Simultaneous recordings of ocular microtremor and microsaccades with a piezoelectric sensor and a video-oculography system

PeerJ

Volumn 2013, Issue 1, 2013, Pages

  McCamy, Michael B ^a,b   Collins, Niamh ^c   Otero Millan, Jorge ^a,d   Al Kalbani, Mohammed ^c   Macknik, Stephen L ^a   Coakley, Davis ^c,e   Troncoso, Xoana G ^a,f   Boyle, Gerard ^e   Narayanan, Vinodh ^a   Wolf, Thomas R ^a,g   Martinez Conde, Susana ^a  

^a BARROW NEUROLOGICAL INSTITUTE   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

^c TRINITY COLLEGE DUBLIN   (Ireland)

^d UNIVERSITY OF VIGO   (Spain)

^e ST JAMES S HOSPITAL   (Ireland)

^f Unite de Neurosciences Integratives et Computationnelles   (France)

^g Neuro Ophthalmology Consultation: Barnett Dulaney Perkins Eye Center   (United States)

Author keywords

Fading; Fixational eye movements; Neural adaptation; Saccadic adaptation; Tremor

Indexed keywords

ALGORITHM; ARTICLE; EYE POSITION; EYELID REFLEX; FEMALE; HUMAN; HUMAN EXPERIMENT; LUMINANCE; MAGNITUDE ESTIMATION METHOD; MALE; MONOCULAR VISION; NORMAL HUMAN; OCULOMOTOR SYSTEM; PERCEPTIVE THRESHOLD; PHOTORECEPTOR; PIEZOELECTRICITY; SACCADIC EYE MOVEMENT; SENSORY STIMULATION; TREMOR; VIDEOOCULOGRAPHY;

EID: 84877139378     PISSN: None     EISSN: 21678359     Source Type: Journal    
DOI: 10.7717/peerj.14     Document Type: Article

References (66)

1. Albano JE, Arzola Marrero J. 1995. Binocular interactions in rapid saccadic adaptation. Vision Research 35(23-24):3439-3450 DOI 10.1016/0042-6989(95)00079-T pa
2. Al-Kalbani M. 2010. Ocular microtremor measurement, characterization & analysis. Ph.D. Trinity College Dublin, Ireland.
3. Al-Kalbani M, Collins N, Boyle G, Foran T, Hegarty F, Sheahan N, Coakley D. 2007. Recovering the Ocular Microtremor Signal using Wavelet Denoising Technique. IEEE International Conference on Signal Processing and Communications, 2007. ICSPC 2007 (pp. 1571-1574). Presented at the IEEE International Conference on Signal Processing and Communications, 2007.
4. Al-Kalbani M, Collins N, Boyle G, Hegarty F, Foran T, Sheahan N, Coakley D. 2007. An automated ocular microtremor feature extraction using the gabor thresholding technique. 29th Annual International Conference of the IEEE Engineering in Medicine and Biology Society, 2007. EMBS 2007 (pp. 2851-2854). Presented at the 29th Annual International Conference of the IEEE Engineering in Medicine and Biology Society, 2007. EMBS 2007, IEEE DOI 10.1109/IEMBS.2007.4352923.
5. Al-Kalbani M,Mihaylova E, Collins N, Coakley D, Boyle G, Toal V. 2009. Ocular microtremor laser speckle metrology. Conference Papers. Retrieved from http://arrow.dit.ie/cieocon2/7.
6. Bahill AT, Ciuffreda KJ, Kenyon R, Stark L. 1976. Dynamic and static violations of Hering's law of equal innervation. American Journal of Optometry and Physiological Optics 53(12):786-796 DOI 10.1097/00006324-197612000-00005.
7. Balslev D, Himmelbach M, Karnath HO, Borchers S, Odoj B. 2012. Eye proprioception used for visual localization only if in conflict with the oculomotor plan. The Journal of Neuroscience 32(25):8569-8573 DOI 10.1523/JNEUROSCI.1488-12.2012.
8. Beer AL, Heckel AH, Greenlee MW. 2008. A motion illusion reveals mechanisms of perceptual stabilization. PLoS ONE 3(7): e2741 DOI 10.1371/journal.pone.0002741.
9. Bengi H, Thomas JG. 1968a. Three electronic methods for recording ocular tremor. Medical & Biological Engineering 6(2):171-179 DOI 10.1007/BF02474271.
10. Bengi H, Thomas JG. 1968b. Fixation tremor in relation to eyeball-muscle mechanics. Nature 217(5130):773-774 DOI 10.1038/217773a0.
11. Betta E, Turatto M. 2006. Are you ready? I can tell by looking at your microsaccades. Neuroreport 17(10): 1001 DOI 10.1097/01.wnr.0000223392.82198.6d.
12. Bojanic S, Simpson T, Bolger C. 2001. Ocular microtremor: a tool for measuring depth of anaesthesia? British Journal of Anaesthesia 86(4):519-522 DOI 10.1093/bja/86.4.519.
13. Bolger C, Bojanic S, Sheahan NF, Coakley D,Malone JF. 1999. Dominant frequency content of ocular microtremor from normal subjects. Vision Research 39(11): 1911-1915 DOI 10.1016/S0042-6989(98)00322-8.
14. Bolger C, Bojanic S, Sheahan N,Malone J, Hutchinson M, Coakley D. 2000. Ocular microtremor (OMT): a new neurophysiological approach to multiple sclerosis. Journal of Neurology, Neurosurgery & Psychiatry 68(5):639-642 DOI 10.1136/jnnp.68.5.639.
15. Boyce PR. 1967. Monocular fixation in human eye movement. Proceedings of the Royal Society of London. Series B. Biological Sciences, 167 (1008):293-315 DOI 10.1098/rspb.1967.0028.
16. Bridgeman B,Macknik SL. 1995. Saccadic suppression relies on luminance information. Psychological Research 58(3):163-168 DOI 10.1007/BF00419631
17. Carpenter RH. 1977. Movements of the eyes. Pion.
18. Coakley D. 1983. Minute eye movement and brain stem function. Boca Raton, FL: CRC press. Retrieved fromhttp://www.getcited.org/pub/102225287.
19. Collewijn H, Kowler E. 2008. The significance of microsaccades for vision and oculomotor control. Journal of Vision 8(14):1-21 DOI 10.1167/8.14.20.
20. Collins T,Wallman J. 2012. The relative importance of retinal error and prediction in saccadic adaptation. Journal of Neurophysiology 107(12):3342-3348 DOI 10.1152/jn.00746.2011.
21. Ditchburn RW, Fender DH,Mayne S. 1959. Vision with controlled movements of the retinal image. The Journal of Physiology 145(1):98-107 DOI 10.1100/2012/956340.
22. Donaldson IML. 2000. The functions of the proprioceptors of the eye muscles. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 355(1404):1685-1754 DOI 10.1098/rstb.2000.0732.
23. Drysdale AE. 1975. The visibility of retinal blood vessels. Vision Research 15(7):813-818 DOI 10.1016/0042-6989(75)90259-X.
24. Engbert R. 2006. Microsaccades: A microcosm for research on oculomotor control, attention, and visual perception. Progress in Brain Research 154:177-192 DOI 10.1016/S0079-6123(06)54009-9.
25. Engbert R, Kliegl R. 2003. Microsaccades uncover the orientation of covert attention. Vision Research 43(9):1035-1045 DOI 10.1016/S0042-6989(03)00084-1.
26. Engbert R, Kliegl R. 2004. Microsaccades keep the eyes' balance during fixation. Psychological Science: A Journal of the American Psychological Society/APS 15(6):431-436 DOI 10.1111/j.0956-7976.2004.00697.x.
27. Engbert R,Mergenthaler K. 2006. Microsaccades are triggered by low retinal image slip. Proceedings of the National Academy of Sciences 103(18):7192-7197 DOI 10.1073/pnas.0509557103.
28. Frens MA, Geest JNV der. 2002. Scleral search coils influence saccade dynamics. Journal of Neurophysiology 88(2):692-698 DOI 10.1152/jn.00457.2001.
29. Funke K, Kerscher NJ, Wörgötter F. 2007. Noise-improved signal detection in cat primary visual cortex via a well-balanced stochastic resonance-like procedure. European Journal of Neuroscience 26(5):1322-1332 DOI 10.1111/j.1460-9568.2007.05735.x.
30. Gauthier GM, Nommay D, Vercher J-L. 1990. Ocular muscle proprioception and visual localization of targets in man. Brain 113(6):1857-1871 DOI 10.1093/brain/113.6.1857.
31. Hafed ZM, Goffart L, Krauzlis RJ. 2009. A neural mechanism for microsaccade generation in the primate superior colliculus. Science 323(5916):940-943 DOI 10.1126/science.1166112.
32. Hennig MH, Kerscher NJ, Funke K,Ẅorg̈otter F. 2002. Stochastic resonance in visual cortical neurons: does the eye-tremor actually improve visual acuity? Neurocomputing 44-46:115-120 DOI 10.1016/S0925-2312(02)00371-5.
33. Hopp JJ, Fuchs AF. 2004. The characteristics and neuronal substrate of saccadic eye movement plasticity. Progress in Neurobiology 72(1):27-53 DOI 10.1016/j.pneurobio.2003.12.002.
34. Laubrock J, Engbert R, Kliegl R. 2005. Microsaccade dynamics during covert attention. Vision Research 45(6):721-730 DOI 10.1016/j.visres.2004.09.029.
35. Luo G, Zhang D. 2012. Wavelet denoising. In: Advances in wavelet theory and their applications in engineering, physics and technology. InTech, 634.
36. Macknik SL, Fisher BD, Bridgeman B. 1991. Flicker distorts visual space constancy. Vision Research 31(12):2057-2064 DOI 10.1016/0042-6989(91)90163-Y.
37. Martinez-Conde S,Macknik SL, Hubel DH. 2004. The role of fixational eye movements in visual perception. Nature Reviews Neuroscience 5(3):229-240 DOI 10.1038/nrn1348.
38. Martinez-Conde S,Macknik SL, Troncoso XG, Dyar TA. 2006. Microsaccades counteract visual fading during fixation. Neuron 49(2):297-305 DOI 10.1016/j.neuron.2005.11.033.
39. Martinez-Conde S,Macknik SL, Troncoso XG, Hubel DH. 2009. Microsaccades: a neurophysiological analysis. Trends in Neurosciences 32(9):463-475 DOI 10.1016/j.tins.2009.05.006.
40. Martinez-Conde S, Otero-Millan J,Macknik SL. 2013. The impact of microsaccades on vision: towards a unified theory of saccadic function. Nature Reviews Neuroscience 14(2):83-96 DOI 10.1038/nrn3405.
41. Matin E. 1974. Saccadic suppression: a review and an analysis. Psychological Bulletin 81(12):899-917 DOI 10.1037/h0037368.
42. McCamy MB,Macknik SL,Martinez-Conde S. (in press). Natural eye movements and vision. In: Werner JS, Chalupa LM, eds. The new visual neurosciences. Cambridge, MA: The MIT Press.
43. McCamy MB, Otero-Millan J,Macknik SL, Yang Y, Troncoso XG, Baer SM, Crook SM et al. 2012. Microsaccadic efficacy and contribution to foveal and peripheral vision. The Journal of Neuroscience 32(27):9194-9204 DOI 10.1523/JNEUROSCI.0515-12.2012.
44. Møller FMøller, Laursen M Laursen, Tygesen J Tygesen, Sjølie et al. 2002. Binocular quantification and characterization of microsaccades. Graefe's Archive for Clinical and Experimental Ophthalmology 240(9):765-770 DOI 10.1007/s00417-002-0519-2.
45. Optican LM, Robinson DA. 1980. Cerebellar-dependent adaptive control of primate saccadic system. Journal of Neurophysiology 44(6):1058-1076 DOI 10.1152/jn.00236.2011.
46. Optican LM, Zee DS, Chu FC. 1985. Adaptive response to ocular muscle weakness in human pursuit and saccadic eye movements. Journal of Neurophysiology 54(1):110-122 DOI 10.1152/jn.00877.2011.
47. Otero-Millan J, Collins N, Al-Kalbani M, Troncoso XG,McCamy MB,Macknik SL, Coakley D et al. 2010. Simultaneous recordings of ocular microtremor and fixational microsaccades with a piezoelectric sensor and a commercial video tracking system. Journal of Vision 10(7): 506 DOI 10.1167/10.7.506.
48. Otero-Millan J, Troncoso XG,Macknik SL, Serrano-Pedraza I,Martinez-Conde S. 2008. Saccades and microsaccades during visual fixation, exploration and search: foundations for a common saccadic generator. Journal of Vision 8:14-21 DOI 10.1167/8.14.21.
49. Ṕelisson D, Alahyane N, Panouill̀eres M, Tilikete C. 2010. Sensorimotor adaptation of saccadic eye movements. Neuroscience & Biobehavioral Reviews 34(8):1103-1120 DOI 10.1016/j.neubiorev.2009.12.010.
50. Riggs LA, Ratliff F, Cornsweet JC, Cornsweet TN. 1953. The disappearance of steadily fixated visual test objects. Journal of the Optical Society of America 43(6):495-500 DOI 10.1364/JOSA.43.000495.
51. Rine RM, Skavenski AA. 1997. Extraretinal eye position signals determine perceived target location when they conflict with visual cues. Vision Research 37(6):775-787 DOI 10.1016/S0042-6989(96)00216-7.
52. Rolfs M. 2009. Microsaccades: small steps on a long way. Vision Research 49(20):2415-2441 DOI 10.1016/j.visres.2009.08.010.
53. Rolfs M, Laubrock J, Kliegl R. 2006. Shortening and prolongation of saccade latencies following microsaccades. Experimental Brain Research 169(3):369-376 DOI 10.1007/s00221-005-0148-1.
54. Ryle JP, Al-Kalbani M, Collins N, Gopinathan U, Boyle G, Coakley D, Sheridan JT. 2009. Compact portable ocular microtremor sensor: design, development and calibration. Journal of Biomedical Optics 14(1): 014021-014021-12 DOI 10.1117/1.3083435.
55. Sharpe CR. 1972. The visibility and fading of thin lines visualized by their controlled movement across the retina. The Journal of Physiology 222(1):113-134 DOI 10.1037/0033-2909.85.2.338.
56. Sheahan NF, Coakley D, Hegarty F, Bolger C,Malone J. 1993. Ocular microtremor measurement system: Design and performance. Medical & Biological Engineering & Computing 31(3):205-212 DOI 10.1007/BF02458038.
57. Snow R, Hore J, Vilis T. 1985. Adaptation of saccadic and vestibulo-ocular systems after extraocular muscle tenectomy. Investigative Ophthalmology & Visual Science 26(7):924-931 DOI 10.1016/0166-2236(83)90026-7.
58. Stark L, Bridgeman B. 1983. Role of corollary discharge in space constancy. Perception & Psychophysics 34(4):371-380 DOI 10.3758/BF03203050.
59. Troncoso XG,Macknik SL,Martinez-Conde S. 2008. Microsaccades counteract perceptual filling-in. Journal of Vision 8(14):1-9 DOI 10.1167/8.14.15.
60. Troncoso XG,Macknik SL, Otero-Millan J,Martinez-Conde S. 2008. Microsaccades drive illusory motion in the Enigma illusion. Proceedings of the National Academy of Sciences 105(41):16033-16038 DOI 10.1073/pnas.0709389105.
61. van Donkelaar P, Gauthier GM. 1996. Changes in saccadic and manual motor control after ocular. Journal of Motor Behavior 28(4): 315 DOI 10.1080/00222895.1996.10544601.
62. Wang J, Pan Y. 2012. Eye proprioception may provide real time eye position information. Neurological Sciences: official journal of the Italian Neurological Society and of the Italian Society of Clinical Neurophysiology 1-6 DOI 10.1007/s10072-012-1172-0.
63. Weir CR. 2006. Proprioception in extraocular muscles. Journal of Neuro-Ophthalmology 26(2):123-127 DOI 10.1097/01.wno.0000223272.86565.74.
64. Weir CR, Knox PC, Dutton GN. 2000. Does extraocular muscle proprioception influence oculomotor control? British Journal of Ophthalmology 84(9):1071-1074 DOI 10.1136/bjo.84.9.1071.
65. Yarbus AL. 1967. Eye movements during fixation on stationary objects, NY: Plenum Press 21, 24-33.
66. Zozor S, Amblard P-O, Duchêne C. 2009. Does eye tremor provide the hyperacuity phenomenon? Journal of Statistical Mechanics: Theory and Experiment 2009(01): P01015 DOI 10.1088/1742-5468/2009/01/P01015.