Microsaccades track shifting but not necessarily maintaining covert visual-spatial attention

Reviewer #1 (Public review):

Summary:

This manuscript describes a study examining the relationship between microsaccades and covert attention. This question has been widely investigated, with numerous studies showing that during sustained fixation, when subjects covertly attend to a peripheral stimulus, microsaccades tend to be biased toward the attended location. Here, the authors ask whether this microsaccade bias reflects a shift of covert attention or the maintenance of covert attention. They conclude that the bias is primarily driven by attention shifts, a finding that also helps reconcile the seemingly conflicting results of prior research, where the bias was questioned in paradigms that largely involved attention maintenance rather than shifting.

Strengths:

The paradigm and conclusions appear sound and supported by the results. A large sample size was used.

Weaknesses:

Weaknesses are mostly related to how the authors enforced fixation in the task, and clarifications are needed regarding some methodological details. A more direct comparison of the effect in the two experimental conditions is missing.

Reviewer #2 (Public review):

Summary:

This study aims to test the hypothesis that microsaccades are linked to the shifting of spatial attention, rather than the maintenance of attention at the cued location. In two experiments, participants were required to judge an orientation change at either a validly cued location (80% of the time) or an invalidly cued location (20% of the time). This change was presented at varying intervals (ranging from 500 to 3,200 ms) after cue onset. Accuracy and reaction times both showed attentional benefits at the valid versus invalid location across the different cue-target intervals. In contrast, microsaccade biases were time-dependent. The authors report a directional bias primarily observed around 400 ms after the cue, with later intervals (particularly in Experiment 2) exhibiting no biases in microsaccade direction towards the cued location. The authors argue that this finding supports their initial hypothesis that microsaccade biases reflect shifts in attention, but that maintaining attention at the cued location after an attention shift is not correlated with microsaccade direction.

Strengths:

The results are straightforward given the chosen experimental design. The manuscript is clearly written, and the presentation of the study and its visualisations are both of a high standard.

Weaknesses:

The major weakness of this paper is its incremental contribution to a widely studied phenomenon. The link between attention and microsaccades has been the subject of extensive research over the past two decades. This study merely provides a limited overview of the key insights gained from these papers and discussions. In fact, it attempts to summarise previous work by stating that many experiments found a link, while others did not, and provides only a relatively small number of references. To make a significant contribution, I believe the authors should evaluate the field more thoroughly, rather than merely scratching the surface.

The authors then present a potential solution to the conflicting past findings, arguing that attention should be considered a dynamic process that can be broken down into an attention shift and a sustained attention phase. Although the authors present this as a novel concept, I cannot think of anyone in the field who considers spatial attention to be a static entity. Nevertheless, I was curious to see how the authors would attempt to determine the precise timing of the attention shift and manipulate the different stages individually. However, the authors only varied the interval between the onset of the attention cue and the test stimulus, failing to further pinpoint their dynamic attention concept.

The current version of the experiment, therefore, takes a correlational approach, similar to initial studies by Engbert and Kliegl (2003) and Hafed and Clark (2002). Meanwhile, we have learned a great deal about the link between microsaccades and attention. Below, I will list just a few of these findings to demonstrate how much we already know. It is important to note that, while the present study cites some of these papers, it does not provide a clear overview of how the current study goes beyond previous research.

(1) Yuval-Greenberg and colleagues (2014) presented stimuli contingent on online-detected microsaccades. A postcue indicated the target for a visual task, and the target could be congruent or incongruent with the microsaccade direction. The authors showed higher visual accuracy in congruent trials. The authors cited that paper, but it is still important to emphasize how this study already tried to go beyond purely correlational links on a single trial level.

(2) The Desimone lab (Lower et al., 2018) showed that firing rates in monkey V4 and IT were increased when a microsaccade was generated in the direction of the attended target.

(3) However, attention can modulate responses in the superior colliculus even in the absence of microsaccades (Yu et al., 2022)

(4) Similarly, Poletti, Rucci & Carrasco (2017) observed attentional modulations in the absence of microsaccades, or comparable attention effects irrespective of whether a microsaccade occurred or not (Roberts & Carrasco, 2019).

Thus, in light of these insights, I believe the current study only adds incrementally to our understanding of the link between microsaccades and spatial attention.

In general, it is important to have an independent measure of the dynamics of an attention shift. I think a shift of 200-600 ms is quite long, and defining this interval is rather arbitrary. Why consider such a long delay as the shift? Rather than taking a data-driven approach to defining an interval for an attention shift, it would be more convincing to derive an interval of interest based on past research or an independent measure.

The present analyses report microsaccade statistics across all trials, but do not directly link single-trial microsaccades to accuracy. Similarly, reaction times and accuracy were analyzed only with respect to valid vs. invalid trials. Here, it would be important to link the findings between microsaccades and performance on a single-trial level. For instance, can the authors report reaction times and accuracy also separately for trials with vs. without microsaccades, and for trials with congruent vs. incongruent microsaccades?

The study would benefit greatly from including a neutral condition to substantiate claims of attentional benefits and costs. It is highly probable that invalid trials would also demonstrate costs in terms of reaction times and accuracy. It would be interesting to observe whether directional biases in microsaccades are also evident when compared to a neutral condition.

Author response:

We wish to thank the reviewers and the editors for their careful evaluation of our article and for their valuable input that we will embrace to strengthen our article. We will still respond in full when we have had time to perform further analyses, which we anticipate will corroborate our main conclusions and make our article more comprehensive.

For now, we provide a provisional response to the major points brought forward by both the editorial summary and the public reviews. As we understood, the two main points that were raised regard: (1) the novelty and, accordingly, the theoretical importance of our work and (2) the (in)completeness of our results. We provide our provisional response to both of these points below.

Novelty and theoretical relevance of the work

Regarding the novelty of our work, we believe the reviews—and, by extension, the editorial summary— underappreciated the main theoretical value of the question we addressed. Our work set out to investigate whether microsaccades track covert attentional shifting, attentional maintenance, or both. We fully recognise that there are ample prior studies that investigated and reported a link between microsaccades and covert attention, but also underscore how other studies report seemingly contradicting evidence by reporting that there is no such link. One such example is a recent high profile paper by Willett & Mayo in PNAS (2023). Prompted by the recent hypothesis that this seemingly conflicting evidence may be due to prior work investigating attention ‘in di erent stages’ (van Ede, PNAS, 2023), we set out to address precisely this using a dedicated task that we designed for this purpose. As acknowledged by the summary and public reviews, this helps to reconcile seemingly opposing views in the literature. In our view, such reconciliation has substantial theoretical value.

While we appreciate that our reported insights may resonate and appear plausible to those working on this topic, we are not aware of any prior studies that directly addressed whether the link between covert attention and microsaccades may fundamentally depend on the ‘stage’ of attentional deployment (‘shift’ vs. ‘maintain’).

To fill this key gap and address this timely issue, we developed a dedicated experiment designed to evaluate the relationship between microsaccades and the di erent stages of attention within a single paradigm. We did so by varying the cue-target intervals to uniquely incentivise early shifting (by having short intervals), while also being able to assess microsaccade biases during subsequent maintenance (in the longer trials). To our knowledge, no previous task has jointly examined these components in this manner. Moreover, our inclusion of two widely adopted approaches to fixational control provides yet another source of novelty. Together, we believe that these features position our work as a substantive advance that reconciles seemingly opposing theoretical views.

Completeness of results

Regarding the completeness of our results, the editorial summary points to “the absence of independent measures, single-trial analyses, and neutral-condition controls needed to substantiate the central claims”. In our view, while the raised points are valuable, they pertain to issues that are tangential to our primary question and stem from misunderstandings of key analytical choices. We consider our results complete and comprehensive with regards to the main question our studies set out to answer. We briefly clarify each of the raised points below, and will respond more elaborately as part of our forthcoming revision.

First, regarding the portrayed “need” for independent measures to define the ‘shift window’ of interest, we wish to clarify how our main analysis is completely agnostic to predetermined time windows, as we employ a cluster-based permutation approach to assess our rich time-resolved data across the full time axis. For the complementary analyses that address the ‘shift’ and ‘maintain’ windows more directly, we use a priori defined windows that are based on ample prior literature (from prior literature studying microsaccade biases, as well as from prior literature on the time course of top-down attention as studied through SOA manipulations). Accordingly, even these ‘zoomed in’ analyses rely on time windows that are empirically grounded in ample prior research.

Second, regarding the use of single-trial analyses, we want to emphasise that single-trial predictability is not where our theoretical question resides. We start from the perspective that the relationship between covert visual-spatial attention and microsaccades is inherently probabilistic. Our aim is not to address or question this. Rather, our aim is to determine whether this probabilistic relationship behaves similarly during attentional shifting and maintenance—an issue our analyses directly and appropriately address. In addition, we also explicitly discuss how the link between microsaccades and attention is fundamentally probabilistic at the single-trial level in our discussion, and prompted by the valuable feedback, we plan to expand on this important contextualisation as part of our revision.

Finally, regarding the portrayed “need” for a neural-attention control condition, we agree that inclusion of a neutral attention condition could be informative for disentangling the ‘benefits’ versus ‘costs’ of attentional cueing. However, such disambiguation is tangential to our central aim. Rather, our behavioural data primarily serve to verify attentional ‘allocation’ at later cue-target intervals. Observing a di erence between valid and invalid cues su ices for this central aim. We also note how inclusion of a neutral condition would have reduced trial-numbers and statistical power for our critical conditions of interest. Accordingly, we do not see this as a limitation that in any way challenges our main conclusions. Prompted by this reflection, during our revision we will ensure to not mention selective ‘benefits’ or ‘costs’ of our cueing manipulation, but to refer to ‘the presence of an attentional modulation’ instead.

Therefore, we believe that the explicit design and analysis choices that we made aligned with the theoretical aims of our study, and that our data provide a complete and coherent test of our central question. The raised points are valuable and we will leverage them to improve our article, but they do not render our findings “incomplete” (as currently portrayed) with regards to the key goal of our article.

Future changes

Naturally, we consider the feedback from the editors and the reviewers of great value, and we will incorporate their suggestions to further strengthen our article. Concretely, we plan to implement the following revisions:

• In our introduction we plan to elaborate on the prior state of knowledge to provide a more complete context.

• We plan to add precise clarifications throughout the paper, ranging from methodological details and methodological choices to interpretation of the results. This should increase the comprehensiveness and transparency of our article.

• We will run and incorporate the outcomes of various additional analyses that we anticipate will further substantiate our conclusions and provide a more comprehensive view of our data and key findings.

We are confident that these revisions will enhance clarity and accessibility while reinforcing the theoretical contributions of the work.

References

Willett, S. M., & Mayo, P. J. (2023). Microsaccades are directed toward the midpoint between targets in a variably cued attention task. Proceedings of the National Academy of Sciences of the United States of America, 120(20). https://doi.org/10.1073/pnas.2220552120