Directional asymmetries in human smooth pursuit eye movements

Investigative Ophthalmology and Visual Science

Volumn 54, Issue 6, 2013, Pages 4409-4421

  Ke, Sally R ^a   Lam, Jessica ^a   Pai, Dinesh K ^a,b   Spering, Miriam ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Asymmetry; Catch up saccades; Directional anisotropies; Smooth pursuit; Visual field

Indexed keywords

ADULT; ANISOTROPY; ARTICLE; CEREBELLUM; CONTROLLED STUDY; DIRECTIONAL VISION; FEMALE; FRONTAL CORTEX; HISTOGRAM; HUMAN; HUMAN EXPERIMENT; MALE; MOTION; NORMAL HUMAN; OCULOGRAPHY; OPTOKINETIC NYSTAGMUS; PRIORITY JOURNAL; SACCADIC EYE MOVEMENT; SMOOTH PURSUIT EYE MOVEMENT; VELOCITY; VISUAL ACUITY; VISUAL STIMULATION;

ASYMMETRY; CATCH-UP SACCADES; DIRECTIONAL ANISOTROPIES; SMOOTH PURSUIT; VISUAL FIELD;

ACCELERATION; ADULT; FEMALE; HUMANS; MALE; MOTION PERCEPTION; PURSUIT, SMOOTH; SACCADES; VISION, BINOCULAR; VISUAL FIELDS; YOUNG ADULT;

EID: 84879578460     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.12-11369     Document Type: Article

References (85)

1. Methling D, Wernicke J. Visual acuity in horizontal tracking movements of the eye. Vision Res. 1968;8:555-565.
2. Brown B. Dynamic visual acuity, eye movements and peripheral acuity for moving targets. Vision Res. 1972;12: 305-321.
3. Westheimer G, McKee SP. Visual acuity in the presence of retinal-image motion. J Opt Soc Am. 1975;65:847-850.
4. Schütz AC, Braun DI, Gegenfurtner KR. Object recognition during foveating eye movements. Vision Res. 2009;49:2241-2253.
5. Schütz AC, Braun DI, Kerzel D, Gegenfurtner KR. Improved visual sensitivity during smooth pursuit eye movements. Nat Neurosci. 2008;11:1211-1216.
6. Hafed ZM, Krauzlis RJ. Ongoing eye movements constrain visual perception. Nat Neurosci. 2006;9:1449-1457.
7. Spering M, Schütz AC, Braun D, Gegenfurtner KR. Keep your eyes on the ball: smooth pursuit eye movements enhance prediction of visual motion. J Neurophysiol. 2011;105:1756-1767.
8. Ball K, Sekuler R. Models of stimulus uncertainty in motion perception. Psychol Rev. 1980;87:435-469.
9. Churchland AK, Gardner JL, Chou I, Priebe NJ, Lisberger SG. Directional anisotropies reveal a functional segregation of visual motion processing for perception and action. Neuron. 2003;37:1001-1011.
10. Dakin SC, Apthorp D, Alais D. Anisotropies in judging the direction of moving natural scenes. J Vis. 2010;10:1-19.
11. Gros BL, Blake R, Hiris E. Anisotropies in visual motion perception: a fresh look. J Opt Soc Am A. 1998;15:2003-2011.
12. Krukowski AE, Stone LS. Expansion of direction space around the cardinal axes revealed by smooth pursuit eye movements. Neuron. 2005;45:315-323.
13. Rottach KG, Zivotofsky AZ, Das VE, et al. Comparison of horizontal, vertical and diagonal smooth pursuit eye movements in normal human subjects. Vision Res. 1996;36:2189-2195.
14. Baloh RW, Yee RD, Honrubia V, Jacobson K. A comparison of the dynamics of horizontal and vertical smooth pursuit in normal human subjects. Aviat Space Environ Med. 1988;59: 121-124.
15. Collewijn H, Tamminga EP. Human smooth and saccadic eye movements during voluntary pursuit of different target motions on different backgrounds. J Physiol. 1984;351:217-250.
16. Evinger C, Fuchs AF. Saccadic, smooth pursuit, and optokinetic eye movements of the trained cat. J Physiol. 1978;285:209-229.
17. Grant MP, Leigh RJ, Seidman SH, Riley DE, Hanna JP. Comparison of predictable smooth ocular and combined eye-head tracking behaviour in patients with lesions affecting the brainstem and cerebellum. Brain. 1992;115:1323-1342.
18. Kettner RE, Leung HC, Peterson BW. Predictive smooth pursuit of complex two-dimensional trajectories in monkey: component interactions. Exp Brain Res. 1996;108:221-235.
19. Leung HC, Kettner RE. Predictive smooth pursuit of complex two-dimensional trajectories demonstrated by perturbation responses in monkeys. Vision Res. 1997;37:1347-1354.
20. Grönqvist H, Gredebäck G, Hofsten C. Developmental asymmetries between horizontal and vertical tracking. Vision Res. 2006;46:1754-1761.
21. Takeichi N, Fukushima J, Kurkin S, Yamanobe T, Shinmei Y, Fukushima K. Directional asymmetry in smooth ocular tracking in the presence of visual background in young and adult primates. Exp Brain Res. 2003;149:380-390.
22. Akao T, Kumakura Y, Kurkin S, Fukushima J, Fukushima K. Directional asymmetry in vertical smooth-pursuit and cancellation of the vertical vestibulo-ocular reflex in juvenile monkeys. Exp Brain Res. 2007;182:469-478.
23. Kasahara S, Akao T, Fukushima J, Kurkin S, Fukushima K. Further evidence for selective difficulty of upward eye pursuit in juvenile monkeys: effects of optokinetic stimulation, static roll tilt, and active head movements. Exp Brain Res. 2006;171: 306-321.
24. Kurkin S, Akao T, Fukushima J, Fukushima K. Discharge of pursuit-related neurons in the caudal part of the frontal eye fields in juvenile monkeys with up-down pursuit asymmetry. Exp Brain Res. 2009;193:181-188.
25. Grasse KL, Lisberger SG. Analysis of a naturally occurring asymmetry in vertical smooth pursuit eye movements in a monkey. J Neurophysiol. 1992;67:164-179.
26. Marti S, Bockisch CJ, Straumann D. Prolonged asymmetric smooth-pursuit stimulation leads to downbeat nystagmus in healthy human subjects. Invest Ophthalmol Vis Sci. 2005;46: 143-149.
27. Tychsen L, Lisberger SG. Visual motion processing for the initiation of smooth-pursuit eye movements in humans. J Neurophysiol. 1986;56:953-968.
28. Mateeff S, Hohnsbein J. Perceptual latencies are shorter for motion towards the fovea than for motion away. Vision Res. 1988;28:711-719.
29. Edwards M, Badcock DR. Asymmetries in the sensitivity to motion in depth: a centripetal bias. Perception. 1993;22:1013-1023.
30. Raymond JE. Directional anisotropy of motion sensitivity across the visual field. Vision Res. 1994;34:1029-1037.
31. Dumoulin SO, Baker CL, Hess RF. Centrifugal bias for secondorder but not first-order motion. J Opt Soc Am. 2001;18:2179-2189.
32. Ball K, Sekuler R. Human vision favors centrifugal motion. Perception. 1980;9:317-325.
33. Miles WR. Ocular dominance in human adults. J Gen Psychol. 1930;3:412-429.
34. Oldfield RC. The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia. 1971;9:97-113.
35. Rashbass C. The relationship between saccadic and smooth tracking eye movements. J Physiol. 1961;159:326-338.
36. Lisberger SG, Westbrook LE. Properties of visual inputs that initiate horizontal smooth pursuit eye movements in monkeys. J Neurosci. 1985;5:1662-1673.
37. Lisberger SG. Visual guidance of smooth pursuit eye movements: sensation, action, and what happens in between. Neuron. 2010;66:477-491.
38. De Brouwer S, Yuksel D, Blohm G, Missal M, Lefèvre P. What triggers catch-up saccades during visual tracking? J Neurophysiol. 2002;87:1646-1650.
39. Haegerstrom-Portnoy G, Brown, B. Contrast effects on smoothpursuit eye movement velocity. Vision Res. 1979;19:169-174.
40. Clark RA, Isenberg SJ. The range of ocular movements decreases with aging. J AAPOS. 2001;5:26-30.
41. Clark RA, Demer JL. Effect of aging on human rectus extraocular muscle paths demonstrated by magnetic resonance imaging. Am J Ophthalmol. 2002;134:872-878.
42. Matthews N, Qian N. Axis-of-motion affects direction discrimination, not speed discrimination. Vision Res. 1999;39:2205-2211.
43. Calderone JB, Kaiser MK. Visual acceleration detection: effect of sign and motion orientation. Percept Psychophys. 1989;45: 391-394.
44. Moscatelli A, Lacquaniti F. The weight of time: gravitational force enhances discrimination of visual motion duration. J Vis. 2011;11:1-17.
45. Benson AJ, Guedry FE. Comparison of tracking task performance and nystagmus during sinusoidal oscillation in yaw and pitch. Aerosp Med. 1971;42:593-601.
46. Garbutt S, Han Y, Kumar AN, Harwood M, Harris CM, Leigh RJ. Vertical optokinetic nystagmus and saccades in normal human subjects. Invest Ophthalmol Vis Sci. 2003;44:3833-3841.
47. Murasugi M, Howard IP. Up-down asymmetry in human vertical optokinetic nystagmus and afternystagmus: contributions of the central and peripheral retinae. Exp Brain Res. 1989;77:183-192.
48. Ogino S, Kato I, Sakuma A, Takahashi K, Takeyama I. Vertical optokinetic nystagmus in normal individuals. Acta Otolaryngol. 1996;522:38-42.
49. Takahashi M, Sakurai S, Kanzaki J. Horizontal and vertical optokinetic nystagmus in man. ORL J Otorhinolaryngol Relat Spec. 1978;40:43-52.
50. van den Berg AV, Collewijn H. Directional asymmetries of human optokinetic nystagmus. Exp Brain Res. 1988;70:597-604.
51. Matsuo V, Cohen B. Vertical optokinetic nystagmus and vestibular nystagmus in the monkey: up-down asymmetry and effects of gravity. Exp Brain Res. 1984;53:197-216.
52. Takahashi M, Igarashi M. Comparison of vertical and horizontal optokinetic nystagmus in the squirrel monkey. ORL J Otorhinolaryngol Relat Spec. 1977;39:321-329.
53. Darlot C, López-Barneo J, Tracey D. Asymmetries of vertical vestibular nystagmus in the cat. Exp Brain Res. 1981;41:420-426.
54. Wallman J, Velez J. Directional asymmetries of optokinetic nystagmus: developmental changes and relation to the accessory optic system and to the vestibular system. J Neurosci. 1985;5:317-329.
55. Knapp CM, Gottlob I, McLean RJ, Proudlock FA. Horizontal and vertical look and stare optokinetic nystagmus symmetry in healthy adult volunteers. Invest Ophthalmol Vis Sci. 2008;49: 581-588.
56. Knapp CM, Gottlob I, McLean RJ, Rafelt S, Proudlock FA. Effect of distance upon horizontal and vertical look and stare OKN. J Vis. 2009;9:1-9.
57. Keller EL, Heinen SJ. Generation of smooth-pursuit eye movements: neuronal mechanisms and pathways. Neurosci Res. 1991;11:79-107.
58. Simoncelli EP, Olshausen BA. Natural image statistics and neural representation. Ann Rev Neurosci. 2001;24:1193-1216.
59. Senot P, Zago M, Lacquaniti F, McIntyre J. Anticipating the effects of gravity when intercepting moving objects: differentiating up and down based on nonvisual cues. J Neurophysiol. 2005;94:4471-4480.
60. Amenedo E, Pazo-Alvarez P, Cadaveira F. Vertical asymmetries in pre-attentive detection of changes in motion direction. Int J Psychophysiol. 2007;64:184-189.
61. Lakha L, Humphreys G. Lower visual field advantage for motion segmentation during high competition for selection. Spat Vis. 2005;18:447-460.
62. Regan D, Erkelens CJ, Collewijn H. Visual field defects for vergence eye movements and for stereomotion perception. Invest Ophthalmol Vis Sci. 1986;27:806-819.
63. Danckert J, Goodale MA. Superior performance for visually guided pointing in the lower visual field. Exp Brain Res. 2001; 137:303-308.
64. Khan MA, Lawrence GP. Differences in visuomotor control between the upper and lower visual fields. Exp Brain Res. 2005;164:395-398.
65. Krigolson O, Heath M. A lower visual field advantage for endpoint stability but no advantage for online movement precision. Exp Brain Res. 2006;170:127-135.
66. Binsted G, Heath M. No evidence of a lower visual field specialization for visuomotor control. Exp Brain Res. 2005; 162:89-94.
67. Brownell K, Rolheiser T, Heath M, Binsted G. Does perception asymmetrically influence motor production in upper and lower visual fields? Motor Control. 2010;14:44-58.
68. Krauzlis RJ. Recasting the smooth pursuit eye movement system. J Neurophysiol. 2004;91:591-603.
69. Leigh RJ, Zee DS. The Neurology of Eye Movements. 4th ed. New York, NY: Oxford University Press; 2006.
70. Maunsell JHR, Van Essen DC. Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. J Neurophysiol. 1983;19:1127-1147.
71. Giaschi, D, Zwicker A, Young SA, Bjornson B. The role of cortical area V5/MT{thorn}in speedtuned directional anisotropies in global motion perception. Vision Res. 2007;47:887-898.
72. Kheradmand A, Zee DS. Cerebellum and ocular motor control. Front Neurol. 2011;2:1-15.
73. Fukushima K, Fukushima J, Kaneko CRS, Fuchs AF. Vertical Purkinje cells of the monkey floccular lobe: simple spike activity during pursuit and passive whole body rotation. J Neurophysiol. 1999;82:787-803.
74. Krauzlis RJ, Lisberger SG. Directional organization of eye movement and visual signals in the floccular lobe of the monkey cerebellum. Exp Brain Res. 1996;109:289-302.
75. Stone LS, Lisberger SG. Visual responses of Purkinje cells in the cerebellar flocculus during smooth-pursuit eye movements in monkeys. I. Simple spikes. J Neurophysiol. 1990;63:1241-1261.
76. Glasauer S, Stephan T, Kalla R, Marti S, Straumann D. Up-down asymmetry of cerebellar activation during vertical pursuit eye movements. Cerebellum. 2009;8:385-388.
77. Marti S, Straumann D, Glasauer S. The origin of downbeat nystagmus: an asymmetry in the distribution of on-directions of vertical gaze-velocity Purkinje cells. Ann N Y Acad Sci. 2005;1039:548-553.
78. Zee DS, Yamazaki A, Butler PH, Gucer G. Effects of ablation of flocculus and paraflocculus on eye movements in primate. J Neurophysiol. 1981;46:878-899.
79. Walker MF, Tian J, Shan X, Tamargo RJ, Ying H, Zee DS. Lesions of the cerebellar nodulus and uvula impair downward pursuit. J Neurophysiol. 2008;100:1813-1823.
80. Fukushima K. Frontal cortical control of smooth-pursuit. Curr Opin Neurobiol. 2003;13:647-654.
81. Krauzlis RJ, Lisberger SG. Simple spike responses of gaze velocity Purkinje cells in the floccular lobe of the monkey during onset and offset of pursuit eye movements. J Neurophysiol. 1994;72:2045-2050.
82. Zhang Y, Partsalis AM, Highstein SM. Properties of superior vestibular nucleus flocculus target neurons in the squirrel monkey. I. General properties in comparison with flocculus projecting neurons. J Neurophysiol. 1995;73:2261-2278.
83. Spering M, Schütz AC, Braun DI, Gegenfurtner KR. Keep your eyes on the ball: smooth pursuit eye movements enhance prediction of visual motion. J Neurophysiol. 2011;105:1756-1767.
84. Mustari MJ, Ono S. Neural mechanisms for smooth pursuit in strabismus. Ann N Y Acad Sci. 2011;1233:187-193.
85. Tychsen L, Lisberger SG. Maldevelopment of visual motion processing in humans who had strabismus with onset in infancy. J Neurosci. 1986;6:2495-2508.