin 2019; 31(1): 25-36.b.
Reinvang I, Grambaite R, Espeseth T. Executive dysfunction in MCI: Subtype or early symptom. Int J Alzheimers Dis 2012; 2012: 936272.
[] [PMID: 22693679]
Duarte-Abritta B, Villarreal MF, Abulafia C, et al. Cortical thickness, brain metabolic activity, and in vivo amyloid deposition in asymptomatic, middle-aged offspring of patients with late-onset Alzheimer’s disease. J Psychiatr Res 2018; 107: 11-8.
[] [PMID: 30308328]
Rösler A, Mapstone ME, Hays AK, et al. Alterations of visual search strategy in Alzheimer’s disease and aging. Neuropsychology 2000; 14(3): 398-408.
[] [PMID: 10928743]
Pereira ML. Camargo Mv, Aprahamian I, Forlenza OV. Eye movement analysis and cognitive processing: Detecting indicators of conversion to Alzheimer’s disease. Neuropsychiatr Dis Treat 2014; 10: 1273-85.
[] [PMID: 25031536]
Olsen RK, Chiew M, Buchsbaum BR, Ryan JD. The relationship between delay period eye movements and visuospatial memory. J Vis 2014; 14(1): 1-11.
[] [PMID: 24403394]
Sperling RA, Aisen PS, Beckett LA, et al. Toward defining the preclinical stages of Alzheimer’s disease: Recommendations from the national institute on aging-Alzheimer’s association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimers Dement 2011; 7(3): 280-92.
[] [PMID: 21514248]
Abulafia C, Duarte-Abritta B, Villarreal MF, et al. Relationship between cognitive and sleep-wake variables in asymptomatic offspring of patients with late-onset Alzheimer’s disease. Front Aging Neurosci 2017; 9: 93.
[] [PMID: 28424614]
Wilson KE, Abulafia C, Loewenstein DA, et al. Individual cognitive and depressive traits associated with maternal versus paternal family history of Late-onset Alzheimer’s disease: Proactive semantic interference versus standard neuropsychological assessments. Personal Med Psych 2018; 11: 1-6.
Duarte-Abritta B, Sánchez SM, Abulafia C, et al. Amyloid and anatomical correlates of executive functioning in middle-aged offspring of patients with late-onset Alzheimer’s disease. Psychiatry Res Neuroimaging 2021; 316: 111342.
[] [PMID: 34365076]
Axelrud LK, Sato JR, Santoro ML, et al. Genetic risk for Alzheimer’s disease and functional brain connectivity in children and adolescents. Neurobiol Aging 2019; 82: 10-7.
[] [PMID: 30305005]
Del Cerro I, Villarreal MF, Abulafia C, et al. Disrupted functional connectivity of the locus coeruleus in healthy adults with parental history of Alzheimer’s disease. J Psychiatr Res 2020; 123: 81-8.
[] [PMID: 32044590]
Sánchez SM, Duarte-Abritta B, Abulafia C, et al. White matter fiber density abnormalities in cognitively normal adults at risk for late-onset Alzheimer’s disease. J Psychiatr Res 2020; 122: 79-87.
[] [PMID: 31931231]
Folstein MF, Folstein SE, McHugh PR. “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975; 12(3): 189-98.
[] [PMID: 1202204]
Rosen WG, Terry RD, Fuld PA, Katzman R, Peck A. Pathological verification of ischemic score in differentiation of dementias. Ann Neurol 1980; 7(5): 486-8.
[] [PMID: 7396427]
Reitan R, Wolfson D. Neuropsychological test battery: Theory and clinical interpretation. In: Neuropsychology press Tuscon. 1985; p. AZ.
Rey A. L’examen clinique en psychologie. Paris: Presses Universitaires de France 1964.
Spreen O, Benton A. Neurosensory Center Comprehensive Examination for Aphasia (NCCEA). Victoria, British Columbia: University of Victoria Neuropsychology Laboratory 1977.
Delis DC, Kaplan E, Kramer JH. Delis-Kaplan executive function system: Technical manual. Psychological Corporation 2001.
Wechsler D. Wechsler adult intelligence scale-III. San Antonio, TX: The Psychological Corporation 1997.
Culbertson WC, Zillmer E. Tower of London-Drexel University (TOLDX). Multi-Health Systems 2001.
Golden CJ. Stroop color and word test: A manual for clinical and experimental uses. Chicago, IL: Stoelting 1978.
Sierra SN, Montañes P, Sierra Matamoros FA, Burin D. Estimating intelligence in Spanish: Regression equations with the Word Accentuation Test and demographic variables in Latin America. Appl Neuropsychol Adult 2015; 22(4): 252-61.
[] [PMID: 25402323]
Beck AT, Steer RA, Brown GK. Beck depression inventory-II. San Antonio 1996 78(2): 490-8.
Fernández G, Mandolesi P, Rotstein NP, Colombo O, Agamennoni O, Politi LE. Eye movement alterations during reading in patients with early Alzheimer disease. Invest Ophthalmol Vis Sci 2013; 54(13): 8345-52.
[] [PMID: 24282223]
Engbert R, Kliegl R. Microsaccades uncover the orientation of covert attention. Vision Res 2003; 43(9): 1035-45.
[] [PMID: 12676246]
Dambacher M, Kliegl R, Hofmann M, Jacobs AM. Frequency and predictability effects on event-related potentials during reading. Brain Res 2006; 1084(1): 89-103.
[] [PMID: 16545344]
Hoffman J. Visual attention and eye movements Attention Hove: Psychology Press 1998; 31(2): 119-54.
Eckstein MK, Guerra-Carrillo B, Miller Singley AT, Bunge SA. Beyond eye gaze: What else can eyetracking reveal about cognition and cognitive development? Dev Cogn Neurosci 2017; 25: 69-91.
[] [PMID: 27908561]
Meghanathan RN, van Leeuwen C, Nikolaev AR. Fixation duration surpasses pupil size as a measure of memory load in free viewing. Front Hum Neurosci 2015; 8: 1063.
[] [PMID: 25653606]
Chen P, Ratcliff G, Belle SH, Cauley JA, DeKosky ST, Ganguli M. Cognitive tests that best discriminate between presymptomatic AD and those who remain nondemented. Neurology 2000; 55(12): 1847-53.
[] [PMID: 11134384]
Fernandez G, Parra Mario A. Oculomotor behaviors and integrative memory functions in the Alzheimer’s clinical syndrome. J Alzheimers Dis 2021.
[] [PMID: 34151787]
Leigh RJ, Zee DS. The neurology of eye movements. Oxford: Oxford University Press 2006; pp. 151-86.
Scudder CA, Kaneko CS, Fuchs AF. The brainstem burst generator for saccadic eye movements: A modern synthesis. Exp Brain Res 2002; 142(4): 439-62.
[] [PMID: 11845241]
Wurtz RH, Goldberg ME. The Neurobiology of Saccadic Eye Movements. Reviews of Oculomotor Research Amsterdam: Elsevier 1989; 3: 257-84.
Liversedge SP, Findlay JM. Saccadic eye movements and cognition. Trends Cogn Sci 2000; 4(1): 6-14.
[] [PMID: 10637617]
Munoz DP, Armstrong IT, Hampton KA, Moore KD, Kimberly D. Altered control of visual fixation and saccadic eye movements in attention-deficit hyperactivity disorder. J Neurophysiol 2003; 90(1): 503-14.
[] [PMID: 12672781]
Hikosaka O, Takikawa Y, Kawagoe R. Role of the basal ganglia in the control of purposive saccadic eye movements. Physiol Rev 2000; 80(3): 953-78.
[] [PMID: 10893428]
Fernández G, Guinjoan S, Sapognikoff M, Orozco D, Agamennoni O. Contextual predictability enhances reading performance in patients with schizophrenia. Psychiatry Res 2016; 241: 333-9.
[] [PMID: 27236087]
Fernández G, Laubrock J, Mandolesi P, Colombo O, Agamennoni O. Registering eye movements during reading in Alzheimer’s disease: Difficulties in predicting upcoming words. J Clin Exp Neuropsychol 2014; 36(3): 302-16.
[] [PMID: 24580505]

Rights & Permissions Print Export Cite as
© 2023 Bentham Science Publishers | Privacy Policy