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Eye Movements in Neuropsychological Tasks

  • Timothy L. HodgsonEmail author
  • Gemma Ezard
  • Frouke Hermens
Chapter
Part of the Current Topics in Behavioral Neurosciences book series (CTBN, volume 41)

Abstract

This chapter reviews how recording and analysis of eye movements have been applied to understanding cognitive functioning in patients with neurological disease. Measures derived from the performance of instructed eye movement tests such as the anti-saccade and memory-guided saccade tasks have been shown to be associated with cognitive test performance and the early stages of neurodegenerative disorders including Alzheimer’s and Parkinson’s disease. Other researchers have taken an ecological approach and recorded the uninstructed pattern of saccades made by patients during performance of established neuropsychological tasks. Studies that have analysed the eye movement strategies used in a number of widely used tests are reviewed, including the Corsi blocks, Tower of London, ‘CANTAB’ Spatial Working Memory and Brixton Spatial Anticipation test. The findings illustrate that eye movements are not purely in the service of vision, but support visuospatial working memory and forward action planning. Eye movement tests and measures also have potential for application in the assessment and diagnosis of neurological disease and cognitive impairment. Establishing large-scale normative data sets in healthy older adults and use of machine learning multivariate classifier algorithms may be key to further developing eye tracking applications in neuropsychological assessment.

Keywords

Cognitive planning Dementia Executive function Frontal lobe Oculomotor Saccades 

References

  1. Aagten-Murphy D, Bays PM (2019) Functions of memory across saccadic eye movements. In: Hodgson TL (ed) Current topics in behavioural neurosciences: processes of visuo-spatial attention and working memory. Springer, New YorkGoogle Scholar
  2. Akdal G, Hodgson TL, Hill AC, Kennard C (2002) Visual object memory and memory guided saccades rely on shared mental representations. Exp Brain Res 143(4):509–514PubMedCrossRefGoogle Scholar
  3. Antoniades CA, Demeyere N, Kennard C, Humphreys GW, Hu MT (2015) Antisaccades and executive dysfunction in early drug-naive Parkinson’s disease: the discovery study. Mov Disord 30(6):843–847PubMedCrossRefGoogle Scholar
  4. Archibald NK, Hutton SB, Clarke MP, Mosimann UP, Burn DJ (2013) Visual exploration in Parkinson’s disease and Parkinson’s disease dementia. Brain 136:739–750PubMedCrossRefGoogle Scholar
  5. Asaad WF, Rainer G, Miller EK (1998) Neural activity in the primate prefrontal cortex during associative learning. Neuron 21:1399–1407PubMedCrossRefGoogle Scholar
  6. Bedell HE, Stevenson SB (2013) Eye movement testing in clinical examination. Vis Res 90:32–37PubMedCrossRefGoogle Scholar
  7. Benson PJ, Beedie SA, Shephard E, Giegling I, Rujescu D, St Clair D (2012) Simple viewing tests can detect eye movement abnormalities that distinguish schizophrenia cases from controls with exceptional accuracy. Biol Psychiatry 72(9):716–724PubMedCrossRefGoogle Scholar
  8. Brandt SA, Stark LW (1997) Spontaneous eye movements during visual imagery reflect the content of the visual scene. J Cogn Neurosci 9(1):27–38PubMedCrossRefGoogle Scholar
  9. Briand KA, Strallow D, Hening W, Poizner H, Sereno AB (1999) Control of voluntary and reflexive saccades in Parkinson’s disease. Exp Brain Res 129:38–48PubMedCrossRefGoogle Scholar
  10. Burgess PW, Shallice T (1997) The Hayling and Brixton Test manual. Thames Valley Test Co., Bury St EdmundsGoogle Scholar
  11. Cameron IGM, Pari G, Alahyane N, Brien DC, Coe BC, Stroman PW, Munoz DP (2012) Impaired executive function signals in motor brain regions in Parkinson’s disease. NeuroImage 60(2):1156–1170PubMedCrossRefGoogle Scholar
  12. Casaletto KB, Heaton RK (2017) Neuropsychological assessment: past and future. J Int Neuropsychol Soc 23:778–790PubMedPubMedCentralCrossRefGoogle Scholar
  13. Chan F, Armstrong IT, Pari G, Riopelle RJ, Munoz DP (2005) Deficits in saccadic eye-movement control in Parkinson’s disease. Neuropsychologia 43:784–796PubMedCrossRefGoogle Scholar
  14. Clark RE, Zola SM, Squire LR (2000) Impaired recognition memory in rats after damage to the hippocampus. J Neurosci 20:8853–8860PubMedPubMedCentralCrossRefGoogle Scholar
  15. Corsi PM (1972) Memory and the medial temporal region of the brain (unpublished doctoral dissertation). McGill University, MontrealGoogle Scholar
  16. Crawford TJ, Henderson L, Kennard C (1989) Abnormalities of non-visual guided eye movements in Parkinson’s disease. Brain 112:1573–1586PubMedCrossRefGoogle Scholar
  17. Crawford TJ, Shaunak S, OSullivan E, Blunt S, Lawden M, Kennard C (1997) A dissociation of internal representation and hypometric memory-guided saccades in de novo Parkinson’s disease. Abstract presented to the European conference on eye movements, UlmGoogle Scholar
  18. 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 57:1052–1060PubMedCrossRefGoogle Scholar
  19. Crutcher MD, Calhoun-Haney R, Manzanares CM, Lah JJ, Levey AI, Zola SM (2009) Eye tracking during a visual paired comparison task as a predictor of early dementia. Am J Alzheimers Dis Other Dement 24(3):258–266CrossRefGoogle Scholar
  20. De Lillo C (2019) Variations in the beneficial effects of spatial structure and serial organisation on working memory span in humans and other species. In: Hodgson TL (ed) Current topics in behavioural neurosciences: processes of visuo-spatial attention and working memory. Springer, New YorkGoogle Scholar
  21. Fukushima J, Fukushima K, Miyasaka K, Yamashita I (1994) Voluntary control of saccadic eye movement in patients with frontal cortical lesions and Parkinsonian patients in comparison with that in schizophrenics. Biol Psychiatry 36:21–30PubMedCrossRefGoogle Scholar
  22. Golding CVP (2004) Eye movements during task switching. PhD thesis, Imperial College Medical School, University of LondonGoogle Scholar
  23. Golding CVP, Danchaivijitr C, Hodgson TL, Tabrizi SJ, Kennard C (2006) Identification of an oculomotor biomarker of preclinical Huntington disease. Neurology 67(3):485–487PubMedCrossRefGoogle Scholar
  24. Grant DA, Berg E (1948) A behavioral analysis of degree of reinforcement and ease of shifting to new responses in Weigl-type card-sorting problem. J Exp Psychol 38:404–411PubMedCrossRefGoogle Scholar
  25. Hallet PE, Adams BD (1980) The predictability of saccadic latency in a novel voluntary oculomotor task. Vis Res 20:329–339CrossRefGoogle Scholar
  26. Hellmuth J, Mirsky J, Heuer HW et al (2012) Multicenter validation of a bedside antisaccade task as a measure of executive function. Neurology 78:1824–1831PubMedPubMedCentralCrossRefGoogle Scholar
  27. Hodgson TL, Golding C (2003) Executive contributions to eye movement control. In: Hyona J, Radach R, Deubel H (eds) The mind’s eye: cognitive and applied aspects of eye movement research. Elsevier, Amsterdam, pp 49–64CrossRefGoogle Scholar
  28. Hodgson TL, Dittrich W, Henderson L, Kennard C (1999) Eye movements and spatial working memory in Parkinson’s disease. Neuropsychologia 37(8):927–938PubMedCrossRefGoogle Scholar
  29. Hodgson TL, Bajwa A, Owen AM, Kennard C (2000) The strategic control of gaze direction in the Tower of London task. J Cogn Neurosci 12(5):894–907PubMedCrossRefGoogle Scholar
  30. Hodgson TL, Tiesman B, Owen AM, Kennard C (2002) Abnormal gaze strategies during problem solving in Parkinson’s disease. Neuropsychologia 40:411–422PubMedCrossRefGoogle Scholar
  31. Hodgson TL, Golding C, Molyva D, Rosenthal C, Kennard C (2004) Eye movements during task switching: reflexive, symbolic, and affective contributions to response selection. J Cogn Neurosci 16(2):318–330PubMedCrossRefGoogle Scholar
  32. Hodgson TL, Chamberlain M, Parris BA, James M, Gutowski NJ, Husain M, Kennard C (2007) The role of the ventrolateral frontal cortex in inhibitory oculomotor control. Brain 130:1525–1537PubMedCrossRefGoogle Scholar
  33. Hodgson TL, Sumner P, Molyva M, Sheridan R, Kennard C (2013) Learning and switching between stimulus-saccade associations in Parkinson’s disease. Neuropsychologia 51(7):1350–1360PubMedPubMedCentralCrossRefGoogle Scholar
  34. Hodgson TL, Parris BA, Benattayallah A, Summers IR (2015) Multi-modal representation of effector modality in frontal cortex during rule switching. Front Hum Neurosci 9:486PubMedPubMedCentralCrossRefGoogle Scholar
  35. Hodgson TL, Hermans F, Pennington K, Pickering JS, Ezard G, Clarke R, Sharma J, Owen AM (2019) Eye movements in the “Morris Maze” spatial working memory task reveal deficits in strategic planning. J Cogn Neurosci 31(4):497–509PubMedCrossRefPubMedCentralGoogle Scholar
  36. Huddy VC, Hodgson TL, Harrison I, Kapasi M, Stanley H, Thomas M, Barnes TRE, Joyce EM (2007) Gaze strategies during performance of the Tower of London planning task in first episode schizophrenia. J Abnorm Psychol 116(3):589–598PubMedPubMedCentralCrossRefGoogle Scholar
  37. Huddy VC, Hodgson TL, Ron MA, Barnes TRE, Joyce EM (2011) Abnormal negative feedback processing in first episode schizophrenia: evidence from an oculomotor rule switching task. Psychol Med 41(9):1805–1814PubMedPubMedCentralCrossRefGoogle Scholar
  38. Hunt AR, Reuther J, Hilchey MD, Klein RM (2019) The relationship between spatial attention and eye movements. In: Hodgson TL (ed) Current topics in behavioural neurosciences: processes of visuo-spatial attention and working memory. Springer, New YorkGoogle Scholar
  39. Hutton SB, Ettinger U (2006) The antisaccade task as a research tool in psychopathology: a critical review. Psychophysiology 43:302–313PubMedCrossRefGoogle Scholar
  40. Hutton SB, Tegally D (2005) The effects of dividing attention on smooth pursuit eye tracking. Exp Brain Res 163:306–313PubMedCrossRefGoogle Scholar
  41. Hutton SB, Huddy V, Barnes TRE, Robbins TW, Crawford TJ, Kennard C, Joyce EM (2004) The relationship between antisaccades, smooth pursuit, and executive dysfunction in first-episode schizophrenia. Biol Psychiatry 56:553–559PubMedCrossRefGoogle Scholar
  42. Ichinose M, Park S (2019) Mechanisms underlying visuospatial working memory impairments in schizophrenia. In: Hodgson TL (ed) Current topics in behavioural neurosciences: processes of visuo-spatial attention and working memory. Springer, New YorkGoogle Scholar
  43. Iliffe S, Pealing L (2010) Subjective memory problems. Br Med J 340:1425CrossRefGoogle Scholar
  44. Kaller CP, Rahm B, Bolkenius K, Unterrainer JM (2009) Eye movements and visuospatial problem solving: identifying separable phases of complex cognition. Psychophysiology 46(4):818–883PubMedCrossRefGoogle Scholar
  45. Kaufman LD, Pratt J, Levine B, Black SE (2012) Executive deficits detected in mild Alzheimers disease using the antisaccade task. Brain Behav 2(1):15–21PubMedPubMedCentralCrossRefGoogle Scholar
  46. Ketcham CJ, Hodgson TL, Kennard C, Stelmach GE (2003) Memory-motor transformations are impaired in Parkinson’s disease. Exp Brain Res 149(1):30–39PubMedCrossRefGoogle Scholar
  47. Kinsler V, Carpenter RHS (1995) Saccadic eye movements while reading music. Vis Res 35:1447–1458PubMedCrossRefGoogle Scholar
  48. Kitagawa M, Fukushima J, Tashiro K (1994) Relationship between antisaccades and the clinical symptoms in Parkinson’s disease. Neurology 44:2285–2289PubMedCrossRefGoogle Scholar
  49. Lagun D, Manzanares C, Zola SM, Buffalo EA, Agichtein E (2011) Detecting cognitive impairment by eye movement analysis using automatic classification algorithms. J Neurosci Methods 201:196–203PubMedPubMedCentralCrossRefGoogle Scholar
  50. Land MF (2019) The evolution of gaze shifting eye movements. In: Hodgson TL (ed) Current topics in behavioural neurosciences: processes of visuo-spatial attention and working memory. Springer, New YorkGoogle Scholar
  51. Land MF, Furneaux S (1997) The knowledge base of the oculomotor system. Philos Trans R Soc Lond B 352:1231–1239CrossRefGoogle Scholar
  52. Land MF, Lee D (1994) Where we look when we steer. Nature 369:742–744PubMedCrossRefGoogle Scholar
  53. Land MF, Mennie N, Rusted J (1999) The roles of vision and eye movements in the control of activities of daily living. Perception 28:1311–1328PubMedPubMedCentralCrossRefGoogle Scholar
  54. Leigh RJ, Zee DS (2006) The neurology of eye movements, 4th edn. Oxford University Press, OxfordGoogle Scholar
  55. Lueck CJ, Tanyeri S, Crawford TJ, Henderson L, Kennard C (1990) Antisaccades and remembered saccades in Parkinson’s disease. J Neurol Neurosurg Psychiatry 53:284–288PubMedPubMedCentralCrossRefGoogle Scholar
  56. Lueck CJ, Crawford TL, Henderson L, Van Gisbergen JAM, Duysens J, Kennard C (1992) Saccadic eye movements in Parkinson’s disease II remembered saccades: towards a unified hypothesis. Q J Exp Psychol 45A(2):211–233CrossRefGoogle Scholar
  57. Martin L, Tapper A, Gonzalez DA, Leclerc M, Niechwiej-Szwedo E (2017) The effects of task-relevant saccadic eye movements performed during the encoding of a serial sequence on visuospatial memory performance. Exp Brain Res 235(5):1519–1529PubMedCrossRefGoogle Scholar
  58. Mosimann UP, Felblinger J, Ballinari P, Hess W, Muri RM (2004) Visual exploration behaviour during clock reading in Alzheimer’s disease. Brain 127:431–438PubMedCrossRefGoogle Scholar
  59. Nitschke K, Ruh N, Kappler S, Stahl C, Kaller CP (2012) Dissociable stages of problem solving (I): temporal characteristics revealed by eye-movement analyses. Brain Cogn 80:160–169PubMedCrossRefGoogle Scholar
  60. Olton DS (1982) Spatially organised behaviours of animals: behavioural and neurological studies. In: Potegal M (ed) Spatial abilities. Pergamon, LondonGoogle Scholar
  61. Owen AM, Sahakian BJ, Hodges JR, Summers BA, Polkey CE, Robbins TW (1995) Dopamine-dependent fronto-striatal planning deficits in early Parkinson’s disease. Neuropsychology 9:126–140CrossRefGoogle Scholar
  62. Owen AM, Iddon JL, Hodges JR, Summers BA, Robbins TW (1997) Spatial and non-spatial working memory at different stages of Parkinson’s disease. Neuropsychologia 35(4):519–532CrossRefGoogle Scholar
  63. Passingham RE (1985) Memory of monkeys (Macaca mulatta) with lesions in the prefrontal cortex. Behav Neurosci 99:3–21PubMedCrossRefGoogle Scholar
  64. Pasupathy A, Miller EK (2005) Different time courses of learning-related activity in the prefrontal cortex and striatum. Nature 433:873–876PubMedCrossRefGoogle Scholar
  65. Patt VM, Thomas ML, Minassian A, Geyer MA, Brown GG, Perry W (2014) Disentangling working memory processes during spatial span assessment: a modelling analysis of preferred eye movement strategies. J Clin Exp Neuropsychol 36(2):186–204PubMedPubMedCentralCrossRefGoogle Scholar
  66. Pavisic IM, Firth NC, Parsons S, Martinez Rego D, Shakespeare TJ, Yong KXX, Slattery CF, Paterson RW, Foulkes AJM, Macpherson K, Carton AM, Alexander DC, Shawe-Taylor J, Fox NC, Schott JM, Crutch SJ, Primativo S (2017) Eye tracking metrics in young onset Alzheimer’s disease: a window into cognitive visual functions. Front Neurol 8:377PubMedPubMedCentralCrossRefGoogle Scholar
  67. Pensyl CC, Benjamin WJ (2006) Ocular motility. In: Benjamin WJ (ed) Borish’s clinical refraction, 2nd edn. Butterworth, St Louis, pp 356–399CrossRefGoogle Scholar
  68. Petrides M, Milner B (1982) Deficits on subject-ordered tasks after frontal- and temporal-lobe lesions in man. Neuropsychologia 20:249–262PubMedCrossRefGoogle Scholar
  69. Primativo S, Clark C, Yong KXX, Firth NC, Nicholas J, Alexander D, Warren JD, Rohrer JD, Crutch SJ (2017) Eyetracking metrics reveal impaired spatial anticipation in behavioural variant frontotemporal dementia. Neuropsychologia 106:328–340PubMedCrossRefGoogle Scholar
  70. Rivaud-Pechoux S, Vidailhet M, Brandel JP, Gaymard B (2007) Mixing pro- and antisaccades in patients with parkinsonian syndromes. Brain 130:256–264PubMedCrossRefGoogle Scholar
  71. Robert MPA, Nachev PC, Hicks SL, Golding CVP, Tabrizi SJ, Kennard C (2009) Saccadometry of conditional rules in presymptomatic Huntington’s disease. basic and clinical aspects of vertigo and dizziness. Ann N Y Acad Sci 1164:444–450PubMedCrossRefGoogle Scholar
  72. Schon F, Hodgson TL, Mort D, Kennard C (2001) Ocular flutter associated with a localised lesion in the paramedian pontine reticular formation. Ann Neurol 50(3):413–416PubMedCrossRefGoogle Scholar
  73. Shakespeare TJ, Kaski D, Yong KXX, Paterson RW, Slattery CF, Ryan NS, Schott JM, Crutch SJ (2015) Abnormalities of fixation, saccade and pursuit in posterior cortical atrophy. Brain 138:1976–1991PubMedPubMedCentralCrossRefGoogle Scholar
  74. Shallice T (1982) Specific impairments of planning. Philos Trans R Soc Lond B 298:199–209CrossRefGoogle Scholar
  75. Stubbs J, Corrow S, Kiang B, Panenka W, Barton J (2018) The effects of enhanced attention and working memory on smooth pursuit eye movement. Exp Brain Res 236:485–495PubMedCrossRefGoogle Scholar
  76. Tremblay S, Saint-Aubin J, Jalbert A (2006) Rehearsal in serial memory for visual-spatial information: evidence from eye movements. Psychon Bull Rev 13(3):452–457PubMedCrossRefGoogle Scholar
  77. Walker R, Husain M, Hodgson TL, Harrison J, Kennard C (1998) Saccadic eye movements and working memory following damage to human prefrontal cortex. Neuropsychologia 36(11):1141–1159PubMedCrossRefPubMedCentralGoogle Scholar
  78. Wong AMF (2008) Eye movement disorders. Oxford University Press, OxfordGoogle Scholar
  79. Zokaei N, Husain M (2019) Working memory in Alzheimer’s disease and Parkinson’s disease. In: Hodgson TL (ed) Current topics in behavioural neurosciences: processes of visuo-spatial attention and working memory. Springer, New YorkGoogle Scholar
  80. Zola SM, Squire LR, Teng E, Stefanacci L, Buffalo EA, Clark RE (2000) Impaired recognition memory in monkeys after damage limited to the hippocampal region. J Neurosci 20:451–463PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Timothy L. Hodgson
    • 1
    Email author
  • Gemma Ezard
    • 2
  • Frouke Hermens
    • 1
  1. 1.School of Psychology, University of LincolnLincolnUK
  2. 2.Lincolnshire Partnership NHS Foundation TrustLincolnUK

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