A Bayesian Model of Perceived Head-Centered Velocity during Smooth Pursuit Eye Movement

Abstract

During smooth pursuit eye movement, observers often misperceive velocity. Pursued stimuli appear slower (Aubert-Fleishl phenomenon [1Fleischl E.V. Physiologisch-optische Notizen, 2. Mitteilung.Sitzung Wiener Bereich der Akademie der Wissenschaften. 1882; 3: 7-25Google Scholar, 2Aubert H. Die Bewegungsempfindung.Pflugers Arch. 1886; 39: 347-370Crossref Scopus (109) Google Scholar]), stationary objects appear to move (Filehne illusion [3Filehne W. Uber das optische Wahrnehmen von Bewegungen.Zeitschrift für Sinnephysiologie. 1922; 53: 134-145Google Scholar]), the perceived direction of moving objects is distorted (trajectory misperception [4Souman J.L. Hooge I.T.C. Wertheim A.H. Frame of reference transformations in motion perception during smooth pursuit eye movements.J. Comput. Neurosci. 2006; 20: 61-76Crossref PubMed Scopus (23) Google Scholar]), and self-motion veers away from its true path (e.g., the slalom illusion [5Freeman T.C.A. Banks M.S. Crowell J.A. Extraretinal and retinal amplitude and phase errors during Filehne illusion and path perception.Percept. Psychophys. 2000; 62: 900-909Crossref PubMed Scopus (29) Google Scholar]). Each illusion demonstrates that eye speed is underestimated with respect to image speed, a finding that has been taken as evidence of early sensory signals that differ in accuracy [4Souman J.L. Hooge I.T.C. Wertheim A.H. Frame of reference transformations in motion perception during smooth pursuit eye movements.J. Comput. Neurosci. 2006; 20: 61-76Crossref PubMed Scopus (23) Google Scholar, 6Freeman T.C.A. Transducer models of head-centred motion perception.Vision Res. 2001; 41: 2741-2755Crossref PubMed Scopus (42) Google Scholar, 7Wertheim A.H. Motion perception during self-motion: The direct versus inferential controversy revisited.Behav. Brain Sci. 1994; 17: 293-311Crossref Scopus (160) Google Scholar, 8Turano K.A. Massof R.W. Nonlinear contribution of eye velocity to motion perception.Vision Res. 2001; 41: 385-395Crossref PubMed Scopus (53) Google Scholar, 9Beintema J.A. van den Berg A.V. Pursuit affects precision of perceived heading for small viewing apertures.Vision Res. 2001; 41: 2375-2391Crossref PubMed Scopus (9) Google Scholar, 10Perrone J.A. Krauzlis R.J. Vector subtraction using visual and extraretinal motion signals: A new look at efference copy and corollary discharge theories.J. Vis. 2008; 8: 1-14Crossref Scopus (28) Google Scholar, 11Souman J.L. Freeman T.C.A. Motion perception during sinusoidal smooth pursuit eye movements: Signal latencies and non-linearities.J. Vis. 2008; 8: 1-14Crossref PubMed Scopus (8) Google Scholar]. Here we present an alternative Bayesian account, based on the idea that perceptual estimates are increasingly influenced by prior expectations as signals become more uncertain [12Ernst M.O. Bülthoff H.H. Merging the senses into a robust percept.Trends Cogn. Sci. 2004; 8: 162-169Abstract Full Text Full Text PDF PubMed Scopus (1208) Google Scholar, 13MacNeilage P.R. Banks M.S. Berger D.R. Bülthoff H.H. A Bayesian model of the disambiguation of gravitoinertial force by visual cues.Exp. Brain Res. 2007; 179: 263-290Crossref PubMed Scopus (168) Google Scholar, 14Ma W.J. Beck J.M. Latham P.E. Pouget A. Bayesian inference with probabilistic population codes.Nat. Neurosci. 2006; 9: 1432-1438Crossref PubMed Scopus (960) Google Scholar, 15Clark J.J. Yuille A.L. Data Fusion for Sensory Information Processing Systems. Kluwer Academic, Boston1990Crossref Google Scholar]. We show that the speeds of pursued stimuli are more difficult to discriminate than fixated stimuli. Observers are therefore less certain about motion signals encoding the speed of pursued stimuli, a finding we use to quantify the Aubert-Fleischl phenomenon based on the assumption that the prior for motion is centered on zero [16Welchman A.E. Lam J.M. Bülthoff H.H. Bayesian motion estimation accounts for a surprising bias in 3D vision.Proc. Natl. Acad. Sci. USA. 2008; 105: 12087-12092Crossref PubMed Scopus (48) Google Scholar, 17Stocker A.A. Simoncelli E.P. Noise characteristics and prior expectations in human visual speed perception.Nat. Neurosci. 2006; 9: 578-585Crossref PubMed Scopus (516) Google Scholar, 18Weiss Y. Simoncelli E.P. Adelson E.H. Motion illusions as optimal percepts.Nat. Neurosci. 2002; 5: 598-604Crossref PubMed Scopus (719) Google Scholar, 19Hürlimann F. Kiper D.C. Carandini M. Testing the Bayesian model of perceived speed.Vision Res. 2002; 42: 2253-2257Crossref PubMed Scopus (61) Google Scholar, 20Ascher D. Grzywacz N.M. A Bayesian model for the measurement of visual velocity.Vision Res. 2000; 40: 3427-3434Crossref PubMed Scopus (36) Google Scholar]. In doing so, we reveal an important property currently overlooked by Bayesian models of motion perception. Two Bayes estimates are needed at a relatively early stage in processing, one for pursued targets and one for image motion.