Marius Peelen

Floris de Lange

eLife assessment
This valuable study uses recently developed EEG analysis methods to investigate spatial distractor suppression in a combined visual search/working memory task. While the reported results are convincing, the combined task design leaves open alternative interpretations than those currently discussed in the manuscript, potentially limiting the generalisability of the findings to other task settings. The study will be of interest to cognitive neuroscientists and psychologists working on visual attention and memory.

anonymous

Reviewer #1 (Public Review):
Summary:
The authors tested whether learning to suppress (ignore) salient distractors (e.g., a lone colored nontarget item) via statistical regularities (e.g., the distractor is more likely to appear in one location than any other) was proactive (prior to paying attention to the distractor) or reactive (only after first attending the distractor) in nature. To test between proactive and reactive suppression the authors relied on a recently developed and novel technique designed to "ping" the brain's hidden priority map using EEG inverted encoding models. Essentially, a neutral stimulus is presented to stimulate the brain, resulting in activity on a priority map which can be decoded and used to argue when this stimulation occurred (prior to or after attending to a distracting item). The authors found evidence that despite learning to suppress the high probability distractor location, the suppression was reactive, not proactive in nature.
Overall, the manuscript is well-written, tests a timely question, and provides novel insight into a long-standing debate concerning distractor suppression.
Strengths (in no particular order):
(1) The manuscript is well-written, clear, and concise (especially given the complexities of the method and analyses).
(2) The presentation of the logic and results is mostly clear and relatively easy to digest.
(3) This question concerning whether location-based distractor suppression is proactive or reactive in nature is a timely question.
(4) The use of the novel "pinging" technique is interesting and provides new insight into this particularly thorny debate over the mechanisms of distractor suppression.
Weaknesses (in no particular order):
(1) The authors tend to make overly bold claims without either A) mentioning the opposing claim(s) or B) citing the opposing theoretical positions. Further, the authors have neglected relevant findings regarding this specific debate between proactive and reactive suppression.
(2) The authors should be more careful in setting up the debate by clearly defining the terms, especially proactive and reactive suppression which have recently been defined and were more ambiguously defined here.
(3) There were some methodological choices that should be further justified, such as the choice of stimuli (e.g., sizes, colors, etc.).
(4) The figures are often difficult to process. For example, the time courses are so far zoomed out (i.e., 0, 500, 100 ms with no other tick marks) that it makes it difficult to assess the timing of many of the patterns of data. Also, there is a lot of baseline period noise which complicates the interpretations of the data of interest.
(5) Sometimes the authors fail to connect to the extant literature (e.g., by connecting to the ERP components, such as the N2pc and PD components, used to argue for or against proactive suppression) or when they do, overreach with claims (e.g., arguing suppression is reactive or feature-blind more generally).

Reviewer #2 (Public Review):
Summary:
The authors investigate the mechanisms supporting learning to suppress distractors at predictable locations, focusing on proactive suppression mechanisms manifesting before the onset of a distractor. They used EEG and inverted encoding models (IEM). The experimental paradigm alternates between a visual search task and a spatial memory task, followed by a placeholder screen acting as a 'ping' stimulus -i.e., a stimulus to reveal how learned distractor suppression affects hidden priority maps. Behaviorally, their results align with the effects of statistical learning on distractor suppression. Contrary to the proactive suppression hypothesis, which predicts reduced memory-specific tuning of neural representations at the expected distractor location, their IEM results indicate increased tuning at the high-probability distractor location following the placeholder and prior to the onset of the search display.
Strengths:
Overall, the manuscript is well-written and clear, and the research question is relevant and timely, given the ongoing debate on the roles of proactive and reactive components in distractor processing. The use of a secondary task and EEG/IEM to provide a direct assessment of hidden priority maps in anticipation of a distractor is, in principle, a clever approach. The study also provides behavioral results supporting prior literature on distractor suppression at high-probability locations.
Weaknesses:
(1) At a conceptual level, I understand the debate and opposing views, but I wonder whether it might be more comprehensive to present also the possibility that both proactive and reactive stages contribute to distractor suppression. For instance, anticipatory mechanisms (proactive) may involve expectations and signals that anticipate the expected distractor features, whereas reactive mechanisms contribute to the suppression and disengagement of attention.
(2) The authors focus on hidden priority maps in pre-distractor time windows, arguing that the results challenge a simple proactive view of distractor suppression. However, they do not provide evidence that reactive mechanisms are at play or related to the pinging effects found in the present paradigm. Is there a relationship between the tuning strength of CTF at the high-probability distractor location and the actual ability to suppress the distractor (e.g., behavioral performance)? Is there a relationship between CTF tuning and post-distractor ERP measures of distractor processing? While these may not be the original research questions, they emerge naturally and I believe should be discussed or noted as limitations.
(3) How do the authors ensure that the increased tuning (which appears more as a half-split or hemifield effect rather than gradual fine-grained tuning, as shown in Figure 5) is not a byproduct of the dual-task paradigm used, rather than a general characteristic of learned attentional suppression? For example, the additional memory task and the repeated experience with the high-probability distractor at the specific location might have led to longer-lasting and more finely-tuned traces for memory items at that location compared to others.
(4) It is unclear how IEM was performed on total vs. evoked power, compared to typical approaches of running it on single trials or pseudo-trials.
(5) Following on point 1. What is the rationale for relating decreased (but not increased) tuning of CTF to proactive suppression? Could it be that proactive suppression requires anticipatory tuning towards the expected feature to implement suppression? In other terms, better 'tuning' does not necessarily imply a higher signal amplitude and could be observable even under signal suppression. The authors should comment on this and clarify.
Minor:
(1) In the Word file I reviewed, there are minor formatting issues, such as missing spaces, which should be double-checked.
(2) Would the authors predict that proactive mechanisms are not involved in other forms of attention learning involving distractor suppression, such as habituation?
(3) A clear description in the Methods section of how individual CTFs for each location were derived would help in understanding the procedure.
(4) Why specifically 1024 resampling iterations?

Reviewer #3 (Public Review):
Summary:
In this experiment, the authors use a probe method along with time-frequency analyses to ascertain the attentional priority map prior to a visual search display in which one location is more likely to contain a salient distractor. The main finding is that neural responses to the probe indicate that the high probability location is attended, rather than suppressed, prior to the search display onset. The authors conclude that suppression of distractors at high-probability locations is a result of reactive, rather than proactive, suppression.
Strengths:
This was a creative approach to a difficult and important question about attention. The use of this "pinging" method to assess the attentional priority map has a lot of potential value for a number of questions related to attention and visual search. Here as well, the authors have used it to address a question about distractor suppression that has been the subject of competing theories for many years in the field. The paper is well-written, and the authors have done a good job placing their data in the larger context of recent findings in the field.
Weaknesses:
The link between the memory task and the search task could be explored in greater detail. For example, how might attentional priority maps change because of the need to hold a location in working memory? This might limit the generalizability of these findings. There could be more analysis of behavioral data to address this question. In addition, the authors could explore the role that intertrial repetition plays in the attentional priority map as these factors necessarily differ between conditions in the current design. Finally, the explanation of the CTF analyses in the results could be written more clearly for readers who are less familiar with this specific approach (which has not been used in this field much previously).

Pinging the Hidden Attentional Priority Map: Suppression Needs Attention

Figures and data

Schematic trial and experiment design

Behavioral findings in the search task

The performance of the Localizer in the training phase

Cross-session encoding: Alpha CTFs of Memory cue display and placeholder display

The gradient pattern of Alpha CTFs following the onset of the placeholder display

Be the first to read new articles from eLife