eye movements reset visual perception · waves were ﬁrst reported over 50 years ago (evans,...

Eye movements reset visual perception

Michael A. Paradiso # $Department of Neuroscience, Brown University,

Providence, RI, USA

Dar Meshi $

Berlin School of Mind & Brain,

Humboldt-Universitat zu Berlin, Berlin, Germany

Department of Education and Psychology,

Freie Universitat Berlin, Berlin, Germany

Jordan Pisarcik $Department of Neuroscience, Brown University,

Providence, RI, USA

Samuel Levine $Department of Neuroscience, Brown University,

Providence, RI, USA

Human vision uses saccadic eye movements to rapidly shift the sensitive foveal portion of our retina to objects of interest.For vision to function properly amidst these ballistic eye movements, a mechanism is needed to extract discrete percepts oneach fixation from the continuous stream of neural activity that spans fixations. The speed of visual parsing is crucialbecause human behaviors ranging from reading to driving to sports rely on rapid visual analysis. We find that a brain signalassociated with moving the eyes appears to play a role in resetting visual analysis on each fixation, a process that may aidin parsing the neural signal. We quantified the degree to which the perception of tilt is influenced by the tilt of a stimulus on apreceding fixation. Two key conditions were compared, one in which a saccade moved the eyes from one stimulus to thenext and a second simulated saccade condition in which the stimuli moved in the same manner but the subjects did notmove their eyes. We find that there is a brief period of time at the start of each fixation during which the tilt of the previousstimulus influences perception (in a direction opposite to the tilt aftereffect)—perception is not instantaneously reset when afixation starts. Importantly, the results show that this perceptual bias is much greater, with nearly identical visual input, whensaccades are simulated. This finding suggests that, in real-saccade conditions, some signal related to the eye movementmay be involved in the reset phenomenon. While proprioceptive information from the extraocular muscles is conceivably afactor, the fast speed of the effect we observe suggests that a more likely mechanism is a corollary discharge signalassociated with eye movement.

Keywords: saccades, eye movements, perception, temporal coding

Citation: Paradiso, M. A., Meshi, D., Pisarcik, J., & Levine, S. (2012). Eye movements reset visual perception. Journal ofVision, 12(13):11, 1–14, http://www.journalofvision.org/content/12/13/11, doi:10.1167/12.13.11.

Introduction

Humans visually explore their environment bymaking three to four fixations every second, eachfollowed by a saccadic eye movement to the next objectof interest. The problem the brain faces interpretingvisual input is illustrated in Figure 1: Neural activity invisual areas of the brain is a continuous stream butperception occurs in discrete epochs of time corre-sponding to eye fixations. A question that has receivedconsiderable attention is how we perceive a stablevisual world amidst the saccades (Melcher & Colby,2008; Von Helmholtz, 1924; Wurtz, 2008); i.e., how isour visual experience tied together from one fixation tothe next? A complementary problem that has received

much less attention is how the brain breaks apart thecontinuum into neural activity that distinctly codesinformation on each fixation. In other words, how isthe beginning of a new fixation recognized so thatsubsequent neural activity can be interpreted as therepresentation of a distinct image? In most laboratorystudies of vision this question is circumvented—theexperiments impose a stimulus onset time by flashingan image after a subject has held fixation for anextended time. However, in natural vision, objectscome into view by saccades rather than flashing and itis unclear how visual analysis is reset so that neuralsignals can be parsed.

One might speculate that neurons’ sudden responseonset at the start of each new fixation is sufficient tosynchronize perception with brain activity. However,

Journal of Vision (2012) 12(13):11, 1–14 1http://www.journalofvision.org/content/12/13/11

doi: 10 .1167 /12 .13 .11 ISSN 1534-7362 � 2012 ARVOReceived June 19, 2012; published December 12, 2012

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there is not a simple relationship between stimulus onsettime and neural response onset: From cell to cell, visualresponse latencies in the visual cortex cover a wide rangeand the latency of any given cell is influenced by contrastand other parameters (Bair, Cavanaugh, Smith, &Movshon, 2002; Huang & Paradiso, 2005; Lennie,1981; Maunsell & Gibson, 1992; Tolhurst, Movshon,& Thompson, 1981). Also, V1 responses tend to betransient (Muller, Metha, Krauskopf, & Lennie, 2001),so a decline in response is not a reliable indication of theend of a fixation. Considered together, these factorssuggest that visual signals alone may not suffice toprecisely infer fixation start and stop times; informationfrom eye movements may be advantageous. The needfor rapid visual analysis is underscored by studiesdemonstrating that behavioral decisions based on visualinput can be made extremely quickly (Stanford,Shankar, Massoglia, Costello, & Salinas, 2010; Thorpe,Fize, & Marlot, 1996).

There is no question that neural activity across manybrain structures is modulated by saccades. Lambdawaves were first reported over 50 years ago (Evans,1953). These occipital electroencephalography (EEG)transients are associated with saccadic eye movementsused to explore complex images; they disappear in thedark, with uniform visual stimulation or with pro-longed fixation (Brigo, 2011). Numerous studies haveshown saccade-related neural activity in BOLD signals,local field potentials (LFPs), and spiking activity (e.g.,in occipital cortex, Bodis-Wollner et al., 2002; Purpura,Kalik, & Schiff, 2003; Rajkai et al., 2008). In somebrain areas and in some situations, there is alsoreceptive field remapping prior to saccades which alters

visual responses (Churan, Guitton, & Pack, 2011;Melcher & Colby, 2008; Nakamura & Colby, 2002;Parks & Corballis, 2010). During saccades there arechanges in brain activity (e.g., Bremmer, Kubischik,Hoffmann, & Krekelberg, 2009; Reppas, Usrey, &Reid, 2002) that may be related to the perceptualphenomenon of saccadic suppression (e.g., Matin,1974; Ross, Morrone, Goldberg, & Burr, 2001;Sylvester, Haynes, & Rees, 2005; Yu & Lee, 2000).

Thus it is well established that brain activity ismodulated by saccades. In our own research we findfurther that macaque V1 neurons carry informationsufficient to precisely estimate the start of new fixations(Ruiz et al., 2010). The question addressed in thepresent study is if there are perceptual indications thatvision is reset on new fixations. To our knowledge,there is only one previous experiment that investigatedthis question, that one using the Necker cube and otherbistable stimuli (Ross & Ma-Wyatt, 2004). The Neckercube is typically perceived in one of two states forintervals of 3–5 s. There was prior evidence of aninteraction between perceptual state and eye move-ments, as it was found that fixations are longer induration just after a state reversal, perhaps reflectingthe time needed to establish the new representation(Ellis & Stark, 1978). In the Ross and Ma-Wyatt (2004)study, bistable stimuli were intermittently presentedand it was found that saccades shorten the duration ofstates of ambiguous figures, suggesting that visual inputon a previous fixation may be erased (Ross & Ma-Wyatt, 2004). Our goal was to investigate visual resetwith a standard measure of visual performance that isthought to tap into low level cortical mechanisms—

Figure 1. The visual parsing problem. (a) A record of eye position in a macaque freely viewing a complex natural image. A saccade about

68 in amplitude separates two fixations. (b) An unfiltered recording from macaque area V1 shows the continuous stream of neural activity

at different frequencies that spans the fixations and intervening saccade. Parsing continuous neural activity into epochs associated with

objects seen on distinct fixations would be simplified if visual processing was informed when a new fixation begins. Data are from

experiments reported in Ruiz and Paradiso (2012).

Journal of Vision (2012) 12(13):11, 1–14 Paradiso, Meshi, Pisarcik, & Levine 2


orientation discrimination. We find that stimulusorientation on each fixation transiently influences theorientation perceived on a subsequent fixation. Sac-cades significantly reduce the magnitude of thisinfluence, consistent with the hypothesis that vision isreset, at least in part, by an eye movement signal.

Methods

To explore the possibility that eye-movement infor-mation assists in resetting and parsing visual signals, anorientation discrimination experiment with Gabor stim-uli was used to measure the extent to which perceptionon one fixation influences perception on the next (Figure

2). Unlike studies of saccadic suppression (Matin, 1974),the experiments here assessed interactions betweenstimuli seen during fixations rather than perception ofstimuli presented during saccades. Presumably becauseof the behavioral importance of edge detection, humansare remarkably sensitive to the orientation of lines oredges; under optimal conditions a tilt less than 0.58 canbe reliably discriminated (Andrews, 1967; Paradiso &Carney, 1988).

Subjects and visual stimuli

Three subjects participated in the study, all withnormal or corrected-to-normal vision. Subjects sat in a

Figure 2. Two experiments used to examine the influence of one stimulus’ orientation (Gabor 1) on the perceived orientation of a second

stimulus (Gabor 2). (a) Task with real saccades. After a subject fixates a 0.18 radius red target (exaggerated in size for illustrative

purposes) for 500 ms, a Gabor stimulus with orientation of 6 88, 6 48, or 08 relative to vertical is displayed for 250 ms. At the end of the

Gabor 1 display period, a green fixation point appeared 108 to the right. The subject made a saccade to Gabor 2 (orientations were 6 48,

6 28, 6 18, and 08 from vertical) and indicated whether it appeared tilted clockwise or counter-clockwise from vertical. To limit the time

interval available to make the discrimination, a binary noise stimulus (mask) was presented at various times after Gabor 2 and stayed

visible until a behavioral response was made. (b) Task with simulated saccades. The subject held fixation at the central location

throughout the trial. The two Gabor stimuli and the mask appeared in the same temporal sequence as with a real saccade. However, in

this simulated saccade condition, Gabor 2 moved into view rather than having a saccade take the eyes to the stimulus.



dimly lit room and used a bite bar that positioned theeyes 60 cm from a visual display (160 Hz). The displayused in the experiments was an Iyama HM204DT CRTwith a P22 phosphor. An infrared eye tracker measuredeye position at 240 Hz (IScan Inc). Stimuli were two-dimensional Gabor patterns (Gaussian damped lumi-nance sinewaves) with a spatial frequency of 0.8 c/8 anda peak Michelson contrast of 0.1. Two experimentswere used to examine the influence of one stimulus’orientation (Gabor 1) on the perceived orientation of asecond stimulus (Gabor 2). In one version of theexperiment, subjects made a saccade to view Gabor 2and in the second version subjects held fixation while asimulated saccade moved Gabor 2 into the fovea. Inboth experiments subjects were instructed to avoidblinking during the trials. This was readily achieved assubjects initiated each trial with a button press andcould pause as desired.

Experiments with saccades

As detailed in Figure 2, in the experiment with realsaccades, subjects viewed a Gabor stimulus at variousorientations for 250 ms and then made a saccade toview a second Gabor stimulus 108 to the right. The taskwas a two-alternative forced-choice discrimination ofthe Gabor 2 tilt (clockwise or counter-clockwise fromvertical). The contrast of Gabor 2 was set at a low valueso that it could not be detected when the subject fixatedGabor 1. At an eccentricity of 108 contrast threshold isabout 0.25 (Rovamo, Virsu, & Nasanen, 1978) and, aswe confirmed, the 0.1 contrast Gabor could not bedetected above chance levels before initiating thesaccade. Indeed, with static fixation, contrast thresholdshould not be reached until the eye is less thanapproximately 28 from the Gabor 2 fixation point(Rovamo et al., 1978). Moreover, at saccadic velocitiescontrast threshold would not be reached until the eyesare significantly less than 28 from the second fixationpoint (Kelly, 1979; Robson, 1966). All of this is to saythat our best estimate is that the temporal interval inwhich Gabor 2 can be examined does not begin untilthe eyes are just about at the second fixation point.

To limit the time available to discriminate the Gabor2 orientation, a binary noise stimulus (mask) waspresented at various times after Gabor 2 and stayedvisible until a behavioral response was made. The maskwas meant to truncate neural activity on the secondfixation (Figure 1) so that the orientation discrimina-tion had to be performed with the early activity on thesecond fixation. Because of the short duration and lowcontrast of the stimuli, afterimages were not seen. Toestimate the viewing time at the second fixation pointprior to masking, we had subjects perform a largenumber of 108 saccades and we recorded the time it

took to plan and execute them. As Gabor 2 was turnedon at the same time as the second fixation point, weestimated the foveal viewing time of Gabor 2 bysubtracting the average planning and execution timefrom the display time prior to masking. Gabor 2duration was adjusted to give estimated viewing times(i.e., time during which Gabor 2 was foveated) of 50,100, 150, and 400 ms. For brevity in describing theresults, we refer to these as ‘‘Gabor 2 times.’’ Note thatfor all stimulus display times in this study, actualdisplay times are roughly 5 ms shorter than thosespecified because on the last display frame the P22phosphor decays before the frame is over (Bridgeman,1998; Elze, 2010).

The three observers completed somewhat differentnumbers of trials. There were trials at each of fourGabor 2 times, seven Gabor 1 orientations, and fiveGabor 2 orientations. Observer TL completed 72 setsof data (10,080 trials), AG completed 57 sets (7,980),and DM completed 60 sets (8,400).

For trials to be accepted, subjects’ saccades had todecelerate and remain within a 1.78 window aroundGabor 2. In this experiment and the simulated saccadeexperiment below, each data point in the graphs comesfrom 57–75 discriminations per subject. Correctivesaccades did not cause a trial to be aborted as long asthe eyes stayed in the fixation window effectivelykeeping the stimulus in the fovea. Likewise, no attemptwas made to limit fixation saccades. It is worth notingthat at 0.8 c/8, the data should not be significantlyaffected by saccadic suppression (Burr, Morrone, &Ross, 1994).

Experiments with simulated saccades

To assess the possible role of saccadic eye move-ments in visual reset, a second experiment wasconducted. The sequence and timing of visual stimu-lation were as similar as possible to the experimentdescribed above, but the subject held fixation at thecentral location throughout the trial. To simulate thechanges in visual stimulation produced by saccades,subjects’ eye movements were measured and interpo-lated at the 160 Hz display rate. On average, it tookobservers 100 ms to initiate a saccade and the 108saccade had a duration of 44 ms. The fast latency of thesaccades is consistent with reports that express saccadesare common when eye movements are made to trainedlocations, especially on a blank background (Bibi &Edelman, 2009; Fischer & Boch, 1982; Fischer, Boch, &Ramsperger, 1984).

At the start of a simulated-saccade trial, Gabor 1appeared for 250 ms as in real-saccade experiments.Gabor 2 then appeared at the peripheral fixation pointand was stationary for 100 ms to simulate the time



prior to saccade initiation measured in real saccades.Gabor 2 was then presented for single video frames (6.3ms) at successive locations moving toward screen centerbased on the accelerations and speeds of real saccades.The stimulus center locations were: 108, 9.28, 7.18, 4.98,3.28, 1.68, 0.48, and 08 from screen center (total durationof simulated saccade ¼ 7 · 6.3 ms ¼ 44.1 ms). AfterGabor 2 was viewed for a variable duration (50, 100,150, and 400 ms), a visual mask appeared as in the real-saccade experiment. As the computer controlled whenGabor 2 entered the fovea in the simulated-saccadeexperiment, we were able to control viewing time priorto masking and match values to those in the real-saccade experiment. In simulated saccade experiments,subjects had to keep their eyes within a central 1.78window for the entire trial. As in the experiments withreal saccades, normal fixation saccades were notlimited.

The three observers completed somewhat differentnumbers of trials. There were trials at each of fourGabor 2 times, seven Gabor 1 orientations, and fiveGabor 2 orientations. Observer TL completed 75 setsof data (10,500 trials), AG completed 57 sets (7,980),and DM completed 60 sets (8,400).

Unlike with real saccades, in the simulated saccadeexperiments, fixation was maintained. Due to this, apotential concern in the simulated saccade experimentsis that the effective Gabor 1 duration might be longerthan desired because of persistence in the CRTphosphor. However, this is not an issue as the P22phosphor of the Iyama display decays to near zero lessthan 2 ms after initial excitation (Elze, 2010).

Control experiments

A control experiment was performed to furtherassess the influence that a stimulus seen on one fixationhas on the perception of a stimulus on a subsequentfixation. Data collected in the real- and simulated-saccade experiments indicated that at short Gabor 2viewing times the perceived tilt of Gabor 2 was biasedby the orientation of Gabor 1. In the controlexperiment, the real- and simulated-saccade experi-ments described above were repeated with one change:At the beginning of the sequence in Figure 2, the firstfixation point was shown for the same time as in theregular experiments, but no Gabor 1 stimulus wasactually shown. Gabor 2 was presented at one of sixorientations: þ/� 48, þ/� 28, þ/� 18. Subjects indicatedwhether Gabor 2 appear tilted clockwise (CW) orcounter-clockwise (CCW) from vertical. Rather thancomputing bias as in the main experiments, we wereable to compute the percentage of correct responses tosee if the task was doable, particularly at short Gabor 2time. In real-saccade control experiments, all three

observers completed 1,440 trials (four Gabor 2 times atsix orientations repeated 60 times). In simulated-saccade control experiments, observer TL completed60 data sets (1,440 trials), AG completed 45 sets (1,080trials), and DM completed 75 sets (1,800 trials).

Results

The data obtained from three observers in theexperiment with real saccades are shown in Figure 3.Figure 3a shows a standard psychometric curve fororientation discrimination of Gabor 2 where psycho-metric curves were fit to the data as logistic functions(origin). In Figure 3a, the probability that the secondGabor was perceived clockwise from vertical at Gabor2 viewing times of 50, 100, 150, and 400 ms is displayed.As one would expect, the more clockwise Gabor 2 was,the more likely the subjects were to say that it was tiltedclockwise. As Gabor 2 time is reduced from 400 ms to50 ms, the curves flatten, indicating that variations inthe tilt are more difficult to discern.

The differently-colored curves in Figure 3a showperformance separately for trials with different orien-tations of Gabor 1. Surprisingly, at all Gabor 2 times,when Gabor 1 was more clockwise, the subjects weremore likely to say that Gabor 2 was clockwise (e.g.,pink and green traces displaced upward compared tored and black traces). Also apparent as Gabor 2 timedecreases is an increasing separation between the curvesrepresenting different Gabor 1 orientations (i.e., theinfluence of Gabor 1 on the perceived tilt of Gabor 2increases as there is less time to view Gabor 2).Evidently, despite the loss of sensitivity that occursduring saccades (saccadic suppression) (Matin, 1974),there are large trans-saccadic influences at the start of asaccade. Consistent with studies of trans-saccadicmemory, subjects did not simultaneously see Gabor 1and Gabor 2 (Bridgeman & Mayer, 1983; Irwin, 1996;Rayner & Pollatsek, 1983); rather, Gabor 1 biased theperception of Gabor 2. Note however that the directionof the interaction is opposite that seen with adaptationin the tilt aftereffect (Gibson & Radner, 1937). Figure3b replots the data to directly show the probability thatGabor 2 was perceived clockwise from vertical as afunction of Gabor 1 orientation. At the shortest Gabor2 time there is a strong relationship between Gabor 1tilt and Gabor 2 perception. This relationship falls offat longer Gabor 2 viewing times. The results in Figure 3make the important point that the transition fromvisual analysis on one fixation to the next is notinstantaneous. When there is sufficient viewing time(hundreds of milliseconds as in a normal fixation), thetilt of a visual stimulus is veridically perceived and itdepends little or not at all on the properties of a



preceding stimulus. At intermediate times, the percep-tion of Gabor 2 has a mixture of the attributes of thefirst and second stimuli and as viewing time decreases,perception is increasingly biased by the precedingstimulus. The timecourse of the falloff is appropriatefor the duration of human fixations and consistent withthe distinct percepts across fixations in our dailyexperience.

Figure 4 shows control data indicating the percent-age of correct orientation discriminations that weremade based on Gabor 2 tilt when Gabor 1 was notpresented. As expected, performance increased withGabor 2 time (e.g., black traces for 400 ms higher inplots than red traces for 50 ms). Panels A and B showvariation between observers in the control experimentswith real (Figure 4a) and simulated (Figure 4b)

Figure 3. Effect of Gabor 1 and Gabor 2 orientation on the perception of Gabor 2 when a saccade separates the two stimuli. The

percentage of clockwise responses averaged across three observers at four Gabor 2 times (50, 100, 150, 400 ms) as a function of Gabor

2 (a) or Gabor 1 (b) orientation. The differently-colored curves show performance separately for trials with different orientations of Gabor 1

(a) or Gabor 2 (b). Data for each Gabor 2 time have a narrow range of Gabor 2 viewing times (checked for variable saccade planning time)

so that the data can be compared to simulated saccade data (Figure 5). Error bars show the standard error of the mean. At longer Gabor 2

times, the perception of Gabor 2’s orientation is correct with little influence from the tilt of the preceding stimulus. At shorter Gabor 2 times

the opposite is true: The perceived orientation of Gabor 2 follows more closely the tilt of Gabor 1 rather than Gabor 2’s actual orientation

(top row). Bias is a measure of the influence of Gabor 1 on the perception of Gabor 2. Bias is defined as the average distance between

data points at the� 88 andþ 88 Gabor 1 orientations (bias is calculated at all Gabor 2 times but is shown here with a black arrow at the 50

ms time).



saccades. Three traces are shown at each masking time,corresponding to the three observers. Figure 4ccompares discrimination in real (solid lines) andsimulated (dashed lines) saccade conditions. Thecontrol data make two valuable points. First, thoughthere are individual conditions at which performance isnear chance, even at the shortest Gabor 2 time,orientation can often be discriminated above chance(not surprisingly, performance is closest to chance forthe smallest tilts). In other words, observers could seethe Gabor 2 stimuli with real and simulated saccades.Second, though there are differences, performance inreal and simulated saccade conditions are similar. Tothe extent one can infer from the control data, it is notthe case that the Gabor 2 stimuli are significantly morevisible or discriminable in one condition or the other.

To assess whether saccadic eye movements play arole in parsing visual signals on distinct fixations, weconducted a second experiment. The visual stimuli wereidentical to those used in the first experiment butinstead of a saccade bringing Gabor 2 into the fovea,the eyes were stationary and Gabor 2 moved (Figure2b). The simulated saccades were created by using theeye tracker to sample subjects’ saccades and interpo-lated at the visual display’s 160 Hz framerate. In thisway simulated saccades were shown to fixating subjects;instead of the eyes moving, the stimuli moved with theaccelerations and velocities of the real saccades. Thekey difference was the absence of actual eye movementsin the simulated condition and consequently theabsence of the associated corollary discharge andproprioceptive signals in the brain.

Experiments conducted with the simulated saccadesgave data that were qualitatively similar to the dataobtained with real saccades. Figure 5 shows how theperception of tilt in Gabor 2 varied with the orientationof Gabor 2 (Figure 5a) and Gabor 1 (Figure 5b). Uponcloser inspection there are differences in the slopes ofthe psychometric curves and more pronounced differ-ences in the separation between the curves compared tothe real saccade data in Figure 3. To quantify theinfluence of Gabor 1 on the perception of Gabor 2 inreal and simulated saccade experiments, we calculated ameasure of bias. Bias is defined, at any Gabor 2 time, asthe average separation in Figures 3a and 4a between thecurves representing the extreme orientations of Gabor 1(6 88). If the perceived tilt of Gabor 2 is based entirelyon its orientation, bias should be zero. On the otherhand, if the perception of Gabor 2 tilt were basedentirely on the orientation of the preceding stimulus(Gabor 1), bias would be one.

Bias is plotted in Figure 6 across the four Gabor 2times. The gradual decrease in bias as Gabor 2 timeincreases shows that the first stimulus influences theperception of the second stimulus for a transient timeperiod. On average across our three subjects, sometrans-saccadic bias persists even with fixations ofnormal durations. Perhaps the most surprising aspectof the data in Figure 6 is the large difference in bias inreal and simulated saccade experiments. At the shortestGabor 2 time (50 ms), bias in the real saccadeexperiment is 0.65 but in the simulated saccadeexperiment bias is 0.93. In other words, with very shortviewing times when a saccade is used to bring Gabor 2into view, the perception of Gabor 2 is based on a

Figure 4. Control experiments in which Gabor 2 orientation was discriminated but Gabor 1 was not presented. (a) Orientation

discrimination in experiments with real saccades. At each of the four viewing times for Gabor 2, data are shown for three observers (color

matched). (b) Orientation discrimination in experiments with simulated saccades. (c) Comparison of orientation discrimination in real and

simulated saccade experiments where data is averaged across the three observers shown in Panels A and B. Solid lines show real

saccade and dotted lines simulated saccade performance.



mixture of the properties of Gabor 1 and Gabor 2.Strikingly, in the same situation, but without thesaccade, the perception of Gabor 2 is based almostentirely on the orientation of the previous stimulus.

Discussion

Saccadic eye movements are a fundamental meansby which humans explore the visual environment.However, saccades introduce two complementarychallenges for vision. On the one hand, we have aremarkably stable sense of the visual world despite thesudden changes in visual input that saccades produce.It is common experience that moving one’s eye bypushing on it appears to displace everything in view,but a similar eye movement resulting from a saccadeleaves the world stationary. Consistent with theproposal made by von Helmholtz in the 19th century,a corollary discharge signal (i.e., a signal sent to visualcortex related to the motor command to move the eyes,Sperry, 1950; Von Holst & Mittelstaedt, 1950, 1971)may be used to internally compensate for eye move-ments and give us a sense of visual stability (VonHelmholtz, 1924; Wurtz, 2008). Physiological studiesindicate that corollary discharge signals from thebrainstem reach cerebral cortex very quickly, causinga burst of activity in the frontal eye fields in about 2 ms(Sommer & Wurtz, 2004a, 2004b). Such an effect onvisual neurons may underlie receptive field remappingthat occurs in some extrastriate areas prior to saccades(Colby, Duhamel, & Goldberg, 1993; Duhamel, Colby,& Goldberg, 1992; Melcher & Colby, 2008). While notyet proven, receptive field remapping via corollarydischarge may be a neural mechanism of visual stability(Melcher & Colby, 2008; Sommer & Wurtz, 2008),though there are experimental and theoretical reasonsfor questioning the link between corollary dischargeand space constancy (Bridgeman, 2007; Ilg, Bridgeman,& Hoffmann, 1989). Another important component of

Figure 5. Effect of Gabor 1 and Gabor 2 orientation on the

perception of Gabor 2 when a simulated saccade separates the

two stimuli. The percentage of clockwise responses averaged

across three observers at four Gabor 2 times (50, 100, 150, 400

ms) as a function of Gabor 2 (a) or Gabor 1 (b) orientation when a

simulated saccade brings Gabor 2 into view. Error bars show the

standard error of the mean. As with real saccades, there is a

graded effect in which the orientation of Gabor 2 appears more

similar to the actual orientation of Gabor 1 at short Gabor 2 times

and progressively becomes more similar to the actual orientation

of Gabor 2 at longer Gabor 2 times. The measure of bias is

computed as with real saccades (illustrated here at the 50 ms

Gabor 2 time).

Figure 6. Summary of perceptual bias measurements with real

and simulated saccades averaged across three observers. At

long Gabor 2 times corresponding to normal length fixations, there

is no difference between bias measures with real and simulated

saccades. At short Gabor 2 times, bias is much greater with

simulated saccades suggesting that real saccades quickly

decrease the influence of the preceding stimulus. Error bars

show the standard error of the mean.



the visual stabilization process may be saccadicsuppression, the reduction in visual sensitivity forobjects seen during saccades (Holt, 1903; Matin,1974; Ross et al., 2001; Wurtz, 2008).

Resetting perception on each fixation

The complementary problem to visual stability,which is addressed here, is the distinct nature ofpercepts on each fixation. Rather than asking how westitch the world together across saccades for thepurpose of visual stability, we have investigated howwe break vision apart into distinct percepts on eachfixation. Vision is based on a continuous stream ofneural activity spanning endless fixations and saccadesand a mechanism is needed, of which little is known, toextract discrete percepts from the continuum. Asdiscussed in the Introduction, it is not obvious thatvisual input alone reliably informs the visual cortexwhen a new fixation starts and stops.

As thousands of experiments have demonstrated, itis certainly possible for vision to carry on withoutsaccades when stimuli are flashed to a fixating animalor person. However, visual responses are markedlydifferent in natural vision (Gallant, Connor, & VanEssen, 1998; Livingstone, Freeman, & Hubel, 1996;Ruiz & Paradiso, 2012) and it isn’t clear if parsing ofvisual signals proceeds in the same manner in unnaturalfixation experiments with flashed stimuli. With asaccade, visual input at every point in the visual fieldis different on the fixations before and after thesaccade. On the other hand, in typical fixationexperiments, there is generally a fixation period of200–300 ms prior to stimulus presentation in whichadaptation will occur; when the target stimulus ispresented there is presumably a response transient toonly the new stimulus.

It is the case that very brief fixations sometimesoccur in natural human vision (Hayhoe, Shrivastava,Mruczek, & Pelz, 2003). If perceptual bias occurs for abrief period of time at the start of each new fixation,this suggests that there might be imprecision inperception on brief fixations. To our knowledge thishas not been studied, in contrast to many experimentson the perception of briefly flashed stimuli duringlonger fixations. To examine perceptual bias on brieffixations, it would be necessary to quantify perception(e.g., orientation estimation) in the context of visualinput on the preceding fixation.

The hypothesis explored here is that in naturalvision, eye movements play an important role inresetting visual analysis on each fixation. The resultsshow that perception is a graded process—there is abrief transition period at the beginning of each newfixation during which perception blends information

from the old and new fixation. We do not experiencesuch blended percepts in daily experience presumablybecause visual processing is not abnormally curtailedby masking stimuli. However, the implication is thatthe neural representation of the stimuli takes a finitetime to transition from one percept to the next,presumably because perception is based on theintegration of information over tens of milliseconds.With a fixation of normal duration (and no masking),the information would come from the image on thecurrent fixation. However, for brief masked stimuli, theneural activity used to make a perceptual judgmentmay extend back into the brain’s response to theprevious stimulus. Most importantly, we find that whena saccade brings an image into view, the influence of thepreceding stimulus is reduced much more quickly thanwhen the visual input is the same but no actual eyemovement occurs (i.e., simulated saccades). It is thisdifference between perceptual bias between fixationswith real and simulated saccades that implies that thesaccade is important for resetting perception.

Alternative interpretations

An alternative to the interpretation made here is thatperceptual bias across fixations results from the tiltaftereffect in which adaptation to a line at oneorientation shifts the perceived orientation of asubsequent line (both lines presented in sequenceduring a single fixation) (Gibson & Radner, 1937).Melcher has shown that the tilt aftereffect is found evenwhen the adaptation and test stimuli are separated by asaccade (Melcher, 2005, 2007, 2008). However, ourexperiment was structured to avoid adaptation and thebias we observed is incompatible with the tilt aftereffectin two critical ways. First, adaptation to a line tiltedclockwise from vertical makes a subsequent line lookmore counterclockwise rather than clockwise as in ourstudy (i.e., the direct tilt aftereffect that occurs at smallangles similar to what we used is a repulsion ratherthan an attraction as we observe). Second, the durationof the Gabor 1 stimulus (250 ms) in our experiment ismuch shorter than the adaptation periods generallyfound to give a significant tilt aftereffect (Gibson &Radner, 1937; Greenlee & Magnussen, 1987). (In theMelcher studies examining trans-saccadic aftereffects,each trial involved adaptation for 3–5 s in contrast tothe 250 ms of our first stimulus.)

Besides the tilt aftereffect, one might speculate thatsome other form of aftereffect, adaptation, masking, orpriming is responsible for the trans-saccadic orientationbias we observe. However, these explanations areunlikely to be correct because they don’t account forthe large performance difference in real and simulatedsaccade conditions despite similar retinal stimulation.



Another possibility is that as the task became moredifficult at shorter Gabor 2 times, the subjectsunwittingly resorted to reporting the orientation ofthe first stimulus. One reason for thinking this is not thecase is that in control experiments we found thatsubjects could discriminate the second Gabor stimulusabove chance levels even at the shortest Gabor 2 time(Figure 4). But even aside from this observation, it isn’tclear why there would be quite different levels ofresponse bias in real and simulated saccade experimentsthat are similar in most every way.

The significant difference between orientation biasmeasurements with real and simulated saccades sug-gests that a signal related to the real eye movement isinvolved. However, this interpretation hinges on thesimilarity of the trials with real and simulated saccades.Ultimately, it is impossible to completely match realand simulated saccades. Even with largely equivalentvisual stimulation, motion in the simulated saccadecondition is discretized by the computer display’srefresh rate, and there are possible differences in themoment-to-moment allocation of attention. We havenot found a straightforward account of the findingsbased on these differences, but it is conceivable thatadditional factors are involved.

Possible mechanisms

The resetting of perception by eye movements isconsistent with the finding that the transient states ofunstable figures are disrupted by saccades (Ross & Ma-Wyatt, 2004). The lack of carry-over between fixationsis also reminiscent of visual memory studies that showthat little information is stored from one fixation to thenext (Bridgeman & Mayer, 1983; Irwin, 1996; Rayner& Pollatsek, 1983). In seeking a neural correlate ofperceptual reset, there is a daunting diversity ofchanges in neural activity at the start of fixations thatis conceivably related. For example, in macaque LGN,saccadic and post-saccadic activity is complex, includ-ing both suppression and facilitation (with facilitationdominant) and a more rapid response to visual input(Buttner & Fuchs, 1973; Ramcharan, Gnadt, & Sher-man, 2001; Reppas et al., 2002). In macaque area V1,Rajkai et al. (2008) found that when macaques makesaccades in the dark there is a phase alignment ofneural activity shortly after the start of each newfixation; they speculated that this may enhanceresponses to new stimuli (Rajkai et al., 2008).Maldonado et al. (2008) reported that 30–90 ms afterthe start of new fixations there is enhanced responsesynchronization to natural image stimuli (Maldonadoet al., 2008). In macaque areas MT and MST, activitysuppression during saccades is followed by enhanced

responses to moving stimuli (Ibbotson, Price, Crowder,Ono, & Mustari, 2007).

The large difference in orientation bias that we foundbetween real and simulated saccades indicates thatsomething about the eye movement is responsible fordecreasing the influence of the preceding stimulus (i.e.,resetting analysis on the new fixation). This processmay be related to saccadic suppression, but there arenotable differences. Rather than suppressed visualsensitivity to objects in view during saccades, ouranalysis is of interactions between objects seen onsuccessive fixations. It has become increasingly clearover the years that the degree of suppression isdependent on multiple stimulus dimensions. Specifical-ly relevant in the present experiments, it is important tonote that there is little or no saccadic suppression at thespatial frequency (0.8 c/8) used in our study (Burr et al.,1994). Finally, the fact that we observe significant biasat short Gabor 2 times even with real saccades suggeststhat a stimulus on one fixation can influence perceptionon the next fixation despite some suppression of stimuliviewed during the saccade. Our data suggest that ittakes a significant portion of each new fixation periodbefore the influence of the previous stimulus is lost.

It is not known by what neural mechanism(s) thevisual system is able to simultaneously parse informa-tion from distinct fixations and create a sense ofperceptual stability that spans saccades. Receptive fieldremapping driven by corollary discharge has beenproposed as a mechanism that might underlie visualstability (Duhamel et al., 1992; Melcher & Colby, 2008;Wurtz, 2008), though recent studies have raisedquestions about the effect (Cavanagh, Hunt, Afraz, &Rolfs, 2010; Churan et al., 2011). In order to parsevisual input, a reliable link between a saccade and theneural activity associated with a new fixation is desired.We propose that a corollary discharge signal may playa significant role in tightening this temporal relation-ship. Clearly, further physiological research will beneeded to pin down this hypothesis and the connectionto the suggestion by others that there are dual spacerepresentations, one disrupted by saccades and theother not (Burr, Morrone, & Ross, 2001; Ross & Ma-Wyatt, 2004).

There are two routes by which eye movements mightalter visual processing. One possibility is that feedbackfrom proprioceptors in the extraocular muscles influ-ences vision (Sherrington, 1918). Neural activityevoked by activation of proprioceptors has beenrecorded in Area 17 of anesthetized cats (Buisseret &Maffei, 1977) and in the nonhuman primate thalamus(Tanaka, 2007) and somatosensory cortex (Wang,Zhang, Cohen, & Goldberg, 2007; Xu, Wang, Peck,& Goldberg, 2011). However, the slow timecourse ofproprioceptive feedback (Buisseret & Maffei, 1977;Wang et al., 2007; Wurtz, 2008) suggests that this is not



the basis for the rapid reset that occurs just after asaccade. The alternative to proprioception is corollarydischarge, a copy of the motor command used to movethe eye. Neural activity correlated with saccades hasbeen recorded in many brain areas with a variety oftechniques (e.g., Bodis-Wollner et al., 2002; Green,1957; Purpura et al., 2003) and there are numerouspaths by which corollary discharge information mayreach the cerebral cortex (Sommer & Wurtz, 2004a,2004b, 2008b) Recently, one circuit for corollarydischarge has been demonstrated and there is signifi-cant evidence that corollary discharge rather thanproprioception provides eye position signals used inplanning saccades (Richmond & Wurtz, 1980; Sommer& Wurtz, 2008; Wurtz, 2008). We hypothesize thatvisual cortical areas responsible for perception usecorollary discharge as an indicator of new fixations sothat the temporal continuum of neural activity can beparsed into perceptual epochs associated with distinctfixations. The fact that bias in our simulated saccadeexperiments decreases at longer Gabor 2 times showsthat parsing can occur without saccades, a pointconsistent with experiments using flashed stimuli.However, our data suggest that parsing visual signalsis faster when the eyes move, presumably an increase inefficiency that takes advantage of the corollarydischarge signals. Because perception must lead tobehavioral decisions in very short periods of time, rapidresponses in the visual system are highly significant(Stanford et al., 2010; Thorpe et al., 1996).

Conclusions

An orientation discrimination task was used toinvestigate a possible role of saccades in the resettingof visual analysis on each fixation. Subjects saw twotilted Gabor stimuli separated by a saccade anddiscriminated the orientation of the second. The resultsshow that for a short period of time the tilt of thesecond stimulus is significantly influenced by the tilt ofthe first. This indicates that perception is not immedi-ately reset on each new fixation. A second experimentwas conducted in which visual stimulation was nearlyidentical to the saccade experiment, but subjects heldfixation while the saccade was simulated. The degree towhich the first stimulus biased the perceived tilt of thesecond stimulus was much greater with stimulatedsaccades. We propose that in the natural situation withsaccades there is less trans-saccadic bias because the eyemovement is being used to reset analysis on the newfixation. The most likely candidate for the signalinvolved in resetting perception is a corollary dischargerelated to the saccade.

Acknowledgments

We thank Aaron Gregoire, Theresa Lii, and DavidFreestone for technical assistance. Dar Meshi wassupported by a NIMH postdoctoral training grant(T32-MH019118) and an award from Brown Univer-sity’s Center for Vision Research.

Commercial relationships: none.Corresponding author: Michael A. Paradiso.Email: [email protected]: Department of Neuroscience, Brown Univer-sity, Providence, RI, USA.

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eye movements reset visual perception · waves were ﬁrst reported over 50 years ago (evans,...

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