Temporal dynamics of peri-microsaccadic modulations within the foveola

Reviewer #1 (Public review):

Summary:

Using high-precision eyetracking, the authors measure foveolar sensitivity modulations before, during, and after instructed microsaccades to a centrally cued orientation stimulus.

Strengths:

The article is clearly written, and the stimulus presentation method is sophisticated and well-established. The data provide interesting insights that will be useful for comparisons between trans-saccadic and trans-microsaccadic sensitivity modulations.

Weaknesses:

Nonetheless, I have major concerns regarding the interpretation of the measured time courses (in particular, inconsistencies in distinguishing enhancement from suppression), the attempt to disentangle these effects from endogenous attention shifts, and the overstatement of the findings' novelty.

(1) Overstatement of novelty

The authors motivate their study by stating that "the temporal dynamics of these pre-microsaccadic modulations remain unknown" (l. 55-56). However, Shelchkova & Poletti (2020) already report a microsaccade-aligned sensitivity time course. I understand that the present study uses shorter target durations and thus provides a more resolved estimate. Nonetheless, a fairer characterization of the study's novelty would be that observers' discrimination performance is continuously measured across the pre-, intra-, and post-movement interval, within the same observers and experimental design. Relatedly, the authors state that it is unclear whether pre-microsaccadic sensitivity modulations reflect "suppression at the non-foveated location, enhancement at the microsaccade target, or both" (l. 70). Guzhang et al. (2024) examined the spatial spread of pre-microsaccadic sensitivity modulations by measuring performance at the PRL, the movement target, and several other equidistant locations. They report that "whereas fine spatial vision is enhanced at the microsaccade goal location, it drops at the very center of gaze". The current authors' reasoning seems to be that performances at locations that are neither the target nor the PRL may behave differently. Why would that be the case? If my understanding is correct, I would recommend incorporating these clarifications into the motivation paragraph, so that readers less familiar with the literature do not overestimate the novelty of the findings. Moreover, and related to point 3, I am unsure if the current analyses provide decisive evidence to distinguish enhancement from suppression, as claimed by the authors.

(2) Distinction from endogenous attention

To "rule out the possible influence of covert attention" (l. 232), the authors compute a cue-aligned in addition to the movement-aligned performance time course. A difference in alignment cannot rule out the influence of a certain mechanism; it can only dilute it. Just like endogenous attention may contribute to the movement-aligned time course, movement preparation will necessarily contribute to the cue-aligned time course, since these timelines are intrinsically correlated: as the trial progresses, observers will be in later and later stages of saccade preparation. For this and several additional reasons, an effect in the cue-aligned time course is in fact expected-and, in my view, clearly present (see below). As the authors themselves note, endogenous attention has been shown to operate within the foveola and should therefore be engaged in the present experiment in addition to movement-related attentional shifts (unless the authors believe that specific design features, e.g., stimulus timing, preclude its involvement?). Regardless of the theoretical considerations, the empirical data show a pronounced, near-linear increase in performance at the target location, with d′ doubling from approximately 1 to 2. Although the interaction between condition and time does not reach significance (p = 0.09), this result should not be taken as conclusive evidence against a plausible and perhaps expected contribution of endogenous attention. I suggest an additional analysis that could more directly address these issues. In previous work (Rolfs & Carrasco, 2012; Kroell & Rolfs, 2025; see Figure 3), the relative contributions of cue-alinged influences and pre-saccadic attention were disentangled by reweighting each data point according to its position on both the cue-locked and saccade-locked timelines. Applied to the present study, the authors could compute, for each cue-to-target offset bin, its proportional contribution to each pre-movement time bin. Microsaccade-locked sensitivities could then be reweighted based on these proportions. As a result, each movement-locked time bin would contain equal contributions from all cue-locked time bins, effectively isolating the effect of microsaccade preparation.

(3) Interpretation and analysis of the time course

(3.1) Discrimination before microsaccade onset
In lines 151-153, the author state "While the enhancement at the target location did not reach significance relative to baseline, the impairment at the non-target location did", suggesting that pre-movement sensitivity advantages for information presented at the target location are due to a decrease in performance at the non-target location and not an enhancement at the target location per se. After analyzing the difference between the two locations, the authors state, "These results show that approximately 100 milliseconds before microsaccade onset, discrimination rapidly improved at the intended target location while decreasing at the non-target location." (l. 159-161). How is the statement that discrimination performance rapidly improved (which is repeated throughout the manuscript) justified by the results?

More generally, the authors may benefit from applying bootstrapping or permutation-based analyses to their data. Such approaches would, for example, allow direct comparisons between congruent and incongruent conditions at every individual time point in Figure 3B and may be more sensitive to temporally confined sensitivity variations while requiring fewer assumptions than analyses based on manually segregated temporal bins and aggregate measures. If enhancement at the target location does not reach significance even in these analyses, all corresponding statements should be removed throughout the manuscript. The term "enhancement" should then be rephrased as "detection advantage" or "relative performance benefit" to emphasize the contrast to enhancement effects classically associated with pre-saccadic attention shifts.

Relatedly, the authors state that pre-microsaccadic enhancement peaks around 70 ms before microsaccade onset, which is earlier than sensitivity enhancements preceding large-scale saccades that often increase monotonically up until movement onset. The authors suggest potential reasons for this in the Discussion, yet an additional one seems conceivable based on Figure 3B. Performances at both the cue-congruent and incongruent location decrease leading up to the movement, reaching values even below their early baselines around 100 ms and 25 ms before movement onset for the incongruent and congruent location, respectively. A spatially non-specific decline that drives sensitivities toward a common absolute minimum may thus dictate the time course of detection advantages. In other words, a spatially widespread decrease in foveolar sensitivity likely contributes to both "suppression" at the non-target location and the decrease in "enhancement" at the target location. If this general decrease is due to saccadic suppression, as the authors suggest, it appears to exert a much more pronounced influence on sensitivity modulations than it does before large-scale saccades (which is interesting). Are there other findings suggesting an increased magnitude of micro-saccadic (as compared to saccadic) suppression? Another potentially related phenomenon is the decrease in pre-saccadic foveal detection performances reported twice before (Hanning & Deubel, 2022; Kroell & Rolfs, 2022). It is possible that whatever mechanism triggers this decrease is engaged by the preparation of microsaccadic and saccadic motor programs alike. In any case, I would ask the authors to acknowledge this general decrease early on to clarify that any currently significant advantage for the target location relies on varied degrees of suppression, and not on true enhancement similar to pre-saccadic attention shifts.

Moreover, in Figure 3C, the final 25 ms before microsaccade onset are excluded from the aggregate measure, presumably since including this interval substantially reduces the effect size. Since the last 25 ms before movement onset is the interval most commonly associated with saccadic suppression, I think that this choice can be justified. Nonetheless, it should be mentioned explicitly in the main text. On a minor note, the authors state that "Performance (evaluated as percent of correct responses) was averaged within a 50 millisecond sliding window, advancing in 1 ms steps (with 24 ms overlap)". Why is the overlap not 49 ms?

(3.2) Discrimination during the microsaccade:
The authors state that "in the "during" trials the target must be presented during the peak speed of the microsaccade." Since the target was presented for 50 ms and the average microsaccade duration was around 60 ms, this implies that the intra-microsaccadic condition includes many trials in which the target overlapped with the pre- or post-movement fixation interval. Were there not enough trials to isolate purely intra-microsaccadic presentations? Are the results descriptively comparable?

(4) Additional analyses

Several additional analyses could strengthen the authors' conclusions. If there are enough trials in which observers erroneously saccaded to the uncued (i.e., wrong) location, these trials could experimentally isolate the influence of pre-microsaccadic attention, assuming that endogenous attention went to the cued location. In addition, the authors speculate whether differences in saccadic and microsaccadic movement latencies may underlie the differences in perceptual time courses. The latency distributions provided in the manuscript look sufficiently broad, such that intra-individual variation could be harnessed to explore this question. Do sensitivity time courses differ before microsaccades with shorter vs. longer latencies?

(5) Clarifications regarding the design

At 50 ms, the duration of the to-be discriminated stimulus, although shorter than in previous investigations, is still rather long. What is the reason for this? I would encourage the authors to state in the main text that the duration of the analyzed/plotted time bins is often shorter than the stimulus duration (i.e., there is some overlap between bins that likely introduces smoothing). In Figure 3A, it would be helpful to plot raw data points computed from non-overlapping bins on top of the moving-window estimates, to allow readers to assess the degree of smoothing and potential temporal delays introduced by this analysis. Moreover, I wonder whether the abrupt onset of the target unmasked by flickering noise masks might induce saccadic inhibition, which would manifest as a transient dip in saccade execution probability. The distributions shown in Figure 2B appear too smoothed or fitted to clearly reveal such a dip. How exactly are all distributions in the manuscript computed (e.g., binning, smoothing, fitting procedures)? Finally, on a minor note, explicitly stating on line 105 that two different orientations can be presented at the cued and non-cued location would help avoid potential confusion.

Reviewer #2 (Public review):

Summary and overall evaluation:

The authors assessed how visual discrimination of stimuli in the foveola changes before, during, and after small instructed eye movements (in the "micro" range). Consistent with (and advancing) related prior work, their main finding regards a pre-saccadic modulation of visual performance at the saccade target vs. the opposite location. This pre-saccadic modulation in foveal vision peaks ~70 ms prior to the instructed small saccade.

Strengths:

The study uses an impressive, technically advanced set-up and zooms in on peri-saccadic modulations in visual acuity at the micro scale. The findings build on related prior findings from the literature on smaller and larger eye movements and add temporal granularity over prior work from the same lab. The writing is easy to follow, and the figures are clear.

Weaknesses:

At the same time, the findings remain relatively empirical in nature and do not profoundly advance theoretical understanding beyond adding valuable granularity to existing knowledge. Relevant prior literature could be better introduced and acknowledged. In addition, there remain concerns regarding potential cue-driven attentional influences that may confound the reported effects (leaving the possibility that the reported effects may be related to cue-driven attention, rather than saccade planning/execution per se). There are also some issues regarding specific statistical inferences. I detail these points below.

Major Points:

(1) Novelty framing and introduction of relevant prior literature

At times, this study is introduced as if no prior study explored the time course of changes in visual perception surrounding small (micro) saccades. Yet, it appears that a prior study from the same lab, using a very similar task, already showed a time course (Figure 5 in Shelchkova & Poletti, 2020). While this study is discussed in the introduction, it is not mentioned that at least some pre-saccade time course was already reported there, albeit a more crude one than the one in the current article. Moreover, the 2013 study by Hafed also specifically looked at "peri-microsaccade modulation in visual perception" and also already showed a temporal modulation that peaked ~50 ms before microsaccade onset. I appreciate how the current study differs in a number of ways (focusing on visual acuity in the foveola), but I was nevertheless surprised to see the first reference to this relevant prior finding in the discussion (and without any elaboration). Though more recent, the same could be argued for the 2025 study by Bouhnik et al. on pre-microsaccade modulations in visual processing in V1, which, like the Hafed study, is first mentioned only in the discussion. Perhaps these studies could be introduced in the paragraph starting at line 48, or in the next paragraph, to do better justice to the existing literature on this topic when motivating the study. This would likely also help to better point out the major advances provided by the current study.

Relatedly, in Shelchkova & Poletti (PNAS, 2020), an apparently similar congruency effect on performance was reported >200 ms milliseconds before saccade onset, as evident from Fig 5 in that article. How should readers rhyme this with the current findings? Ideally, the authors would not only acknowledge that such a time course was already reported previously, but also discuss the discrepancies between these findings further: why may the performance effects appear much earlier in this prior study compared to in the current study, where the congruency effect emerges only ~100 ms prior to the instructed small saccade?

(2) Saccade- or cue-driven? (assumption that attention is unaltered in failed saccade trials)

Because the authors used a cue to instruct saccade direction, it remains a possibility that the reported modulations in visual performance may be driven directly by the spatial cue (cue-related attentional allocation), rather than the instructed small saccade per se. While the authors are clearly aware of this potential confound, questions remain regarding the convincingness of the presented control analyses. In my view, a more compelling control would require an additional experiment.

The central argument against a cue-locked (purely attentional) modulation is the absence of a performance modulation in so-called "failed" saccade trials. However, a key assumption here is that putative cue-driven attention was unaltered in these trials. This is never verified and, in my opinion, highly unlikely. Rather, trials with failed microsaccades could very well be the result of failing to process the cue in the first place (indeed, if the task is to make a saccade to the cue, failure to make a saccade equates failure to perform the task). In such trials, any putative cue-driven influences over spatial attention would also be expected to be substantially reduced. Accordingly, just because failed saccade trials show little performance modulation does not rule out cue-driven attention effects, because attention may also have "failed" in these failed saccade trials. The control for potential cue-driven attention effects would be more convincing if the authors included a condition with the same cues, where participants are simply not instructed to make any saccades to the cues. Unfortunately, such an experimental condition appears not to have been included here. The author may still consider adding such a control experiment.

Another argument against a cue-driven effect is that the authors found no interaction with time in the cue-locked data, whereas they did find such an interaction in the saccade-locked data. However, the lack of significance in the cue-locked data but significance in the saccade-locked data is not strong evidence against a cue-driven influence. Statistically, there is no direct comparison here, and more importantly, with longer delays, the cue-locked data may also start to show a dip (this could potentially be tested by the authors if they have enough trials available to extend their cue-locked analysis further in time). Indeed, exogenous attention, that may have been automatically evoked by the spatial cue, is known to be transient and to eventually even reverse after a brief initial facilitation (see e.g., Klein TiCS, 2000).

Finally, the authors consistently refer to "endogenous" attention (starting at line 221) when addressing potential cue-driven attention confounds. However, because the cue is not predictive, but is a spatial cue that differs in a bottom-up manner between left and right cues, "exogenous" attention is a more likely confound here in my view. Specifically, the spatial cue may automatically trigger attention in the direction of the target location it points to (and such exogenous effects would be expected even for unpredictive cues).

(3) Benefit and cost, or just cost?

Line 151 states that no statistically significant benefit for the saccade target was found compared to the neutral baseline. Yet, the claim throughout the article is distinct, such as in line 159: "These results show that approximately 100 milliseconds before microsaccade onset, discrimination rapidly improved at the intended target location". I do not question the robustness of the congruency effect, but the authors should be more careful when inferring "improved" perception at the target location because, as far as I could tell (as well as in the authors' own writing in line 151), this is not substantiated statistically when compared to the neutral baseline.

Related to this point, in Figure 3B, it would be informative to also see the average performance in the neutral cue condition (for example, as a straight line as in some other figures). This would help to better appreciate the relative benefits and/or costs compared to the neutral condition, also in the time-resolved data.

(4) Statistical inference for the comparison between failed and non-failed trials

Currently, the lack of modulation in the failed saccade trials hinges on a null effect. It would be stronger to support the claims with a significant difference in the congruency effect between failed and non-failed trials. Indeed, lack of significance in failed saccade trials does by itself not constitute valid evidence that the congruency effect is larger in saccade compared to failed saccade trials. For this, a significant interaction between saccade-trial-type (failed/non-failed) and congruency (congruent/incongruent) should be established (see e.g., Nieuwenhuis et al., Nat Neurosci, 2011).

(5) Time window justification

While the authors nicely depict their data across the full time axis, all statistics are currently performed on data extracted from specific time windows. How exactly were these time windows determined and justified? Likewise, how were the specific times picked for visualizing and statistically quantifying the data in e.g., Figures 3D and E? It would be reassuring to add justification for these specific time windows and/or to verify (using follow-up analyses) that the presented results are robust when different time windows are chosen.

(6) Microsaccade definition

Microsaccades are explicitly defined as being below half a degree. This appears rather arbitrary and rigid. Does the size of saccades not ultimately depend on the task and stimulus (e.g., Otero-Millan et al., PNAS, 2013) rather than being a fixed biological property? Perhaps this could be stated less rigidly, such as by stating how microsaccades are often observed below 0.5 degrees.

(Relatedly, one may wonder whether the type of instructed saccades that the authors studied here involves the same type of eye movements as the type of fixational microsaccades that have been the focus of ample prior studies. However, I recognize that this specific reflection may open a debate that is beyond the scope of this article.