Saccadic velocity as an arousal index in naturalistic tasks

Neuroscience and Biobehavioral Reviews

Volumn 37, Issue 5, 2013, Pages 968-975

  Di Stasi, Leandro L ^a,b   Catena, Andrés ^b   Cañas, José J ^b   Macknik, Stephen L ^a   Martinez Conde, Susana ^a  

^a BARROW NEUROLOGICAL INSTITUTE   (United States)

^b UNIVERSITY OF GRANADA   (Spain)

Author keywords

Air traffic control; Arousal neurons; Cognitive load; Complex tasks; Depressive disorder; Driving simulation; Drowsy driving; Eye movements; Main sequence; Mental fatigue; Mental workload; Neuroergonomics; Omnipause neurons; Saccades; Sleep deprivation; Warning system

Indexed keywords

ADRENERGIC SYSTEM; ARMY; AROUSAL; COGNITION; COGNITIVE DEFECT; ERGONOMICS; GAZE; HUMAN; MAJOR DEPRESSION; MOTIVATION; PRIORITY JOURNAL; RETINA; REVIEW; SACCADIC EYE MOVEMENT; SACCADIC VELOCITY; SLEEP DEPRIVATION; SLEEP WAKING CYCLE; SOMNOLENCE; STIMULUS RESPONSE; TASK PERFORMANCE; VISUAL SYSTEM PARAMETERS;

AROUSAL; HUMAN ENGINEERING; HUMANS; MENTAL DISORDERS; REACTION TIME; SACCADES; SLEEP DEPRIVATION;

EID: 84877351307     PISSN: 01497634     EISSN: 18737528     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2013.03.011     Document Type: Review

References (106)

1. Ahlstrom U., Friedman-Berg F.J. Using eye movement activity as a correlate of cognitive workload. Int. J. Ind. Ergon. 2006, 36:623-636.
2. Ahlstrom C., Nyström M., Holmqvist K., Fors C., Sandberg D., Anund A., Kecklund G., Åkerstedt T. Fit-for-duty test for estimation of drivers' sleepiness level: Eye movements improve the sleep/wake predictor. Transport. Res. Part C: Emerg. Technol. 2013, 26:20-32.
3. AIDE [Adaptive Integrated Driver-vehicle Interface], 2012. AIDE Project [Official web], June. Retrieved from . http://www.aide-eu.org/.
4. Åkerstedt T., Gillberg M. Subjective and objective sleepiness in the active individual. Int. J. Neurosci. 1990, 52:29-37.
5. App E., Debus G. Saccadic velocity and activation: development of a diagnostic tool for assessing energy regulation. Ergonomics 1998, 41:689-697.
6. Bahill A.T., Stark L. Overlapping saccades and glissades are produced by fatigue in the saccadic eye movement system. Exp. Neurol. 1975, 48:95-106.
7. Bahill A.T., Clark M.R., Stark L. The main sequence, a tool for studying human eye movements. Math. Biosci. 1975, 24:191-204.
8. Ball D., Glue P., Wilson S., Nutt D. Pharmacology of saccadic eye movements in man, 1. 1. Effects of the benzodiazepine receptor ligands midazolam and flumazenil. Psychopharmacology 1991, 105:361-367.
9. Baloh R.W., Sills A.W., Kumley W.E., Honrubia V. Quantitative measurement of saccade amplitude, duration, and velocity. Neurology 1975, 25:1065-1070.
10. Barker M.J., Greenwood K.M., Jackson M., Crowe S.F. Cognitive effects of long-term benzodiazepine use: a meta-analysis. CNS Drugs 2004, 18:37-48.
11. Becker W. Saccadic eye movements as a control system: metrics. Reviews of Oculomotor Research. The Neurobiology of Saccadic Eye Movements 1989, vol. 3:13-67. Elsevier, Hillsdale NJ.
12. Becker W., Fuchs A.F. Further properties of the human saccadic system: eye movements and correction saccades with and without visual fixation points. Vision Research 1969, 9:1247-1258.
13. Benedetto S., Pedrotti M., Bridgeman B. Microsaccades and exploratory saccades in a naturalistic environment. J. Eye Movement Res. 2011, 4:1-10.
14. Bocca M.-L., Denise P. Total sleep deprivation effect on disengagement of spatial attention as assessed by saccadic eye movements. Clin. Neurophysiol. 2006, 117:894-899.
15. Boghen D., Troost B.T., Daroff R.B., Dell'Osso L.F., Birkett J.E. Velocity characteristics of normal human saccades. Invest. Ophthalmol. Vis. Sci. 1974, 13:619-623.
16. Cacciabue P.C. Modelling Driver Behaviour in Automotive Environments: Critical Issues in Driver Interactions with Intelligent Transport Systems 2007, Springer-Verlag Inc, New York, NY.
17. Cacciabue P.C., Carsten O. A simple model of driver behaviour to sustain design and safety assessment of automated systems in automotive environments. Appl. Ergon. 2010, 41:187-197.
18. Casucci M., Marchitto M., Cacciabue P.C. A numerical tool for reproducing driver behaviour: experiments and predictive simulations. Appl. Ergon. 2010, 41:198-210.
19. Chalder T., Berelowitz G., Pawlikowska J., Watts L., Wessely D. Development of a fatigue scale. J. Psychosom. Res. 1993, 37:147-153.
20. Collewijn H., Steinman R.M., Erkelens C.J., Pizlo Z., Van Der Steen J. The effect of freeing the head on eye movement characteristics during 3-D shifts of gaze and tracking. The Head-Neck Sensory Motor System 1992, Oxford, London, UK. A. Berthoz, P.P. Vidal, W. Graf (Eds.).
21. Cooper G.E., Harper R.P. The Use of Pilot Ratings in the Evaluation of Aircraft Handling Qualities (NASA Ames Technical Report NASA TN-D-5153) 1969, NASA Ames Research Center, Moffett Field, CA.
22. De Genaro L., Ferrara M., Urbani L., Bertini M. Oculomotor impairment after 1 night of total sleep deprivation: a dissociation between measures of speed and accuracy. Clin. Neurophysiol. 2000, 111:1771-1778.
23. Dey A.K., Mann D.D. A complete task analysis to measure the workload associated with operating an agricultural sprayer equipped with a navigation device. Appl. Ergon. 2010, 41:146-149.
24. Diefendorf A.R., Dodge R. An experimental study of the ocular reactions of the insane from photographic records. Brain 1908, 31:451-489.
25. Di Stasi L.L., Álvarez V., Cañas J.J., Maldonado A., Catena A., Antolí A., Cándido A. Risk behaviour and mental workload: multimodal assessment techniques applied to motorbike riding simulation. Transport. Res. Part F 2009, 12:361-370.
26. Di Stasi L.L., Antolí A., Cañas J.J. Main sequence: an index for detecting mental workload variation in complex tasks. Appl. Ergon. 2011, 42:807-813.
27. Di Stasi L.L., Contreras D., Cañas J.J., Cándido A., Maldonado A., Catena A. The consequences of unexpected emotional sounds on driving risk behaviuor. Safety Sci. 2010, 48:1463-1468.
28. Di Stasi L.L., Marchitto M., Antolí A., Baccino T., Cañas J.J. Approximation of on-line mental workload index in ATC simulated multitasks. J. Air Trans. Manage. 2010, 16:330-333.
29. Di Stasi L.L., Renner R., Staehr P., Helmert J.R., Velichkovsky B.M., Cañas J.J., Catena A., Pannasch S. Saccadic peak velocity is sensitive to variations in mental workload while driving in a virtual environment. Aviat. Space Environ. Med. 2010, 81:413-417.
30. Di Stasi L.L., Renner R., Cañas J.J., Catena A., Velichkovsky B.M., Pannasch S. Towards a driver fatigue test based on the saccadic main sequence: a partial validation by subjective report data. Transport. Res. Part C 2012, 21:122-133.
31. Dodge R. The laws of relative fatigue. Psychol. Rev. 1917, 14:89-113.
32. Dodge R., Benedict F.G., Wells F.L. Psychological Effects of Alcohol: An Experimental Investigation of the Effects of Moderate Doses of ethyl Alcohol on a Related Group of Neuro-muscular Processes in Man 1915, Carnegie Institution of Washington.
33. Dodge R., Cline T.S. The angle velocity of eye movements. Psychol. Rev. 1901, 8:145-157.
34. Edelman J.A., Goldberg M.E. Dependence of saccade-related activity in the primate superior colliculus on visual target presence. J. Neurophysiol. 2001, 86:676-691.
35. Edelman J.A., Valenzuela N., Barton J.J.S. Antisaccade velocity, but not latency, results from a lack of saccade visual guidance. Vision Res. 2006, 46:1411-1421.
36. Fransson P.A., Patel M., Magnusson M., Berg S., Almbladh P., Gomez S. Effects of 24-hour and 36-hour sleep deprivation on smooth pursuit and saccadic eye movements. J. Vestibul. Res. 2008, 18:209-222.
37. Friedl K.E., Grate S.J., Proctor S.P., Ness J.W., Lukey B.L., Kane R.L. Army research needs for automated neuropsychological tests: monitoring soldier health and performance status. Arch Clin. Neuropsychol. 2007, 22(Suppl. 1):7-14.
38. Galley N. Saccadic eye movement velocity as an indicator of deactivation. a review and some speculations. J. Psychophysiol. 1989, 3:229-244.
39. Galley N. The evaluation of the electrooculogram as a psychophysiological measuring instrument in the driver study of driver behaviour. Ergonomics 1993, 36:1063-1070.
40. Galley N. An enquiry into the relationship between activation and performance using saccadic eye movement parameters. Ergonomics 1998, 41:698-720.
41. Galley N., Andrés G. Saccadic eye movements and blinks during long term driving on the autobahn with minimal alcohol ingestion. Vision in Vehicles 1996, 381-388. Elsevier, Amsterdam, Holland. A.G. Gale, I.D. Brown, C.M. Haslegrave, S.P. Taylor (Eds.).
42. Gancarz G., Grossberg S. A neural model of the saccade generator in the reticular formation. Neural Netw. 1998, 11:1159-1174.
43. Garbutt S., Harwood M.R., Kumar A.N., Han Y.H., Leigh R.J. Evaluating small eye movements in patients with saccadic palsies. Ann. N Y Acad. Sci. 2003, 1004:337-346.
44. Gijsman H.J., Van Gerven J.M., Tieleman M.C., Schoemaker R.C., Pieters M.S., Ferrari M.D., Cohen A.F., Van Kempen G.M. Pharmacokinetic and pharmacodynamic profile of oral and intravenous meta-chlorophenylpiperazine in healthy volunteers. J. Clin. Psychopharmacol. 1998, 18:289-295.
45. Gijsman H.J., Van Gerven J.M.A., Verkes R.J., Schoemaker R.C., Pieters M.S.M., Pennings E.J.M., Cohen A.F. Saccadic peak velocity and EEG as end-points for a serotonergic challenge test. Hum. Psychopharmacol. 2002, 17:83-89.
46. Girard B., Berthoz A. From brainstem to cortex: computational models of saccade generation circuitry. Progr. Neurobiol. 2005, 77:215-251.
47. Glue P., White E., Wilson S., Ball D., Nutt D. Pharmacology of saccadic eye movements in man, 2. white effects of the alpha-2-adrenoceptor ligands idaxozan and clonidine. Psychopharmacology pharmacology of saccadic eye movements in man. 2. Effects of the a 2-adrenoceptor ligands clonidine and idaxozan. Psychopharmacology 1991, 105:368-373.
48. Gooding D.C., Basso M.A. The tell-tale tasks: a review of saccadic research in psychiatric patient populations. Brain Cognition 2008, 68:371-390.
49. Grace P.M., Stanford T., Gentgall M., Rolan P.E. Utility of saccadic eye movement analysis as an objective biomarker to detect the sedative interaction between opioids and sleep deprivation in opioid-naïve and opioid-tolerant populations. J. Psychopharmacol. 2010, 24:1631-1640.
50. Graupner S.T., Velichkovsky B.M., Pannasch S., Marx J. Surprise, surprise: two distinct components in the visually evoked distractor effect. Psychophysiology 2007, 44:251-261.
51. Grossberg S., Kuperstein M. Neural Dynamics of Adaptive Sensory-Motor Control 1986, Ballistic eye movements, North Holland.
52. Harwood M.R., Mezey L.E., Harris C.M. The spectral main sequence of human saccades. J. Neurosci. 1999, 19:9098-9106.
53. Henn V., Baloh R.W., Hepp K. The sleep-wake transition in the oculomotor system. Exp. Brain Res. 1984, 54:166-176.
54. Hirvonen K., Puttonen S., Gould K., Korpela J., Koefoed V.F., Müller K. Improving the saccade peak velocity measurement for detecting fatigue. J. Neurosci. Methods 2010, 187:199-206.
55. Hoar R.M. Embryology of the eye. Environ Health Perspective 1982, 44:31-34.
56. Hoddes E., Zarcone V., Smythe H., Phillips R., Dement W.C. Quantification of sleepiness: a new approach. Psychophysiology 1973, 10:431-436.
57. Jou Y.-T., Yenn T.-C., Lin C.-J., Yang C.-W., Chiang C.-C. Evaluation of operators' mental workload of human-system interface automation in the advanced nuclear power plants. Nucl. Eng. Design 2009, 239:2537-2542.
58. ISI-PADAS. [Integrated Simulation - Partially Autonomous Driver Assistance Systems], 2012. ISI-PADAS Project [Official web], June. Retrieved from . http://www.isi-padas.eu/.
59. ITERATE. [(IT for Error Remediation And Trapping Emergencies], 2012. ITERATE Project [Official web], June. Retrieved from . http://www.iterate-project.eu/.
60. Iwamoto Y., Kaku Y. Saccade adaptation as a model of learning in voluntary movements. Exp. Brain Res. 2010, 204:145-162.
61. Kaber D.B., Perry C.M., Segall N., McClernon C.K., Prinzel L.J. Situation awareness implications of adaptive automation for information processing in an air traffic control-related task. Int. J. Ind. Ergonom. 2006, 36:447-462.
62. Kaneko C.R. Effect of ibotenic acid lesions of the omnipause neurons on saccadic eye movements in rhesus macaques. J. Neurophysiol. 1996, 75:2229-2242.
63. Le Duc P.A., Greig J.L., Dumond S.L. Involuntary eye responses as measures of fatigue in U.S, Army Apache aviators. Aviat. Space Environ. Med. 2005, 76:86-92.
64. Leigh R.J., Zee D.S. The Neurology of Eye Movements 1999, Oxford University Press, New York, NY. third ed.
65. Lin H.-H., Chen Y.-F., Chen T., Tsai T.-T. Temporal analysis of the acceleration and deceleration phases for visual saccades. Biomed. Eng. Appl. Basis Commun. 2004, 16:355-362.
66. Martinez-Conde S., Otero-Millan J., Macknik S.L. The impact of microsaccades on vision: towards a unified theory of saccadic function. Nat. Rev. Neurosci. 2013, 14:83-96.
67. McCamy M.B., Macknik S.L., Martinez-Conde S. Natural eye movements and vision. The New Visual Neurosciences 2014, 849-863. MIT Press, Cambridge, MA, USA. J. Werner, L. Chalupa (Eds.).
68. Malhi G.S., Parker G.B., Greenwood J. Structural and functional models of depression: from sub-types to substrates. Acta Psychiat. Scand. 2005, 111:94-105.
69. Martinez-Conde S., Macknik S.L., Troncoso X.G., Hubel D.H. Microsaccades: a neurophysiological analysis. Trends Neurosci. 2009, 32:463-475.
70. Miles W.R. Horizontal eye movements at the onset of sleep. Psychol. Rev. 1929, 36:122-141.
71. Miura K., Optican L. Membrane channel properties of premotor excitatory burst neurons may underlie saccade slowing after lesions of omnipause neurons. J. Comput. Neurosci. 2006, 20:25-41.
72. Morad Y., Barkana Y., Zadok D., Hartstein M., Pras E., Bar-Dayan Y. Ocular parameters as an objective tool for the assessment of truck drivers fatigue. Accid. Anal. Prev. 2009, 41:856-860.
73. Moschovakis A.K. Neural network simulations of the primate oculomotor system. Biol. Cybern. 1994, 70:291-302.
74. Munoz D.P., Everling S. Look away: the anti-saccade task and the voluntary control of eye movement. Nat. Rev. Neurosci. 2004, 5:218-228.
75. Oken B.S., Salinsky M.C., Elsas S.M. Vigilance, alertness, or sustained attention: physiological basis and measurement. Clin. Neurophysiol. 2006, 117:1885-1901.
76. Omodei M.Y., Wearing A. The Firechief Microworld generating program: an illustration of computer simulated microworld as an experimental paradigm for studying complex decision-making behaviour. Behav. Res. Method. Instrum. Comput. 1995, 27:303-316.
77. Otero-Millan J., Troncoso X.G., Macknik S.L., Serrano-Pedraza I., Martinez-Conde S. Saccades and microsaccades during visual fixation, exploration and search: foundations for a common saccadic generator. J. Vision 2008, 8:1-18.
78. Pannasch S., Helmert J.R., Roth K., Herbold A.K., Walter H. Visual fixation durations and saccadic amplitudes: shifting relationship in a variety of conditions. J. Eye Movement Res. 2008, 2:1-19.
79. Parasuraman R., Rizzo M. Neuroergonomics: The Brain at Work 2007, Oxford University Press, New York, NY.
80. Pastukhov A., Braun J. Rare but precious: microsaccades are highly informative about attentional allocation. Vision Res. 2010, 50:1173-1184.
81. Piao J., McDonald M. Advanced driver assistance systems from autonomous to cooperative approach. Trans. Rev. 2008, 28:659-684.
82. Porcu S., Ferrara M., Urbani L., Bellatreccia A., Casagrande M. Smooth pursuit and saccadic eye movements as possible indicators of nighttime sleepiness. Physiol. Behav. 1998, 65:437-443.
83. Prsa M., Dicke P.W., Thier P. The absence of eye muscle fatigue indicates that the nervous system compensates for non-motor disturbances of oculomotor function. J. Neurosci. 2010, 30:15834-15842.
84. Rahafrooz A., Fallah A., Jafari A.H., Bakouie F., Zendehrouh S., Gharibzadeh S. Saccadic and smooth pursuit eye movements: computational modeling of a common inhibitory mechanism in brainstem. Neurosci. Lett. 2008, 448:84-89.
85. Rolfs M. Microsaccades: small steps on a long way. Vision Res. 2009, 49:2415-2441.
86. Rowland L.M., Thomas M.L., Thorne D.R., Sing H.C., Krichmar J.L., Davis H.Q., Belenky G. Oculomotor responses during partial and total sleep deprivation. Aviat. Space Environ. Med. 2005, 76:104-113.
87. Russo M., Thomas M., Thorne D., Sing H., Redmond D., Rowland L., et al. Oculomotor impairment during chronic partial sleep deprivation. Clin. Neurophysiol. 2003, 114:723-736.
88. Schleicher R., Galley N., Briest S., Galley L. Blinks and saccades as indicators of fatigue in sleepiness warnings: looking tired?. Ergonomics 2008, 51:982-1010.
89. Schmidt D., Abel L.A., Dell'Osso F., Daroff R.B. Saccadic velocity characteristics: intrinsic variability and fatigue. Aviat. Space Environ. Med. 1979, 50:393-395.
90. Snyder L.H., Calton J.L., Dickinson A.R., Lawrence B.M. Eye-hand coordination: saccades are faster when accompanied by a coordinated arm movement. J. Neurophysiol. 2002, 87:2279-2286.
91. Soetedjo R., Kaneko C.R.S., Fuchs A.F. Evidence that the superior colliculus participates in the feedback control of saccadic eye movements. J. Neurophysiol. 2002, 87:679-695.
92. Sparks D.L. The brainstem control of saccadic eye movements. Nat. Rev. Neurosci. 2002, 3:952-964.
93. Straube A., Robinson F.R., Fuchs A.F. Decrease in saccadic performance after many visually guided saccadic eye movements in monkeys. Invest. Ophthalmol. Vis. Sci. 1997, 38:2810-2816.
94. Stewart S.A. The effects of benzodiazepines on cognition. J. Clin. Psychiat. 2005, 66:9-13.
95. Takagi M., Abe H., Hasegawa S., Yoshizawa T., Usui T. Velocity profile of human horizontal saccades. Ophthalmologica 1993, 206:169-176.
96. Takikawa Y., Kawagoe R., Hikosaka O. Reward-dependent spatial selectivity of anticipatory activity in monkey caudate neurons. J. Neurophysiol. 2002, 87:508-515.
97. Tennison M.N., Moreno J.D. Neuroscience, ethics, and national security: the state of the art. PLoS Biol. 2012, 10:e1001289.
98. Thomas M.I., Russo M.B. Neurocognitive monitors: toward the prevention of cognitive performance decrements and catastrophic failures in the operational environment. Aviat. Space Environ. Med. 2007, 78:144-152.
99. Unema P., Pannasch S., Joos M., Velichkovsky B.M. Time-course of information processing during scene perception: the relationship between saccade amplitude and fixation duration. Vis. Cognition 2005, 12:473-494.
100. Wang L. Glissadic saccades: a possible measure of vigilance. Ergonomics 1998, 41:721-732.
101. Wiese E.E., Lee J.D. Effects of multiple auditory alerts for in-vehicle information systems on driver attitudes and performance. Ergonomics 2004, 9:965-986.
102. Wilson G.F., O'Donnell R.D. Measurement of operator workload with the neuropsychological workload test battery. Human Mental Workload 1988, 63-100. Elsevier, Amsterdam, Holland. P.A. Hancock, N. Meshkati (Eds.).
103. Winograd-Gurvich C., Georgiou-Karistianis N., Fitzgerald P.B., Millist L., White O.B. Ocular motor differences between melancholic and non-melancholic depression. J. Affect. Dis. 2006, 93:193-203.
104. Yoshikazu S., Sugiuchi Y., Takahashi M., Izawa Y. Neural substrate for suppression of omnipause neurons at the onset of saccades. Ann. N Y Acad. Sci. 2011, 1233:100-106.
105. Zils E., Sprenger A., Heide W., Born J., Gais S. Differential effects of sleep deprivation on saccadic eye movements. Sleep 2005, 28:1109-1115.
106. Zuber B.L., Stark L., Cook G. Microsaccades and the velocity-amplitude relationship for saccadic eye movements. Science 1965, 150:1459-1460.