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Proc Natl Acad Sci U S A
Proc Natl Acad Sci U S A
PNAS
Proceedings of the National Academy of Sciences of the United States of America
0027-8424
1091-6490
National Academy of Sciences

39226351
202408067
10.1073/pnas.2408067121
brief-reportBrief Reportpsych-socPsychological and Cognitive Sciences431
524
Social Sciences
Psychological and Cognitive Sciences
Brief ReportDifferent temporal dynamics of foveal and peripheral visual processing during fixation
de la Malla Cristina c.delamalla@ub.edu
a 1 https://orcid.org/0000-0003-4605-9166

Poletti Martina b c d https://orcid.org/0000-0002-4773-8745

aVision and Control of Action Group, Department of Cognition, Development and Psychology of Education, Institut de Neurociències, Universitat de Barcelona, Barcelona, Catalonia 08035, Spain
bDepartment of Brain and Cognitive Sciences, University of Rochester, Rochester, NY 14627
cDepartment of Neuroscience, University of Rochester, Rochester, NY 14642
dCenter for Visual Science, University of Rochester, Rochester, NY 14627-0270
1To whom correspondence may be addressed. Email: c.delamalla@ub.edu.
Edited by Michael Goldberg, Columbia University, New York, NY; received April 23, 2024; accepted August 6, 2024

3 9 2024
10 9 2024
3 9 2024
121 37 e240806712123 4 2024
06 8 2024
Copyright © 2024 the Author(s). Published by PNAS.
2024
https://creativecommons.org/licenses/by-nc-nd/4.0/ This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

Humans explore visual scenes by alternating short fixations with saccades directing the fovea to points of interest. During fixation, the visual system not only examines the foveal stimulus at high resolution, but it also processes the extrafoveal input to plan the next saccade. Although foveal analysis and peripheral selection occur in parallel, little is known about the temporal dynamics of foveal and peripheral processing upon saccade landing, during fixation. Here we investigate whether the ability to localize changes across the visual field differs depending on when the change occurs during fixation, and on whether the change localization involves foveal, extrafoveal processing, or both. Our findings reveal that the ability to localize changes in peripheral areas of the visual field improves as a function of time after fixation onset, whereas localization accuracy for foveal stimuli remains approximately constant. Importantly, this pattern holds regardless of whether individuals monitor only foveal or peripheral stimuli, or both simultaneously. Altogether, these results show that the visual system is more attuned to the foveal input early on during fixation, whereas change localization for peripheral stimuli progressively improves throughout fixation, possibly as a consequence of an increased readiness to plan the next saccade.

temporal dynamics
peripheral processing
foveal processing
fixation
Ministerio de Ciencia, Innovación y Universidades (MCIU) 100014440 PID2020-116400GA-I00 Cristina De la Malla NIH EY029788-01 Martina Poletti
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pmcPicture yourself driving in a busy street. Skilled drivers generally perform this task effortlessly, but at each fixation the visual system not only focuses on what lies at the center of gaze (e.g., a car, a traffic light, or a pedestrian) but also monitors what happens across the rest of the visual field. Potential dangers can emerge from various locations at any given moment and, to react properly, localizing them accurately is essential.

Although previous work has shown that processing of foveal and peripheral stimuli proceeds in parallel (1, 2), there may be moments during fixation in which the visual system is more attuned to processing foveal vs. peripheral stimulation or vice-versa. Here we posit that the visual system is more attuned to foveal stimulation early on during fixation, whereas later on, when planning the next saccade usually becomes more pressing, it is more receptive to stimulation in the visual periphery. To address this issue, we examined humans’ ability to localize brief orientation changes across the visual field during the course of fixation immediately following a saccade. In line with our expectation, our findings reveal an intrinsic advantage in processing foveal stimuli early on during fixation.

Results

Subjects (N = 8) performed a change localization task. Each trial started with subjects maintaining fixation on a marker presented in the lower part of the screen. After a few milliseconds, subjects were prompted to make a saccade toward a central fixation marker, and maintain their gaze steady until the trial ended. The central marker was surrounded by four vertical bars located either all in the fovea or all in the periphery (0.3° and 9° of eccentricity, respectively) or two in each region, requiring simultaneous monitoring of both areas (Fig. 1). Peripheral stimuli were enlarged to compensate for cortical magnification (3) and ensure comparable visual acuity (4). To mimic natural viewing conditions, the bars were shown throughout the trial, before and after saccade onset. To avoid unnatural fading due to the reduced retinal motion caused by head stabilization (5), especially in the periphery, a small jitter was added to each bar. Upon saccade landing, one of the four bars briefly (50 ms) changed orientation. The degree of orientation change was fixed for each stimulus and subject, and it was chosen to yield 79% of correct localizations when the change occurred ~490 ms after fixation onset. At the end of each trial subjects reported the location of the stimulus that changed orientation (see SI Appendix for details). Importantly, this task avoided the burden of a dual task (1); subjects always monitored the same number of items, focusing solely on localizing orientation changes regardless of stimulus location (fovea, periphery, or both).

Fig. 1. Experimental paradigm. In the illustrated condition, targets were presented both foveally and peripherally. The probability of a stimulus changing in the periphery or in the fovea was the same, and both regions were monitored simultaneously. In the other conditions, all four bars appeared either in the fovea or in the periphery. See SI Appendix for details.

Our results show that the ability to correctly localize orientation changes depended both on the time and the location of the changes. When all the stimuli were displayed in the fovea (Fig. 2 A and B, Left panels), performance was statistically comparable when the changes happened 100 to 250 ms after fixation onset and when they happened 750 to 900 ms after fixation onset (68.7%, SD = 14 vs. 75.0%, SD = 15; post hoc using the Benjamini–Hochberg method to control for multiple comparisons: t-ratio = −2.00, P = 0.13). Instead, when stimuli were displayed in the periphery, performance improved over time, from 55% (SD = 15) when the changes occurred soon after fixation started (100 to 250 ms) to 76.7% (SD = 5) at 750 to 900 ms (t-ratio = −6.91, P < 0.001). These results indicate that early on during fixation there is an advantage in localizing changes in the foveal vs peripheral visual field (t-ratio = 2.98, P = 0.03). Yet, this advantage disappears when changes occur later on during fixation (t-ratio = −0.38, P = 0.81).

Fig. 2. Results. (A) Mean percentage of correct responses (sliding window of 100 ms) across subjects as a function of when the orientation change occurred with respect to fixation onset. Error bars are SEM. Performance during selective monitoring of foveal or peripheral stimuli (Left panel) and during simultaneous monitoring of both areas (Right panel). (B) Average performance across subjects for changes occurring 100 to 250 ms, 440 to 540 ms, and 750 to 900 ms after fixation onset. Error bars are SEM. Dots represent individual subjects’ performance. Colors as in A.

Similarly, when monitoring foveal and peripheral stimuli simultaneously (Fig. 2 A and B, Right panels), foveal performance remained constant throughout fixation (72.2%, SD = 17 vs. 72%, SD = 14 for changes occurring 100 to 250 ms and 750 to 900 ms after fixation onset; t-ratio = −0.01, P = 0.99). In the periphery, performance largely improved over time (60.8%, SD = 11 vs. 79.5%, SD = 8; t-ratio = −5.912, P < 0.001) reaching levels comparable to performance when changes occurred at the foveal level (t-ratio = −1.61, P = 0.26).

Discussion

Our findings reveal distinct temporal dynamics for foveal and peripheral visual processing during fixation. Upon fixation onset, there is an advantage for processing foveal vs extrafoveal stimuli. While performance for foveal stimuli remained relatively constant as fixation progressed, a gradual improvement was observed in localizing peripheral changes. This improvement unfolded within the first 250 to 350 ms of fixation, i.e., within the timeframe of typical fixations duration (6), showing significant variation in the ability to localize peripheral changes over time even during brief fixations. Observers remained engaged in the task well after this period, so this trend was not due to saccade planning and execution. Yet, it may well be related to the typical fixation-saccade cycle and be so ingrained in the visual system that it unfolds even in the absence of an impending saccade. Further, this modus operandi seems to be obligatory as the same temporal course was observed regardless of whether the visual system monitored only foveal or peripheral stimuli or both simultaneously.

Attention research debates the ability to attend to multiple spatial locations concurrently (7, 8). Foveal tasks hinder peripheral processing (9, 10), and attempting to detect briefly flashed foveal targets while trying to simultaneously localize peripheral ones impairs both foveal detection and peripheral localization (11). Interestingly, we do not observe a compromise between foveal and peripheral performance, suggesting a simultaneous and independent monitoring of both areas, rather than a trade-off of attentional resources. Possibly, compared to a combined task, localization of changes is a rather parallel and automatic operation that does not require a significant amount of attentional resources, as the moving targets almost pop out from the display.

Our paradigm differs from previous work in that it examines the temporal evolution of visual perception during fixation rather than the overall subjects’ performance for foveal and peripheral stimuli. Stimuli were continuously presented throughout the trial, and brought into the fovea via a saccade, which may allow processing the visual scene more naturally than when stimuli are flashed at fixation. Importantly, by measuring orientation change thresholds at each tested location, correcting for cortical magnification, and using the same number of stimuli in the fovea and in the periphery, and by not requiring subjects to perform a dual task, our paradigm ensured comparable task difficulty for foveal and peripheral stimuli, which was not always the case in previous work (e.g., ref. 11). It remains an open question whether temporal dynamics for foveal and peripheral processing differ in the same fashion for other visual functions (e.g., contrast sensitivity or acuity). Ultimately, these findings are consistent with the idea that later on during fixation the visuomotor system is more likely to execute a saccade to move the foveola toward its next target, and as a result, sensitivity increases for peripheral stimuli that can potentially become saccadic targets.

Materials and Methods

Details on methods and analyses are available as SI Appendix. The data to reproduce the figures are accessible through OSF.

Subjects provided written informed consent before participating. The study was part of a project approved by the Ethics Committee of the University of Barcelona (IRB00003099).

Supplementary Material

Appendix 01 (PDF)

We thank Manel Moreno and Pau Abellanet for their help in programming and data collection, respectively. This work was supported by Grants PID2020-116400GA-I00 and PID2023-150883NB-I00 funded by MICIU/AEI/10.13039/501100011033 to C.d.l.M. and NIH R01 EY029788-01 and funding from META Inc. to M.P., and NIH P30 EY001319.

Author contributions

C.d.l.M. and M.P. designed research, C.d.l.M. performed research; C.d.l.M. analyzed data; C.d.l.M. and M.P. acquired funding; and C.d.l.M. and M.P. wrote the paper.

Competing interests

The authors declare no competing interest.

Data, Materials, and Software Availability

Anonymized (R data frame) data have been deposited in OSF (https://osf.io/7n5hd/) (12).

Supporting Information
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