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N.S. and research; data; performed M.P. analyzed M.P. and N.S. research; designed M.P. contributions: Author foveal fixation. of of discrimination locus preferred in visual the nonuniformities from facilitate away reducing and stimuli in modu- (21) role these vision crucial present, foveal a If play locations. could peripheral lations more selec- rather at itself, can just foveola the than attention within the perception of visual raises modulate shifts finding tively This premicrosaccadic (25). away that fixation arcmin of 20 possibility than locus less preferred are the within that from landing locations deployed retinal selectively their to be foveola from the inde- can attention, microsaccades, far covert of that very pendently shown stimuli has research with recent positions, only examined been visual the in an periphery. exerted associated primarily at are effects direction. preparation presented the microsaccade microsaccade that with are suggests leads the therefore, that evidence, preparation with stimuli Current congruent microsaccade of location (24); enhancement eccentric level neural a neural a to the the of process- by at peripheral presence and targeted ing the preparation location revealed microsaccade between findings retinal link locations Other the at (23). from perception microsaccade away visual existence farther of the much shown changes have premicrosaccadic findings to of Recent task-driven strategies (22). enable similar saccades following to stimulus larger 21) foveal (20, the foveola of exploration the the shift within They object controlled. fixated precisely are saccades miniature these owo orsodnemyb drse.Eal martina Email: addressed. be may correspondence whom To edu. ieehneeto ihaut iinocr tistarget its at occurs in selec- vision and surprisingly high-acuity space location. a in of onset both enhancement microsaccade way tive before peculiar foveal Right a fixation in time. during microsaccade modulated that by is show affected vision findings is Our vision foveal preparation. how examined and less we been whether eyetracking has high-precision occur. microsaccades Using to and investigated. attention continue between boundaries, fix- link foveal is The the the target within maintaining the object once saccades ated Yet, before tiny fovea. target execution, microsaccades, high-resolution saccade foveated, the saccade the in of of lands processing it ahead the shifts to contributing briefly Attention atten- and movements tion. eye between exists relationship tight A Significance hl h ecpulcneune fmcoacdshave microsaccades of consequences perceptual the While y . y raieCmosAttribution-NonCommercial- Commons Creative . y https://www.pnas.org/lookup/suppl/ NSLts Articles Latest PNAS [email protected]. | f6 of 1

PSYCHOLOGICAL AND COGNITIVE SCIENCES Addressing these issues is important to better understand the documenting the accuracy of these small eye movements when oculomotor contribution to foveal vision, as well as the spa- produced voluntarily in response to a central cue. Therefore, we tiotemporal dynamics of during fixation. Here first ensured that subjects were capable of precisely shifting their we investigate whether and how visual acuity at selected foveal gaze to the nearby stimuli based on the saccade cue. To this end, locations changes before the onset of microsaccades. we examined the average landing error of microsaccades, i.e., the distance between the microsaccade landing position and the Results stimulus location as indicated by the saccade cue. Fig. 2A and SI To investigate whether premicrosaccadic attentional shifts mod- Appendix, Fig. S1 show the average two-dimensional (2D) distri- ulate visual perception in the foveola we recorded eye move- bution of microsaccade landing positions for trials in which the ments at high resolution while subjects performed a fine spatial saccade cue pointed to the left and to the right location, respec- vision task. Subjects were asked to discriminate the orienta- tively. The average SD of the landing error was 6.40 ± 1.80 and tion of a high-acuity stimulus briefly presented before the onset 4.10 ± 1.20 on the x and y axes for leftward microsaccades and of a microsaccade (Fig. 1 A–C ). They were instructed to fix- 6.20 ± 1.70 and 3.50 ± 10 on the x and y axes for rightward ate on a marker and shift their gaze as soon as a saccade cue microsaccades (the average landing location was –180 ± 3.80 on appeared at the marker position indicating where to look. Based x, −0.10 ± 1.70 on y and 17.90 ± 2.20 on x, 0.60 ± 1.40 on y for left- on the direction of this signal, gaze was shifted toward one of ward and rightward microsaccades, respectively). Although with two foveal locations only 200 away. Microsaccades had to be some variability (SI Appendix, Fig. S1), all subjects were able to performed to precisely shift gaze. Soon after the saccade sig- shift their gaze with remarkable precision based on the direction nal, while the microsaccade was being prepared, two high-acuity indicated by the cue. stimuli were briefly presented, one at each location. After the Executing precise microsaccades was not the only task require- gaze shifted, a response cue appeared, and subjects reported the ment. Microsaccades also had to be performed in a timely orientation of the stimulus that was previously presented at that manner soon after the presentation of the saccade signal. It is location. known that microsaccades are characterized by longer latencies Because of the way the experiment was designed, microsac- compared to saccades (27). Depending on the task, latencies of cades performed in a trial could either land at the position microsaccades can be up to 200 ms slower than those of sac- indicated by the response cue (congruent trials) or land at cades (28, 29). In our task, the average latency of microsaccades, the opposite location (incongruent trials). The experiment also measured as the time between the saccade signal onset and the included a neutral condition. In this condition, the saccade sig- onset of the microsaccade, was 457 ± 112 ms (Fig. 2B and SI nal was not presented, and subjects maintained fixation without Appendix, Fig. S2). These values are larger than those reported performing a microsaccade (Fig. 1B). Congruent, incongruent, in the literature, most likely because microsaccades in this task and neutral trials had the same probability of occurring in the were elicited by a central cue rather than by a stimulus pre- task; i.e., the saccade cue was independent of the response sented at a given foveal eccentricity or by a step of the fixation cue location. marker. Furthermore, the central fixation marker was not turned Shifting the gaze in minute amounts on command may not off, but remained visible throughout the trial, further delaying be as simple as executing a saccade toward a peripheral target. the gaze shift (30). To ensure that microsaccades were performed Early work has shown that humans are capable of generating in a timely manner, we selected only the trials with the faster microsaccades as small as 30 in response to small steps of a microsaccade latencies for our main analysis. This selection was fixation marker (26). However, there are no previous reports based on each subject’s latency distribution (SI Appendix, Fig. S2;

A 20’

Enlarged display

Fixation Saccade Cue Target Blank Interval Response Cue (Variable Time) (100 ms) (100 ms) (Saccade Execution) (100 ms) (600 ms)

B C Saccade cue Target Response Cue Center of gaze Cued location Saccade cue 20

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Fig. 1. Methods. (A) Experimental protocol. Subjects maintain fixation on a central marker surrounded by two squares (50 × 50 in size) 200 away. After a brief period of fixation, a central saccade cue appears, instructing the subject to shift the gaze as soon as possible to one of the two squares. Immediately after the saccade signal, two stimuli, bars tilted ±45◦, are briefly presented (100 ms), one in each square. After a blank interval (600 ms), a response cue appears. Subjects are instructed to report the orientation of the stimulus previously presented at the cued location. The direction of the saccade cue is not predictive of the response cue location. (B) Microsaccades are prepared during the brief interval between the saccade cue onset and the target offset and are executed right after the target is turned off. In congruent trials, microsaccades land on the previously cued location. In incongruent trials, microsaccades land on the opposite side of the cued location. In neutral trials, the saccade cue is replaced by central arrows pointing in both directions, and subjects maintain fixation throughout the trial. All types of trials had the same probability of occurrence. (C) An example of a typical trace during the course of a trial.

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Fig. r meddi ope iulevrnetweeseveral they where conditions environment natural visual complex in a isolation; in are in embedded targets are Saccade viewed of distractors. not down of impact impor- slowing generally the the The highlights reducing also here. of trials tance reported incongruent in effect times main respon- processing was the longer preparation for microsaccade i.e., sible further that tradeoff; accuracy, idea discrimination speed–accuracy the increase supporting of not Crucially, result did tri- times criteria. the congruent reaction selection in not performance trial was higher the the als that by shows finding driven this not was times incongruent, vs. congruent gruent, 9.9, tests, hoc = post P F(4,20) HSD ANOVA Tukey’s respectively, 0.001; trials, neutral and (309 longer also 437 were times reaction response manual of ahead well opposite starts target show the execution. microsaccade microsaccade results at the the These of vision impaired. processing spatial substantially that fine was target location contrary, its at foveal the vision immedi- spatial On the fine enhancing location. had selectively microsaccade of a effect ate Preparing S3). Fig. Appendix, incongruent, con- vs. tests, neutral 0.006; hoc post incongruent, 9.88, (HSD) vs. = gruent significance F(4,20) honest ANOVA Tukey’s (2.07 respectively, 0.0001; trials trials, neutral neutral and and incongruent to 0.69, compared trials ent vrg aulrsos ie.Errbr r E.Atrssmr ttsial infiatdfeec (*P difference significant statistically a mark Asterisks SEM. are bars Error times. response manual Average ) u aaso htteaiiyt iciiaeteorientation the discriminate to ability the that show data Our o nywspromnelwri h nogun trials; incongruent the in lower performance was only Not < ± 3 s n 338 and ms, ±133 .01 ogun s neutral, vs. congruent 0.0001; 0.83 0 ms. 105 vrg (N Average (A) preparation. microsaccade of effects Perceptual vrg Dnraie irscaelnigpsto itiuinpoaiiyfrtil nwihtescaecue saccade the which in trials for probability distribution position landing microsaccade normalized 2D Average (A) task. the in Microsaccades P ± .0;Fg 3C Fig. 0.004; = and 0.41, 1.28 P BC AB 0 s o ogun,incongruent, congruent, for ms, ±100 < ± .01 ogun s neutral, vs. congruent 0.0001; .Sc ifrnei reaction in difference a Such ). −0.7, 0.49 P .1 i.3 Fig. 0.21; = d o ogun,incongruent, congruent, for P −0.4, 0 a nacdi congru- in enhanced was , .;nurlv.incon- vs. neutral 0.8; = .,0.8, −0.6, A and .,1.7). −0.8, 1 ms, ±118 B and P P P )sniiiy(d sensitivity 6) = SI = < < ± elyd(13) ntepeetpooo,teitra between interval the protocol, present vs. the In (congruent (31–34). cue deployed landed response it the not by or indicated trials). whether incongruent location stimulus and the the trials) con- at vs. after incongruent (neutral occurred and only microsaccade gruent a behavior not or oculomotor whether offset, the conditions presenta- in trials, stimulus across differed during comparable was Since, stimulation S4 ). retinal saccade tion, Fig. rightward , Appendix and leftward (SI both fixation signals for and the ( 4) Fig. and conditions respectively; gaze all of in and similar center average was the the marker marker analysis between data fixation for distance in selected central retinal trials trials the the In only from stimuli. reti- acuity selected gaze similar we below of at remained conditions distance displayed Therefore, the all always drift. which in were ocular eccentricities stimuli to arcminutes nal due that many marker ensure shift central to may cue. the fixation saccade from the during away before position occurred gaze microsaccade Still, no tri- which only occurred in selected we Because als normally Furthermore, stimuli. presentation. microsaccades the stimuli the dynamics, of after onset temporal the their preceding of interval the in sensitivity tion where fixation of falling locus target highest. preferred saccade is the small in the result a may outside even accu- amplitude when in and for stimuli, error the important spatial small precision fine particularly has the toward be directed could likely improving and microsaccades This in goal, target microsaccades. saccade of instrumental saccade the racy be to the may sensitivity than increasing it process- further other the of stimuli down effect slowing of Therefore, ing present. are distractors noeoscvr teto eursa es 0 st be to ms 300 least at requires attention covert Endogenous posi- gaze of changes to due not are here reported results The −0.4 0 0 ndfeettiltps efrac sas hw o rasin trials for shown also is Performance types. trial different in ) ± 0. 8 0 o ogun,icnret n eta trials, neutral and incongruent, congruent, for 10 0 aciue)utlteofe ftehigh- the of offset the until (arcminutes) < 5 ue’ othctest). hoc post Tukey’s 0.05, −0.5 NSLts Articles Latest PNAS 0 ± 1. 1 0 , −0.5 | 0 ± f6 of 3 1 0 ,

PSYCHOLOGICAL AND COGNITIVE SCIENCES Fig. 4. Gaze position during stimuli presentation. Shown is average distribution of horizontal gaze position when stimuli were displayed in the three conditions tested. Red dashed lines indicate the locations of the stimuli. Solid lines represent the average of the distributions.

the onset of the saccade cue and stimuli offset was of only 200 ms, decreases with time. Although at a different spatial and temporal suggesting that covert voluntary attention was not responsible for scale, these findings echo what happens in the visual periphery the reported effect. To determine whether these spatially selec- during saccade preparation (4). Notably, these findings are not tive modulations of foveal vision were caused by microsaccade what we would expect based on the current evidence, accord- preparation rather than covert shifts of attention, we exam- ing to which the effects of microsaccade execution/preparation ined subjects’ performance in the congruent and incongruent are associated with peripheral modulations of sensitivity/neural trials in which microsaccades did not occur. Our findings show activity and peripheral allocation of covert attention (23, 24). that on average, the difference in performance (∆d 0) between Differently, here we show that, in the presence of complex these two types of trials was minimal and statistically not dif- foveal stimuli, a condition more akin to natural viewing, there ferent from zero in the absence of microsaccades (1.46 ± 0.6 are significant perceptual consequences of microsaccades at the and 1.49 ± 0.5 for congruent and incongruent trials, respec- foveal scale. tively; P = 0.87, Tukey’s HSD post hoc test, Fig. 3A). SI The outcome of our study prompts the question, what is the Appendix, Fig. S3 shows that this null effect was the result of function of such a refined premicrosaccadic attention mecha- some observers exhibiting a higher and others a lower perfor- nism? One possibility is that it connects pre- and postmicrosac- mance in the congruent compared to the incongruent trials. For cadic percepts, in a similar way to how presaccadic attention the two observers showing a higher performance in the con- operates at a larger scale. Presaccadic attention is, indeed, gruent condition, the size of the effect was about half of that believed to act as a bridge between the lower-resolution pre- when a microsaccade was executed. A residual effect in the saccadic and the high-resolution postsaccadic stimulation (9, absence of microsaccades may reflect either an early influence 10, 14). At the foveal scale, the differences between the pre- of covert attention or a planned and then aborted microsaccade. and postmicrosaccadic stimulation are not as drastic as between On the other hand, a lower performance in congruent compared the fovea and the visual periphery. Yet, fine pattern vision to incongruent trials for other subjects may be the result of an is not uniform across the foveola and it begins to deterio- 0 active suppression of microsaccades, as in most of these trials rate already 10 away from the preferred locus of fixation (21). subjects were explicitly instructed to maintain fixation. There- Hence, enhancing visual discrimination at the microsaccade tar- fore, the difference between congruent and incongruent trials get location may effectively render the percept at that location seen in the task was primarily the consequence of microsaccade more homogenous with the percept at the preferred locus of preparation. fixation. The reported changes in visual perception preceding microsac- cade execution were also modulated by the onset time of the microsaccade. If microsaccades with longer latencies were included in the analysis, a stronger effect was observed when the target appeared 233 ± 72 ms before the onset of the microsaccade; the intensity of the effect then progressively decreased as the temporal interval between the target onset and the microsaccade onset increased (1.2 ± 0.42, 0.52 ± 0.4, shortest vs. longest delay; P = 0.02, Tukey’s post hoc test; Fig. 5). Although individual differences were present, all sub- jects showed the same trend (SI Appendix, Fig. S5). These results indicate that closer to the onset time of a microsac- cade, the modulation of visual perception within the foveola is stronger. Discussion In this study we examined modulations of visual perception within the foveola during the time of microsaccade prepara- tion. This was possible due to high-precision and a gaze-contingent display system allowing for accurate gaze local- ization, capabilities that are beyond what can be achieved with standard eye-tracking techniques. Our findings reveal that during fixation, visual perception at the foveal scale is constantly being reshaped in a spatially selective way before the onset of microsac- cades. More specifically, microsaccade preparation leads to an Fig. 5. Temporal course of the effect. Shown is the difference in perfor- enhancement of fine spatial vision at the microsaccade target mance between congruent and incongruent trials (∆d0) as a function of location, as well as a concomitant reduction of fine spatial vision time relative to saccade onset (red line). Dashed lines indicate the average at the nontargeted location, even if these locations are just a difference between fixation congruent and incongruent trials in which no few arcminutes away from each other. This effect is strongest microsaccades were performed. Error bars are SEM. The asterisk marks a up to about 200 ms before the onset of the microsaccade and statistically significant difference (*P < 0.05, Tukey’s post hoc test).

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PSYCHOLOGICAL AND COGNITIVE SCIENCES direction and the response cue direction matched and incongruent if they of tracks (0.2%) were discarded. Only congruent and incongruent trials in did not match. which only one microsaccade occurred in the interval between target off- set and response cue onset were used for analysis. In all conditions, trials Data Analysis. Recorded eye movement traces were segmented into sep- with microsaccades occurring in an 80-ms period preceding the saccade sig- arate periods of drift and saccades. Classification of eye movements was nal onset were discarded. Comparisons between conditions across observers performed automatically and then validated by trained laboratory person- were tested using d0 tests. On average, performance was evaluated over nel with extensive experience in classifying eye movements. Periods of blinks more than 400 trials per observer. d0 was used as a measure of the sen- were automatically detected by the DPI eye tracker and removed from sitivity index based on subjects’ performance in the visual discrimination data analysis. Only trials with optimal, uninterrupted tracking, in which task (41). the fourth Purkinje image was never eclipsed by the pupil margin, were 0 selected for data analysis. Eye movements with minimal amplitude of 3 and Data Availability. The data necessary to generate all of the figures (contain- ◦ a peak velocity higher than 3 /s were selected as saccadic events. Saccades ing data) in the main text and the matlab scripts used to produce these ◦ 0 with an amplitude of less than 0.5 (30 ) were defined as microsaccades. figures have been deposited in the Open Science Framework repository Consecutive events closer than 15 ms were merged together into a single (https://osf.io/hvjy7/). saccade to automatically exclude postsaccadic overshoots. Saccade ampli- tude was defined as the vector connecting the point where the speed ◦ ACKNOWLEDGMENTS. We thank Michele Rucci and Marisa Carrasco for of the gaze shift grew greater than 3 /s (saccade onset) and the point helpful comments and discussions. This work was supported by National Sci- ◦ where it became less than 3 /s (saccade offset). Periods that were not clas- ence Foundation Grant BCS-1534932 (to M.P.) and by the National Institutes sified as saccades or blinks were labeled as drifts. Trials with blinks/loss of Health Grant R01EY029788-01 (to M.P.).

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