Alfred Lukyanovich Yarbus (1914–1986) pioneered the study of stabilized retinal images, miniature eye movements, and the cognitive influences that act on visual scanning. Yarbus’s studies of these different topics have remained fundamentally disconnected and independent of each other, however. In this review, we propose that Yarbus’s various research lines are instead deeply and intrinsically interconnected, as are the small eye movements produced during visual fixation and the large-scale scanning patterns associated with visual exploration of objects and scenes. Such apparently disparate viewing behaviors may represent the extremes of a single continuum of oculomotor performance that operates across spatial scales when we search the visual world.
BarlowH. B. (1952) Eye movements during fixation. The Journal of Physiology116: 290–306.
2.
BarlowH. B. (1963) Slippage of contact lenses and other artifacts in relation to fading and regeneration of supposedly stable retinal images. The Quarterly Journal of Experimental Psychology15: 36–51.
3.
BenedettoS.PedrottiM.BridgemanB. (2011) Microsaccades and exploratory saccdes in a naturalistic environment. Journal of Eye Movement Research4: 1–10.
4.
BrienD. C.CorneilB. D.FecteauJ. H.BellA. H.MunozP. M. (2009) The behavioural and neurophysiological modulation of microsaccades in monkeys. Journal of Eye Movement Research3: 1–12.
5.
CoppolaD.PurvesD. (1996) The extraordinarily rapid disappearance of entoptic images. Proceedings of the National Academy of Sciences of the United States of America93: 8001–8004.
6.
Di StasiL. L.McCamyM. B.CatenaA.MacknikS. L.CañasJ. J.Martinez-CondeS. (2013) Microsaccade and drift dynamics reflect mental fatigue. European Journal of Neuroscience38: 2389–2398.
7.
Di StasiL. L.McCamyM. B.PannaschS.RennerR.CatenaA.CañasJ. J.Martinez-CondeS. (2015) Effects of driving time on microsaccadic dynamics. Experimental Brain Research233: 599–605.
8.
DitchburnR. W.FenderD. H.MayneS. (1959) Vision with controlled movements of the retinal image. The Journal of Physiology145: 98–107.
9.
DitchburnR. W.GinsborgB. L. (1952) Vision with a stabilized retinal image. Nature170: 36–37.
10.
DitchburnR. W.GinsborgB. L. (1953) Involuntary eye movements during fixation. The Journal of Physiology119: 1–17.
11.
DodgeR. (1907) An experimental study of visual fixation. Psychological Monographs: General and Applied8: 1–95.
12.
DrysdaleA. E. (1975) The visibility of retinal blood vessels. Vision Research15: 813–818.
13.
Fabre-ThorpeM.DelormeA.MarlotC.ThorpeS. (2001) A limit to the speed of processing in ultra-rapid visual categorization of novel natural scenes. Journal of Cognitive Neuroscience13: 171–180.
14.
GawneT. J.MartinJ. M. (2000) Activity of primate V1 cortical neurons during blinks. Journal of Neurophysiology84: 2691–2694.
15.
GawneT. J.MartinJ. M. (2002) Responses of primate visual cortical neurons to stimuli presented by flash, saccade, blink, and external darkening. Journal of Neurophysiology88: 2178–2186.
16.
GerritsH. J.VendrikA. J. (1970) Artificial movements of a stabilized image. Vision Research10: 1443–1456.
17.
GilchristI. D.BrownV.FindlayJ. M. (1997) Saccades without eye movements. Nature390: 130–131.
18.
GilchristI. D.BrownV.FindlayJ. M.ClarkeM. P. (1998) Using the eye-movement system to control the head. Proceedings of the Royal Society of London, Series B: Biological Sciences265: 1831–1836.
19.
GoffartL.ChenL. L.SparksD. L. (2004) Deficits in saccades and fixation during muscimol inactivation of the caudal fastigial nucleus in the rhesus monkey. Journal of Neurophysiology92: 3351–3367.
20.
GowenE.AbadiR. V.PoliakoffE.HansenP. C.MiallR. C. (2007) Modulation of saccadic intrusions by exogenous and endogenous attention. Brain Research1141: 154–167.
21.
GuerrasioL.QuinetJ.ButtnerU.GoffartL. (2010) Fastigial oculomotor region and the control of foveation during fixation. Journal of Neurophysiology103: 1988–2001.
22.
HafedZ. M.GoffartL.KrauzlisR. (2009) A neural mechanism for microsaccade generation in the primate superior colliculus. Science323: 940–943.
23.
Helmholtz, H. (1985). Helmholtz's treatise on physiological optics (J. P. C. Southall, Trans. Translated from 3rd German ed. Vol. 2). Birmingham, Alabama: Gryphon Editions, Ltd.
24.
JurinJ. (1738) An essay on distinct and indistinct vision. In: SmithR. (ed.) A compleat system of opticks in four books, Cambridge: Published by the author, pp. 115–171.
25.
Kitaoka, A. (2002). Trick eyes graphics: Kanzen, Tokyo.
26.
KrauskopfJ. (1957) Effect of retinal image motion on contrast thresholds for maintained vision. Journal of the Optical Society of America47: 740–744.
27.
KrauskopfJ.CornsweetT. N.RiggsL. A. (1960) Analysis of eye movements during monocular and binocular fixation. Journal of the Optical Society of America50: 572–578.
28.
LandM. F.FurneauxS. M.GilchristI. D. (2002) The organization of visually mediated actions in a subject without eye movements. Neurocase8: 80–87.
29.
LordM. P. (1951) Measurement of binocular eye movements of subjects in the sitting position. British Journal of Ophthalmology35: 21–30.
30.
MacknikS. L.LivingstoneM. S. (1998) Neuronal correlates of visibility and invisibility in the primate visual system. Nature Neuroscience1: 144–149.
31.
MacknikS. L.Martinez-CondeS. (2004) The spatial and temporal effects of lateral inhibitory networks and their relevance to the visibility of spatiotemporal edges. Neurocomputing58–60: 775–782.
32.
MacknikS. L.Martinez-CondeS.HaglundM. M. (2000) The role of spatiotemporal edges in visibility and visual masking. Proceedings of the National Academy of Sciences of the United States of America97: 7556–7560.
33.
MalinovI. V.EpelboimJ.HerstA. N.SteinmanR. M. (2000) Characteristics of saccades and vergence in two types of sequential looking tasks. Vision Research40: 2083–2090.
34.
Martinez-CondeS. (2006) Fixational eye movements in normal and pathological vision. Progress in Brain Research154: 151–176.
35.
Martinez-CondeS.MacknikS. L.HubelD. H. (2000) Microsaccadic eye movements and firing of single cells in the striate cortex of macaque monkeys. Nature Neuroscience3: 251–258.
36.
Martinez-CondeS.MacknikS. L.HubelD. H. (2002) The function of bursts of spikes during visual fixation in the awake primate lateral geniculate nucleus and primary visual cortex. Proceedings of the National Academy of Sciences of the United States of America99: 13920–13925.
37.
Martinez-CondeS.MacknikS. L.HubelD. H. (2004) The role of fixational eye movements in visual perception. Nature Reviews Neuroscience5: 229–240.
38.
Martinez-CondeS.MacknikS. L.TroncosoX.DyarT. A. (2006) Microsaccades counteract visual fading during fixation. Neuron49: 297–305.
39.
Martinez-Conde, S., Macknik, S. L., Troncoso, X. G., & Hubel, D. H. (2009). Microsaccades: A neurophysiological analysis. Trends in Neurosciences, 32, 463–475.
40.
Martinez-CondeS.Otero-MillanJ.MacknikS. L. (2013) The impact of microsaccades on vision: Towards a unified theory of saccadic function. Nature Reviews Neuroscience14: 83–96.
41.
McCamy, M. B., Macknik, S. L., & Martinez-Conde, S. (2013). Natural eye movements and vision. In J. S. Werner & L. M. Chalupa (Eds.), The new visual neurosciences (pp. 849–863). Cambridge, MA: The MIT Press.
42.
McCamyM. B.MacknikS. L.Martinez-CondeS. (2014) Different fixational eye movements mediate the prevention and the reversal of visual fading. The Journal of Physiology592: 4381–4394.
43.
McCamyM. B.Otero-MillanJ.MacknikS. L.YangY.TroncosoX. G.BaerS. M.Martinez-CondeS. (2012) Microsaccadic efficacy and contribution to foveal and peripheral vision. Journal of Neuroscience32: 9194–9204.
44.
McCamyM. B.Otero-MillanJ.Di StasiL. L.MacknikS. L.Martinez-CondeS. (2014) Highly informative natural scene regions increase microsaccade production during visual scanning. The Journal of Neuroscience34: 2956–2966.
45.
MunozD. P.WurtzR. H. (1993) Fixation cells in monkey superior colliculus. I. Characteristics of cell discharge. Journal of Neurophysiology70: 559–575.
46.
Otero-MillanJ.MacknikS. L.LangstonR. E.Martinez-CondeS. (2013) An oculomotor continuum from exploration to fixation. Proceedings of the National Academy of Sciences110: 6175–6180.
47.
Otero-MillanJ.MacknikS. L.Martinez-CondeS. (2012) Microsaccades and blinks trigger illusory rotation in the “rotating snakes” illusion. Journal of Neuroscience32: 6043–6051.
48.
Otero-MillanJ.SchneiderR.LeighR. J.MacknikS. L.Martinez-CondeS. (2013) Saccades during attempted fixation in parkinsonian disorders and recessive ataxia: From microsaccades to square-wave jerks. PLoS One8: 1–9.
49.
Otero-MillanJ.SerraA.LeighR. J.TroncosoX. G.MacknikS. L.Martinez-CondeS. (2011) Distinctive features of saccadic intrusions and microsaccades in progressive supranuclear palsy. Journal of Neuroscience31: 4379–4387.
50.
Otero-MillanJ.TroncosoX.MacknikS. L.Serrano-PedrazaI.Martinez-CondeS. (2008) Saccades and microsaccades during visual fixation, exploration and search: Foundations for a common saccadic generator. Journal of Vision8: 21.1–21.18.
51.
PritchardR. M. (1961) Stabilized images on the retina. Scientific American204: 72–78.
52.
RatliffF.RiggsL. A. (1950) Involuntary motions of the eye during monocular fixation. Journal of Experimental Psychology40: 687–701.
53.
RiggsL. A.RatliffF. (1952) The effects of counteracting the normal movements of the eye. Journal of the Optical Society of America42: 872–873.
54.
RobinsonF. R.StraubeA.FuchsA. F. (1993) Role of the caudal fastigial nucleus in saccade generation. II. Effects of muscimol inactivation. Journal of Neurophysiology70: 1741–1758.
55.
RolfsM. (2009) Microsaccades: Small steps on a long way. Vision Research49: 2415–2441.
56.
RolfsM.LaubrockJ.KlieglR. (2006) Shortening and prolongation of saccade latencies following microsaccades. Experimental Brain Research169: 369–376.
57.
RolfsM.LaubrockJ.KlieglR. (2008) Microsaccade-induced prolongation of saccadic latencies depends on microsaccade amplitude. Journal of Eye Movement Research1: 1, 1–8.
58.
SharpeC. R. (1972) The visibility and fading of thin lines visualized by their controlled movement across the retina. Journal of Physiology (London)222: 113–134.
59.
ShelleyM.McLaughlinD.ShapleyR.WielaardJ. (2002) States of high conductance in a large-scale model of the visual cortex. Journal of Computational Neuroscience13: 93–109.
60.
SimonsD. J.FranconeriS. L.ReimerR. L. (2000) Change blindness in the absence of a visual disruption. Perception29: 1143–1154.
61.
TatlerB. W.WadeN. J.KwanH.FindlayJ. M.VelichkovskyB. M. (2010) Yarbus, eye movements, and vision. i-Perception1: 7.
62.
ThorpeS.FizeD.MarlotC. (1996) Speed of processing in the human visual system. Nature381: 520–522.
UchidaN.KepecsA.MainenZ. F. (2006) Seeing at a glance, smelling in a whiff: Rapid forms of perceptual decision making. Nature Reviews Neuroscience7: 485–491.
65.
Van GisbergenJ. A.RobinsonD. A.GielenS. (1981) A quantitative analysis of generation of saccadic eye movements by burst neurons. Journal of Neurophysiology45: 417–442.
66.
Van GisbergenJ. A. M.RobinsonD. A. (1977) Generation of micro and macrosaccades by burst neurons in the monkey. In: BakerR.BerthozA. (eds) Control of gaze by brain stem neurons, New York, NY: Elsevier/North-Holland.
67.
Van HornM. R.CullenK. E. (2012) Coding of microsaccades in three-dimensional space by premotor saccadic neurons. Journal of Neuroscience32: 1974–1980.
68.
Wade, N. J. (2015). How were eye movements recorded before Yarbus? Perception (This Issue).
69.
WilliamsP. E.ShapleyR. M. (2007) A dynamic nonlinearity and spatial phase specificity in macaque V1 neurons. Journal of Neuroscience27: 5706–5718.
70.
YarbusA. L. (1957) The perception of an image fixed with respect to the retina. Biophysics2: 683–690.
71.
Yarbus, A. L. (1967). Eye movements and vision (B. Haigh, Trans.). New York, NY: Plenum Press.
72.
ZuberB. L.StarkL.CookG. (1965) Microsaccades and the velocity-amplitude relationship for saccadic eye movements. Science150: 1459–1460.
