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  1. Author Response:

    Reviewer #1 (Public Review):

    This is a clearly written manuscript describing an elegant study that demonstrates how microsaccades are not the triggers of attentional effects, and that attentional modulations can be observed in the absence of microsaccades. This is a very much needed work, especially in the light of the recent debate regarding whether or not microsaccades are the cause of peripheral attentional effects. By explicitly comparing and quantifying the effects of attention on neuronal responses in the presence and in the absence of microsaccades, this work provides important insights on this debate. I think the work is well conducted and the results are solid.

    We thank the reviewer for their supportive comments!

    I only have few comments/suggestions:

    1. Lines 125-126, the authors report that monkeys generated frequent microsaccades but their overall direction was not systematically biased towards the cue location. This seems to be in contrast with what previously reported in the literature in humans and monkeys. I think this discrepancy should be discussed in the discussion. Is this simply the result of different experimental paradigms (maybe exogenous vs endogenous attention, or the presence of the cue for the entire duration of the trial, ect)?

    As suggested, we discuss three main factors which may contribute to this discrepancy:

    The first factor is the difference in the time window used for microsaccades analyses. Previous reports focused their analyses of microsaccades on the time window immediately after cue onset. In our analyses, the time window focused on is the ‘delay period’ which is hundreds of milliseconds after the cue and the time epoch used in most electrophysiology studies about attention.

    A second factor is how the spatial cues were presented. In our paradigm the cue ring appeared in the periphery and then disappeared. In contrast, previous paradigms used a cue presented near fixation that persisted throughout the trial. Our brief peripheral cue provides less of an impetus to generate small saccades directed towards the cue, compared to the case when the cue is continuously near the center of gaze.

    A third factor is that monkeys in our task were trained to release a joystick to report their detection of stimulus events, rather than make a saccade. Because human and monkey subjects tend to make microsaccades in the same direction as their upcoming saccadic choices (Yu et al., 2016), attention tasks using saccade reports will tend to introduce this direction bias on microsaccades. By using a joystick release, we minimized these lateralized effects related to saccade preparation.

    These points are now addressed in the second paragraph of discussion.

    1. It is very interesting that microsaccades modulate neural responses for stimuli that are much further away from their landing location. However, the stimulus used in these cueing tasks is also unnatural. Normally we are not fixating on a meaningless dot while all the interesting stimuli are presented in the periphery. In normal conditions the foveal input is rich in detail and it is generally relevant (that's why we are foveating certain stimuli in the first place). I wonder if the authors can comment on whether the modulations reported here would also occur in more natural conditions when an interesting and maybe salient/relevant stimulus is presented at the center of gaze, while subjects are also attending to a peripheral target. Will the neural response be modulated selectively for neurons for which the receptive field is on the peripheral target or will it also affect neurons where the receptive field aligns with the microsaccade target location in the fovea?

    The reviewer raises a very good point. In our study, the relationship between microsaccades and attention-related modulation was examined when monkeys selectively attended a stimulus located in the near peripheral visual field while maintaining central fixation. We agree that under more natural conditions, the monkey would just look directly at the peripheral stimulus. As in many attention studies with this type of design, our experiments hold the system in a state of sustained peripheral attention which would otherwise be much shorter.

    We believe that similar modulation at the peripheral location would be briefly observed if the monkey were allowed to satisfy the natural tendency to look at the stimulus, although this would make it more difficult to examine the relationship with microsaccades. This would be consistent with the documented pre-saccadic modulation of attention (e.g., documented by the Carrasco lab, Li, Hanning, & Carrasco, 2021).

    Once the attended stimulus is foveated, there is strong behavioral evidence from several recent studies demonstrating that attention can be selectively distributed even within the fovea (Poletti, Rucci, & Carrasco, 2017). Considering the now substantial evidence that the foveal portion of the SC map is activated when the behaviorally relevant location is at the center of the visual field (e.g., during parafoveal smooth pursuit as in Hafed & Krauzlis, 2008), we expect that SC neurons with foveal RFs would display similar attention-related modulation as we found here. However, to the best of our knowledge, there have not yet been studies documenting the attention-related modulation of neurons with foveal RFs and the possible influence of microsaccades.

    We agree with the reviewer that these are interesting points, and have now added a new paragraph in the discussion (final paragraph) to address this point.

    1. The authors do not report behavioral performance. Presumably the task is very easy, but I wonder if reaction times and performance correct was related with the attentional effects and how did it change with respect to microsaccade direction, e.g., were subjects' reaction times shorter at the cued location also when microsaccades were directed at the opposite location? I think this information would be very valuable.

    We agree it is valuable to document the behavioral performance; we had omitted this because this is the same task we have used in previous studies which do include such behavioral documentation.

    To address the reviewer’s comments, we added an analysis and plot documenting the hit and false alarm rate for each subject in each experimental session. To accommodate this new plot, we have now divided the original Figure 1 (which included task, neuronal data and microsaccades) into a new Figure 1 (task, behavior, and neuronal data) and a new Figure 2 (microsaccades). The new plot showing hit and false alarms is Figure 1b in the revised manuscript.

    The task was not especially easy – we adjusted the amplitude of the color saturation change to be just slightly above the threshold for detection; hence, the hit rates were generally between 75-90%. The performance was very consistent across sessions in our well-trained monkeys, and the low rate of false alarms for ‘foil’ changes provides behavioral confirmation that they attended to the correct stimulus location.

    To address the comments about reaction time, we have added a new plot to our new Figure 2 (Figure 2c) showing the monkeys’ hit rates (top) and joystick release times (bottom) subdivided based on whether there were no microsaccades, microsaccade towards, and microsaccades away from the cued location (-50 to 50ms relative to cued stimulus change onset). These plots show that when there were no microsaccades, behavioral performance was at least as good as with microsaccades. When there were microsaccades, reaction times were slower when microsaccades were directed away from the cued location. As the reviewer may have anticipated, these effects again confirm that differences in attentional state as evident in task performance covary with the direction of microsaccades, and we thank them for the suggestions. We now added a new paragraph in the results to describe these findings.

    1. Another important difference in the paradigm used in Lowet et al vs the one described in this manuscript is that in Lowet et al monkeys were instructed to saccade toward the target position at some point during the trial after the cue and the target presentation. Hence, monkeys presumably prepared the saccade and held off its execution during the time the cue and the target were presented. This was not the case in the current paradigm, where the monkey is instructed to maintain fixation as in a standard spatial cueing paradigm. I wonder if this difference may explain some discrepancies in the results.

    This is a very good point. As mentioned in our reply to point #1 above, previous studies (Yu et al., 2016) have shown that human and monkey subjects tend to make microsaccades in the same direction as their upcoming saccadic choices. As pointed out by the reviewer, in the Lowet et al. study the directions of microsaccades might be related to the motor preparation of the upcoming choice saccade as well as related to the allocation of attention. In contrast, in our experiments, monkeys reported their choice by releasing the joystick and were prohibited from making larger saccades.

    We agree this can be an important factor for the differences in the results, and we now address these points in the second paragraph of discussion.

    Reviewer #2 (Public Review):

    This is a correlative study with the main result that microsaccades do not alter attention-related modulations of neuronal activity. This is an important question, speaking to the origin of one of the mind's most fundamental processes. The experimental manipulations and analyses are well chosen, carefully conducted and visualized. They include critical controls for alternative explanations.

    Thank you for your constructive comments.

    To ascertain their claims, however, it is important that the authors cover their ground. In pursuit of that, a few important analyses are required.

    1. Did the manipulation of attention work? In the present version of the manuscript, the authors do not report behavioral results, which is necessary to confirm that the cue was successful in manipulating attention. That is, the observed modulation in firing (in RF vs outside of RF) should be related to a behavioral advantage in sensitivity to changes at the cued location. To confirm the link of the neural results to attention (rather than, say, just the cue), the behavioral results provide opportunities for critical tests. One way to do this would be to analyze neural firing rates as a function of response rather than cue location (provided subjects made enough errors). Note: A detailed discussion of why the cue cannot be equated to attention can be found in Laubrock et al. (2010, Atten Percept Psychophys; https://doi.org/10.3758/app.72.3.683).

    Yes, the manipulation of attention worked. As suggested, we now document the effectiveness of the attention manipulation by plotting the hit and false-alarm rates for each subject in each experimental session (new Figure 1b). We also confirmed that the SC neuronal attention-related modulation depended on subjects’ behavioral response (new Figure 1d). We also note that these same attention manipulations have been used in previous studies examining the neuronal mechanisms of attention.

    1. Were all microsaccades detected? One of the main results of the study is that attention-related modulations were observed even in the absence of microsaccades. These results hinge on successful detection of all microsaccades, even at a very small scale. Given the video-based eye tracking the authors will have missed a (possibly large) number of smaller microsaccades (Poletti & Rucci, Vision Res, 2016; https://doi.org/10.1016/j.visres.2015.01.018). This concern is exacerbated by the fact that eye tracking was monocular, such that a validation of detected microsaccades based on the signal in the other eye could not be performed.

    We have performed additional microsaccade detection analyses using both more stringent and more lenient thresholds (the "lambda" value of Engbert & Kliegl, 2003). We have verified that our findings are robust over a range of detection thresholds and include a new supplemental figure to demonstrate this point (Figure 4 – figure supplement 2).

    1. Relation to previous claims of causality Hafed (2013, Neuron) reported perceptual changes in attentional cueing that covaried with the occurrence of microsaccades. Hafed (2013) argued that microsaccades might be underlying the performance changes commonly attributed to covert shifts of attention. This point seems central to the current paper's line of argument and should thus be discussed in detail with respect to the current findings. At present, the paper by Hafed (2013) is not cited in the current manuscript when its conclusions may need reconsideration based on the current results.

    We agree, and a similar point was raised by Reviewer #1. We have expanded the main text based on your recommendations.

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  2. Evaluation Summary:

    This is very much needed work, especially in light of the recent debate regarding whether or not microsaccades are the cause of peripheral attentional effects. A few influential papers have been published recently strongly suggesting that attentional effects are primarily the result of the execution of tiny microsaccades that humans/primates perform during fixation while attending to peripheral stimuli. These past findings have, naturally, a number of implications for the way we interpret visual attention, and raised the question of whether shifts of attention are dependent on microsaccades. By explicitly comparing and quantifying the effects of attention on neuronal responses in the presence and in the absence of microsaccades, this work provides important insights into this debate.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their names with the authors.)

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  3. Reviewer #1 (Public Review):

    This is a clearly written manuscript describing an elegant study that demonstrates how microsaccades are not the triggers of attentional effects, and that attentional modulations can be observed in the absence of microsaccades. This is a very much needed work, especially in the light of the recent debate regarding whether or not microsaccades are the cause of peripheral attentional effects. By explicitly comparing and quantifying the effects of attention on neuronal responses in the presence and in the absence of microsaccades, this work provides important insights on this debate. I think the work is well conducted and the results are solid. I only have few comments/suggestions:

    1. Lines 125-126, the authors report that monkeys generated frequent microsaccades but their overall direction was not systematically biased towards the cue location. This seems to be in contrast with what previously reported in the literature in humans and monkeys. I think this discrepancy should be discussed in the discussion. Is this simply the result of different experimental paradigms (maybe exogenous vs endogenous attention, or the presence of the cue for the entire duration of the trial, ect)?

    2. It is very interesting that microsaccades modulate neural responses for stimuli that are much further away from their landing location. However, the stimulus used in these cueing tasks is also unnatural. Normally we are not fixating on a meaningless dot while all the interesting stimuli are presented in the periphery. In normal conditions the foveal input is rich in detail and it is generally relevant (that's why we are foveating certain stimuli in the first place). I wonder if the authors can comment on whether the modulations reported here would also occur in more natural conditions when an interesting and maybe salient/relevant stimulus is presented at the center of gaze, while subjects are also attending to a peripheral target. Will the neural response be modulated selectively for neurons for which the receptive field is on the peripheral target or will it also affect neurons where the receptive field aligns with the microsaccade target location in the fovea?

    3. The authors do not report behavioral performance. Presumably the task is very easy, but I wonder if reaction times and performance correct was related with the attentional effects and how did it change with respect to microsaccade direction, e.g., were subjects' reaction times shorter at the cued location also when microsaccades were directed at the opposite location? I think this information would be very valuable.

    4. Another important difference in the paradigm used in Lowet et al vs the one described in this manuscript is that in Lowet et al monkeys were instructed to saccade toward the target position at some point during the trial after the cue and the target presentation. Hence, monkeys presumably prepared the saccade and held off its execution during the time the cue and the target were presented. This was not the case in the current paradigm, where the monkey is instructed to maintain fixation as in a standard spatial cueing paradigm. I wonder if this difference may explain some discrepancies in the results.

    Read the original source
    Was this evaluation helpful?
  4. Reviewer #2 (Public Review):

    This is a correlative study with the main result that microsaccades do not alter attention-related modulations of neuronal activity. This is an important question, speaking to the origin of one of the mind's most fundamental processes. The experimental manipulations and analyses are well chosen, carefully conducted and visualized. They include critical controls for alternative explanations. To ascertain their claims, however, it is important that the authors cover their ground. In pursuit of that, a few important analyses are required.

    1. Did the manipulation of attention work?
    In the present version of the manuscript, the authors do not report behavioral results, which is necessary to confirm that the cue was successful in manipulating attention. That is, the observed modulation in firing (in RF vs outside of RF) should be related to a behavioral advantage in sensitivity to changes at the cued location. To confirm the link of the neural results to attention (rather than, say, just the cue), the behavioral results provide opportunities for critical tests. One way to do this would be to analyze neural firing rates as a function of response rather than cue location (provided subjects made enough errors). Note: A detailed discussion of why the cue cannot be equated to attention can be found in Laubrock et al. (2010, Atten Percept Psychophys; https://doi.org/10.3758/app.72.3.683).

    2. Were all microsaccades detected?
    One of the main results of the study is that attention-related modulations were observed even in the absence of microsaccades. These results hinge on successful detection of *all* microsaccades, even at a very small scale. Given the video-based eye tracking the authors will have missed a (possibly large) number of smaller microsaccades (Poletti & Rucci, Vision Res, 2016; https://doi.org/10.1016/j.visres.2015.01.018). This concern is exacerbated by the fact that eye tracking was monocular, such that a validation of detected microsaccades based on the signal in the other eye could not be performed.

    3. Relation to previous claims of causality
    Hafed (2013, Neuron) reported perceptual changes in attentional cueing that covaried with the occurrence of microsaccades. Hafed (2013) argued that microsaccades might be underlying the performance changes commonly attributed to covert shifts of attention. This point seems central to the current paper's line of argument and should thus be discussed in detail with respect to the current findings. At present, the paper by Hafed (2013) is not cited in the current manuscript when its conclusions may need reconsideration based on the current results.

    Read the original source
    Was this evaluation helpful?