Can people react to objects in their visual field that they do not consciously perceive? We investigated how visual perception and motor action respond to moving objects whose visibility is reduced, and we found a dissociation between motion processing for perception and for action. We compared motion perception and eye movements evoked by two orthogonally drifting gratings, each presented separately to a different eye. The strength of each monocular grating was manipulated by inducing adaptation to one grating prior to the presentation of both gratings. Reflexive eye movements tracked the vector average of both gratings (pattern motion) even though perceptual responses followed one motion direction exclusively (component motion). Observers almost never perceived pattern motion. This dissociation implies the existence of visual-motion signals that guide eye movements in the absence of a corresponding conscious percept.
AlmeidaJ.MahonB.Z.NakayamaK.CaramazzaA. (2008). Unconscious processing dissociates along categorical lines. Proceedings of the National Academy of Sciences, USA, 105, 15214–15218.
3.
AndrewsT.J.BlakemoreC. (1999). Form and motion have independent access to consciousness. Nature Neuroscience, 2, 405–406.
4.
BermanR.A.WurtzR.H. (2008). Exploring the pulvinar path to visual cortex. Progress in Brain Research, 171, 467–473.
5.
Büttner-EnneverJ.A.CohenB.HornA.K.E.ReisineH. (1996). Efferent pathways of the nucleus of the optic tract in monkeys and their role in eye movements. Journal of Comparative Neurology, 373, 90–107.
6.
Cobo-LewisA.B.GilroyL.A.SmallwoodT.B. (2000). Dichoptic plaids may rival but their motions can integrate. Spatial Vision, 13, 415–429.
7.
DistlerC.HoffmannK.P. (2008). Private lines of cortical visual information to the nucleus of the optic tract and dorsolateral pontine nucleus. Progress in Brain Research, 171, 363–368.
8.
EnokssonP. (1963). Binocular rivalry and monocular dominance studied with optokinetic nystagmus. Acta Ophthalmologica, 41, 544–563.
9.
FangF.HeS. (2005). Cortical responses to invisible objects in the human dorsal and ventral pathways. Nature Neuroscience, 8, 1380–1385.
10.
FoxR.ToddS.BettingerL.A. (1975). Optokinetic nystagmus as an indicator of binocular rivalry. Vision Research, 15, 849–853.
11.
GegenfurtnerK.R.XingD.ScottB.H.HawkenM.J. (2003). A comparison of pursuit eye movement and perceptual performance in speed discrimination. Journal of Vision, 3(11), Article 19. Retrieved January 29, 2008, from http://journalofvision.org/3/11/19/
12.
GoodaleM.A.MilnerA.D. (1992). Separate visual pathways for perception and action. Trends in Neurosciences, 15, 20–25.
13.
GoodaleM.A.MilnerA.D.JakobsonL.S.CareyD.P. (1991). A neurological dissociation between perceiving objects and grasping them. Nature, 349, 154–156.
14.
GrohJ.M.BornR.T.NewsomeW.T. (1997). How is a sensory map read out? Effects of microstimulation in visual area MT on saccades and smooth pursuit eye movements. Journal of Neuroscience, 17, 4312–4330.
15.
GutniskyD.A.DragoiV. (2008). Adaptive coding of visual information in neural populations. Nature, 452, 220–224.
16.
HukA.C.HeegerD.J. (2001). Pattern motion responses in human visual cortex. Nature Neuroscience, 5, 72–75.
17.
HuxlinK.R.MartinT.KellyK.RileyM.FriedmanD.I.BurginW.S.HayhoeM. (2009). Perceptual relearning of complex visual motion after V1 damage in humans. Journal of Neuroscience, 29, 3981–3991.
18.
KohnA. (2007). Visual adaptation: Physiology, mechanisms, and functional benefits. Journal of Neurophysiology, 97, 3155–3164.
19.
KomatsuH.WurtzR.H. (1988). Relation of cortical areas MT and MST to pursuit eye movements: I. Localization and visual properties of neurons. Journal of Neurophysiology, 60, 580–603.
20.
KowlerE.McKeeS.P. (1987). Sensitivity of smooth eye movement to small changes in target velocity. Vision Research, 27, 993–1015.
21.
LisbergerS.G.FerreraV.P. (1997). Vector averaging for smooth pursuit eye movements initiated by two moving targets in monkeys. Journal of Neuroscience, 17, 7490–7502.
22.
LogothetisN.K.SchallJ.D. (1990). Binocular motion rivalry in macaque monkeys: Eye dominance and tracking eye movements. Vision Research, 30, 1409–1419.
23.
MarcarV.L.ZihlJ.CoweyA. (1997). Comparing the visual deficits of a motion blind patient with the visual deficits of monkeys with area MT removed. Neuropsychologia, 35, 1459–1465.
24.
MassonG.S.CastetE. (2002). Parallel motion processing for the initiation of short-latency ocular following in humans. Journal of Neuroscience, 22, 5149–5163.
25.
MilnerA.D.GoodaleM.A. (2006). The visual brain in action (2nd ed.). Oxford, England: Oxford University Press.
26.
NewsomeW.T.BrittenK.H.MovshonJ.A. (1989). Neuronal correlates of a perceptual decision. Nature, 341, 52–54.
27.
NewsomeW.T.WurtzR.H.DürstelerM.R.MikamiA. (1985). Deficits in visual motion processing following ibotenic acid lesions of the middle temporal visual area of the macaque monkey. Journal of Neuroscience, 5, 825–840.
28.
PestilliF.VieraG.CarrascoM. (2007). How do attention and adaptation affect contrast sensitivity?Journal of Vision, 7(7), Article 9. Retrieved March 17, 2010, from http://www.journalofvision.org/content/7/7/9
29.
SperingM.GegenfurtnerK.R. (2007). Contrast and assimilation in motion perception and smooth pursuit eye movements. Journal of Neurophysiology, 98, 1355–1363.
30.
SperingM.GegenfurtnerK.R. (2008). Contextual effects on motion perception and smooth pursuit eye movements. Brain Research, 1225, 76–85.
31.
SperingM.PomplunM.CarrascoM. (2009). Differential effects of suppressed visual motion information on perception and action during binocular rivalry flash suppression. Journal of Vision, 9(8), Article 285. Retrieved April 22, 2010, from http://www.journalofvision.org/content/9/8/285
32.
StoneL.S.KrauzlisR.J. (2003). Shared motion signals for human perceptual decisions and oculomotor actions. Journal of Vision, 3(11), Article 7. Retrieved January 29, 2008, from http://www.journalofvision.org/content/3/11/7
33.
SunF.TongJ.YangQ.TianJ.HungG.K. (2002). Multidirectional shifts of optokinetic responses to binocular-rivalrous motion stimuli. Brain Research, 944, 56–64.
34.
TailbyC.MajajN.J.MovshonJ.A. (2010). Binocular integration of pattern motion signals by MT neurons and by human observers. Journal of Neuroscience, 30, 7344–7349.
35.
TamiettoM.CaudaF.CorazziniL.L.SavazziS.MarziC.A.GoebelR., et al. (2010). Collicular vision guides nonconscious behavior. Journal of Cognitive Neuroscience, 22, 888–902.
36.
TavassoliA.RingachD.L. (2010). When your eyes see more than you do. Current Biology, 20, 93–94.
37.
WeiM.SunF. (1998). The alternation of optokinetic responses driven by moving stimuli in humans. Brain Research, 813, 406–410.
38.
WeiskrantzL. (2004). Roots of blindsight. Progress in Brain Research, 144, 229–241.
39.
WilkeM.MüllerK.-M.LeopoldD.A. (2009). Neural activity in the visual thalamus reflects perceptual suppression. Proceedings of the National Academy of Sciences, USA, 106, 9465–9570.
40.
WolfeJ.M. (1984). Reversing ocular dominance and suppression in a single flash. Vision Research, 24, 471–478.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
