Computational Techniques for Eye Movements Analysis towards Supporting Early Diagnosis of Alzheimer's Disease: A Review

An opportune early diagnosis of Alzheimer's disease (AD) would help to overcome symptoms and improve the quality of life for AD patients. Research studies have identified early manifestations of AD that occur years before the diagnosis. For instance, eye movements of people with AD in different tasks differ from eye movements of control subjects. In this review, we present a summary and evolution of research approaches that use eye tracking technology and computational analysis to measure and compare eye movements under different tasks and experiments. Furthermore, this review is targeted to the feasibility of pioneer work on developing computational tools and techniques to analyze eye movements under naturalistic scenarios. We describe the progress in technology that can enhance the analysis of eye movements everywhere while subjects perform their daily activities and give future research directions to develop tools to support early AD diagnosis through analysis of eye movements.

[1]  Z. Kapoula,et al.  Long Latency and High Variability in Accuracy-Speed of Prosaccades in Alzheimer's Disease at Mild to Moderate Stage , 2011, Dementia and Geriatric Cognitive Disorders Extra.

[2]  Jenny Benois-Pineau,et al.  Goal-oriented top-down probabilistic visual attention model for recognition of manipulated objects in egocentric videos , 2015, Signal Process. Image Commun..

[3]  G. Fernández,et al.  Eye movement alterations during reading in patients with early Alzheimer disease. , 2013, Investigative ophthalmology & visual science.

[4]  Ziad M Hafed,et al.  How is visual salience computed in the brain? Insights from behaviour, neurobiology and modelling , 2017, Philosophical Transactions of the Royal Society B: Biological Sciences.

[5]  Qing Yang,et al.  Specific saccade deficits in patients with Alzheimer’s disease at mild to moderate stage and in patients with amnestic mild cognitive impairment , 2012, AGE.

[6]  Ivan Aprahamian,et al.  Eye movement analysis and cognitive processing: detecting indicators of conversion to Alzheimer’s disease , 2014, Neuropsychiatric disease and treatment.

[7]  Noel E. O'Connor,et al.  SalGAN: Visual Saliency Prediction with Generative Adversarial Networks , 2017, ArXiv.

[8]  Takahiro Okabe,et al.  Attention Prediction in Egocentric Video Using Motion and Visual Saliency , 2011, PSIVT.

[9]  Chokri Ben Amar,et al.  Prediction of visual attention with deep CNN on artificially degraded videos for studies of attention of patients with Dementia , 2017, Multimedia Tools and Applications.

[10]  James M. Rehg,et al.  Learning to recognize objects in egocentric activities , 2011, CVPR 2011.

[11]  Matthias Rauterberg,et al.  The Evolution of First Person Vision Methods: A Survey , 2014, IEEE Transactions on Circuits and Systems for Video Technology.

[12]  Ali Borji,et al.  State-of-the-Art in Visual Attention Modeling , 2013, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[13]  Ali Borji,et al.  Quantitative Analysis of Human-Model Agreement in Visual Saliency Modeling: A Comparative Study , 2013, IEEE Transactions on Image Processing.

[14]  Kamila Czarnecka,et al.  New Perspectives of Alzheimer Disease Diagnosis - the Most Popular and Future Methods. , 2018, Medicinal chemistry (Shariqah (United Arab Emirates)).

[15]  Tania Giovannetti,et al.  The Potential Utility of Eye Movements in the Detection and Characterization of Everyday Functional Difficulties in Mild Cognitive Impairment , 2015, Neuropsychology Review.

[16]  L. Itti New Eye-Tracking Techniques May Revolutionize Mental Health Screening , 2015, Neuron.

[17]  Carole Dufouil,et al.  Guidelines for reporting methodological challenges and evaluating potential bias in dementia research , 2015, Alzheimer's & Dementia.

[18]  Neil D. B. Bruce,et al.  Predicting task from eye movements: On the importance of spatial distribution, dynamics, and image features , 2016, Neurocomputing.

[19]  Nick Tyler,et al.  Locomotion and eye behaviour under controlled environment in individuals with Alzheimer's disease , 2015, 2015 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[20]  Chokri Ben Amar,et al.  Prediction of visual attention with Deep CNN for studies of neurodegenerative diseases , 2016, 2016 14th International Workshop on Content-Based Multimedia Indexing (CBMI).

[21]  Rita Cucchiara,et al.  Predicting Human Eye Fixations via an LSTM-Based Saliency Attentive Model , 2016, IEEE Transactions on Image Processing.

[22]  Frans R. J. Verhey,et al.  The impact of early dementia diagnosis and intervention on informal caregivers , 2013, Progress in Neurobiology.

[23]  Hans-Werner Gellersen,et al.  Monitoring dementia with automatic eye movements analysis , 2016 .

[24]  Jochen Laubrock,et al.  Registering eye movements during reading in Alzheimer’s disease: Difficulties in predicting upcoming words , 2014, Journal of clinical and experimental neuropsychology.

[25]  Christine T. O. Nguyen,et al.  The Eye As a Biomarker for Alzheimer's Disease , 2016, Frontiers in neuroscience.

[26]  Yorghos Tripodis,et al.  Screening Utility of the King-Devick Test in Mild Cognitive Impairment and Alzheimer Disease Dementia , 2017, Alzheimer disease and associated disorders.

[27]  Diederick C. Niehorster,et al.  What to expect from your remote eye-tracker when participants are unrestrained , 2017, Behavior Research Methods.

[28]  B. Miller,et al.  Antisaccade task reflects cortical involvement in mild cognitive impairment , 2013, Neurology.

[29]  D. Stuss,et al.  Visual attention deficits in Alzheimer's disease: simple versus conjoined feature search. , 1999, Neuropsychology.

[30]  Steve Higham,et al.  The role of working memory and attentional disengagement on inhibitory control: effects of aging and Alzheimer's disease , 2012, AGE.

[31]  Sei Naito,et al.  An Attention-Based Activity Recognition for Egocentric Video , 2014, 2014 IEEE Conference on Computer Vision and Pattern Recognition Workshops.

[32]  S. Martinez-Conde,et al.  Distinctive features of microsaccades in Alzheimer’s disease and in mild cognitive impairment , 2014, AGE.

[33]  Simone Frintrop,et al.  Computational Visual Attention , 2011, Computer Analysis of Human Behavior.

[34]  Yizhou Yu,et al.  Deep Contrast Learning for Salient Object Detection , 2016, 2016 IEEE Conference on Computer Vision and Pattern Recognition (CVPR).

[35]  Roy Jones,et al.  The effects of saliency and task difficulty on visual search performance in ageing and Alzheimer’s disease , 2004, Neuropsychologia.

[36]  G. Humphreys,et al.  The eyes have it: An exploration of eye movements in action disorganisation syndrome , 2010, Neuropsychologia.

[37]  Liliana R. Castro,et al.  Diagnosis of mild Alzheimer disease through the analysis of eye movements during reading. , 2015, Journal of integrative neuroscience.

[38]  Nick C. Fox,et al.  Eyetracking Metrics in Young Onset Alzheimer’s Disease: A Window into Cognitive Visual Functions , 2017, Front. Neurol..

[39]  A. Treisman,et al.  A feature-integration theory of attention , 1980, Cognitive Psychology.

[40]  Daniel P. Kennedy,et al.  Atypical Visual Saliency in Autism Spectrum Disorder Quantified through Model-Based Eye Tracking , 2015, Neuron.

[41]  Kris M. Kitani,et al.  Going Deeper into First-Person Activity Recognition , 2016, 2016 IEEE Conference on Computer Vision and Pattern Recognition (CVPR).

[42]  Shuyuan Yang,et al.  Object-level saliency detection with color attributes , 2016, Pattern Recognit..

[43]  James M. Rehg,et al.  Learning to Predict Gaze in Egocentric Video , 2013, 2013 IEEE International Conference on Computer Vision.

[44]  C. Koch,et al.  Faces and text attract gaze independent of the task: Experimental data and computer model. , 2009, Journal of vision.

[45]  F. Pirozzolo,et al.  Oculomotor reaction time in dementia reflects degree of cerebral dysfunction. , 1981, Science.

[46]  J. Sharpe,et al.  Saccadic eye movement dysfunction in Alzheimer's disease , 1986, Annals of neurology.

[47]  Muriel Boucart,et al.  Animal spotting in Alzheimer's disease: an eye tracking study of object categorization. , 2014, Journal of Alzheimer's disease : JAD.

[48]  C. Koch,et al.  Computational modelling of visual attention , 2001, Nature Reviews Neuroscience.

[49]  Alicia Peltsch,et al.  Saccade deficits in amnestic mild cognitive impairment resemble mild Alzheimer's disease , 2014, The European journal of neuroscience.

[50]  Nicolas Carvalho,et al.  Saccadic Eye Movements and Attentional Control in Alzheimer's Disease , 2018, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[51]  C. V. Jawahar,et al.  First Person Action Recognition Using Deep Learned Descriptors , 2016, 2016 IEEE Conference on Computer Vision and Pattern Recognition (CVPR).

[52]  Brian Barton,et al.  Visual cortex in aging and Alzheimer's disease: changes in visual field maps and population receptive fields , 2012, Front. Psychol..

[53]  Matthai Philipose,et al.  Egocentric recognition of handled objects: Benchmark and analysis , 2009, 2009 IEEE Computer Society Conference on Computer Vision and Pattern Recognition Workshops.

[54]  Radouil Tzekov,et al.  Vision function abnormalities in Alzheimer disease. , 2014, Survey of ophthalmology.

[55]  M. Cordeiro,et al.  Visual and Ocular Manifestations of Alzheimer’s Disease and Their Use as Biomarkers for Diagnosis and Progression , 2016, Front. Neurol..

[56]  Olivier A Coubard,et al.  What do we know about eye movements in Alzheimer's disease? The past 37 years and future directions. , 2016, Biomarkers in medicine.

[57]  B. Cullen,et al.  Update on Alzheimer's Disease Therapy and Prevention Strategies. , 2017, Annual review of medicine.

[58]  Camilla Forsell,et al.  Supporting Exploration of Eye Tracking Data: Identifying Changing Behaviour Over Long Durations , 2016, BELIV '16.

[59]  C. V. Jawahar,et al.  Trajectory aligned features for first person action recognition , 2016, Pattern Recognit..

[60]  Philip C. Ko,et al.  Eye movements in Alzheimer's disease. , 2015, Journal of Alzheimer's disease : JAD.

[61]  Steve Higham,et al.  The disengagement of visual attention in Alzheimer's disease: a longitudinal eye-tracking study , 2015, Front. Aging Neurosci..

[62]  Laura Dempere-Marco,et al.  Eye-Tracking Data in Visual Search Tasks: A Hallmark of Cognitive Function , 2017 .

[63]  Srinivas S. Kruthiventi,et al.  Saliency Unified: A Deep Architecture for simultaneous Eye Fixation Prediction and Salient Object Segmentation , 2016, 2016 IEEE Conference on Computer Vision and Pattern Recognition (CVPR).

[64]  L. Itti,et al.  High-throughput classification of clinical populations from natural viewing eye movements , 2012, Journal of Neurology.

[65]  Eli Brenner,et al.  Maybe they are all circles: clues and cues. , 2009, Journal of vision.

[66]  Jenny Benois-Pineau,et al.  Visual saliency maps for studies of behavior of patients with neurodegenerative diseases: Observer's versus Actor's points of view , 2013 .

[67]  Rongrong Ji,et al.  Toward Statistical Modeling of Saccadic Eye-Movement and Visual Saliency , 2014, IEEE Transactions on Image Processing.

[68]  Michael S. Landy,et al.  Computational models of visual attention , 2011, Vision Research.

[69]  R. Armstrong,et al.  Alzheimer's disease and the eye , 1996, Ophthalmic & physiological optics : the journal of the British College of Ophthalmic Opticians.

[70]  Karl J. Friston,et al.  Action perception as hypothesis testing , 2017, Cortex.

[71]  Anne B. Sereno,et al.  Slowed Prosaccades and Increased Antisaccade Errors As a Potential Behavioral Biomarker of Multiple System Atrophy , 2017, Front. Neurol..

[72]  Alan Kennedy,et al.  Book Review: Eye Tracking: A Comprehensive Guide to Methods and Measures , 2016, Quarterly journal of experimental psychology.

[73]  L F Dell'Osso,et al.  Saccadic latency measurements in dementia. , 1983, Archives of neurology.

[74]  Justin Dauwels,et al.  Diagnosis of Alzheimer ’ s Disease using Electric Signals of the Brain A Grand Challenge , 2012 .

[75]  Liam D. Kaufman,et al.  Executive deficits detected in mild Alzheimer's disease using the antisaccade task , 2012, Brain and behavior.

[76]  Osvaldo Agamennoni,et al.  Lack of contextual-word predictability during reading in patients with mild Alzheimer disease , 2014, Neuropsychologia.

[77]  B. Miller,et al.  Oculomotor function in frontotemporal lobar degeneration, related disorders and Alzheimer's disease , 2008, Brain : a journal of neurology.

[78]  Liliana R. Castro,et al.  Patients with mild Alzheimer’s disease produced shorter outgoing saccades when reading sentences , 2015, Psychiatry Research.

[79]  Brian Levine,et al.  Antisaccades: a probe into the dorsolateral prefrontal cortex in Alzheimer's disease. A critical review. , 2010, Journal of Alzheimer's disease : JAD.

[80]  Roland J. Baddeley,et al.  High frequency edges (but not contrast) predict where we fixate: A Bayesian system identification analysis , 2006, Vision Research.

[81]  Juha Koikkalainen,et al.  Differential diagnosis of neurodegenerative diseases using structural MRI data , 2016, NeuroImage: Clinical.

[82]  T. Nef,et al.  Effects of Alzheimer’s Disease on Visual Target Detection: A “Peripheral Bias” , 2016, Front. Aging Neurosci..

[83]  M. Land Eye movements and the control of actions in everyday life , 2006, Progress in Retinal and Eye Research.

[84]  M. Hayhoe,et al.  In what ways do eye movements contribute to everyday activities? , 2001, Vision Research.

[85]  Gang Wang,et al.  Recurrent Attentional Networks for Saliency Detection , 2016, 2016 IEEE Conference on Computer Vision and Pattern Recognition (CVPR).

[86]  Sarah A. Chau,et al.  Visual Selective Attention Toward Novel Stimuli Predicts Cognitive Decline in Alzheimer's Disease Patients. , 2016, Journal of Alzheimer's disease : JAD.

[87]  Francois Bremond,et al.  The Role of Information and Communication Technologies in Clinical Trials with Patients with Alzheimer’s Disease and Related Disorders , 2015, Front. Aging Neurosci..

[88]  Yu-Chiang Frank Wang,et al.  Exploring Visual and Motion Saliency for Automatic Video Object Extraction , 2013, IEEE Transactions on Image Processing.

[89]  F W Bylsma,et al.  Changes in visual fixation and saccadic eye movements in Alzheimer's disease. , 1995, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[90]  B. Långström,et al.  The use of PET in Alzheimer disease , 2010, Nature Reviews Neurology.

[91]  B. Miller,et al.  Saccade abnormalities in autopsy-confirmed frontotemporal lobar degeneration and Alzheimer disease. , 2012, Archives of neurology.

[92]  Kristen Grauman,et al.  Detecting Engagement in Egocentric Video , 2016, ECCV.

[93]  Qi Zhao,et al.  Learning saliency-based visual attention: A review , 2013, Signal Process..

[94]  A Jon Stoessl,et al.  Neuroimaging in the early diagnosis of neurodegenerative disease , 2012, Translational Neurodegeneration.

[95]  Muriel Boucart,et al.  Scene Categorization in Alzheimer's Disease: A Saccadic Choice Task , 2015, Dementia and Geriatric Cognitive Disorders Extra.

[96]  Belinda G. Smith,et al.  Saccadic eye movements as indicators of cognitive function in older adults , 2015, Neuropsychology, development, and cognition. Section B, Aging, neuropsychology and cognition.

[97]  H. Braak,et al.  The premotor region essential for rapid vertical eye movements shows early involvement in Alzheimer's disease-related cytoskeletal pathology , 2001, Vision Research.

[98]  G. Díaz,et al.  AUTOMATIC CLASSIFICATION OF STRUCTURAL MRI FOR DIAGNOSIS OF NEURODEGENERATIVE DISEASES Clasificación automática de IRM estructural para el diagnóstico de enfermedades neurodegenerativas , 2010 .

[99]  Steve Higham,et al.  Distinguishing between impairments of working memory and inhibitory control in cases of early dementia , 2016, Neuropsychologia.

[100]  Jean-Christophe Nebel,et al.  Recognition of Activities of Daily Living with Egocentric Vision: A Review , 2016, Sensors.

[101]  Sudha Seshadri,et al.  Visual Association Pathology in Preclinical Alzheimer Disease , 2006, Journal of neuropathology and experimental neurology.

[102]  Liliana R. Castro,et al.  Patients with Mild Alzheimer's Disease Fail When Using Their Working Memory: Evidence from the Eye Tracking Technique. , 2016, Journal of Alzheimer's disease : JAD.

[103]  Daniel Campos,et al.  Persistence in eye movement during visual search , 2016, Scientific Reports.

[104]  Tim J Anderson,et al.  Eye movements in neurodegenerative diseases. , 2016, Current opinion in neurology.

[105]  Heinz Hügli,et al.  Assessing the contribution of color in visual attention , 2005, Comput. Vis. Image Underst..

[106]  P Reinagel,et al.  Natural scene statistics at the centre of gaze. , 1999, Network.

[107]  M. Land,et al.  The Roles of Vision and Eye Movements in the Control of Activities of Daily Living , 1998, Perception.

[108]  Sarah A. Chau,et al.  Apathy and Attentional Biases in Alzheimer's Disease. , 2016, Journal of Alzheimer's disease : JAD.

[109]  H. Amièva,et al.  Compensatory mechanisms in higher-educated subjects with Alzheimer's disease: a study of 20 years of cognitive decline. , 2014, Brain : a journal of neurology.

[110]  Zhen Yang,et al.  Bio-inspired Visual Attention Model and Saliency Guided Object Segmentation , 2013, ICGEC.

[111]  Ali Borji,et al.  Salient object detection: A survey , 2014, Computational Visual Media.