Author response:
The following is the authors’ response to the original reviews.
Public Reviews:
Reviewer #1 (Public review):
(1) Why was V1 separated from the rest of the visual cortex, and why the rest of the areas were simply lumped into an EVC ROI? It would be helpful to understand the separation into ROIs.
We thank the reviewer for raising the concerns regarding the definition of ROI. Our approach to analyze V1 separately was based on two key considerations. First, previous studies consistently identify V1 as the main locus of sensory-like templates during featurespecific preparatory attention (Kok et al., 2014; Aitken et al., 2020). Second, V1 shows the strongest orientation selectivity within the visual hierarchy (Priebe, 2016). In contrast, the extrastriate visual cortex (EVC; comprising V2, V2, V3AB and V4) demonstrates broader selectivity, such as complex features like contour and texture (Grill-Spector & Malach, 2004). Thus, we think it would be particularly informative to analyze V1 data separately as our experiment examines orientation-based attention. We should also note that we conducted MVPA separately for each visual ROIs (V2, V3, V3AB and V4). After observing similar patterns of results across these regions, we averaged the decoding accuracies into a single value and labeled it as EVC. This approach allowed us to simplify data presentation while preserving the overall data pattern in decoding performance. We now added the related explanations on the ROI definition in the revised texts (Page 26; Line 576-581).
(2) It would have been helpful to have a behavioral measure of the "attended" orientation to show that participants in fact attended to a particular orientation and were faster in the cued condition. The cue here was 100% valid, so no such behavioral measure of attention is available here.
We thank the reviewer for the comments. We agree that including valid and neutral cue trials would have provided valuable behavioral measures of attention; Yet, our current design was aimed at maximizing the number of trials for decoding analysis due to fMRI time constraints. Thus, we could not fit additional conditions to measure the behavioral effects of attention. However, we note that in our previous studies using a similar feature cueing paradigm, we observed benefits of attentional cueing on behavioral performance when comparing valid and neutral conditions (Liu et al., 2007; Jigo et al., 2018). Furthermore, our neural data indeed demonstrated attention-related modulation (as indicated by MVPA results, Fig. 2 in the main texts) so we are confident that on average participants followed the instruction and deployed their attention accordingly. We now added the related explanations on this point in the revised texts (Page 23; Line 492-498).
(3) As I was reading the manuscript I kept thinking that the word attention in this manuscript can be easily replaced with visual working memory. Have the authors considered what it is about their task or cognitive demand that makes this investigation about attention or working memory?
We thank the reviewer for this comment. We added the following extensive discussion on this point in the revised texts (Page 18; Line 363-381).
“It could be argued that preparatory attention relies on the same mechanisms as working memory maintenance. While these functions are intuitively similar and likely overlap, there is also evidence indicating that they can be dissociated (Battistoni et al., 2017). In particular, we note that in our task, attention is guided by symbolic cues (color-orientation associations), while working memory tasks typically present the actual visual stimulus as the memorandum. A central finding in working memory studies is that neural signals during WM maintenance are sensory in nature, as demonstrated by generalizable neural activity patterns from stimulus encoding to maintenance in visual cortex (Harrison & Tong, 2009; Serences et al., 2009; Rademaker et al., 2019). However, in our task, neural signals during preparation were nonsensory, as demonstrated by a lack of such generalization in the No-Ping session (see also Gong et al., 2022). We believe that the differences in cue format and task demand in these studies may account for such differences. In addition to the difference in the sensory nature of the preparatory versus delay-period activity, our ping-related results also exhibited divergence from working memory studies (Wolff et al., 2017; 2020). While these studies used the visual impulse to differentiate active and latent representations of different items (e.g., attended vs. unattended memory item), our study demonstrated the active and latent representations of a single item in different formats (i.e., non-sensory vs. sensory-like). Moreover, unlike our study, the impulse did not evoke sensory-like neural patterns during memory retention (Wolff et al., 2017). These observations suggest that the cognitive and neural processes underlying preparatory attention and working memory maintenance could very well diverge. Future studies are necessary to delineate the relationship between these functions both at the behavioral and neural level.”
(4) If I understand correctly, the only ROI that showed a significant difference for the crosstask generalization is V1. Was it predicted that only V1 would have two functional states? It should also be made clear that the only difference where the two states differ is V1.
We thank the reviewer for this comment. We would like to clarify that our analyses revealed similar patterns of preparatory attentional representations in V1 and EVC. During the Ping session, the cross-task generalization analyses revealed decodable information in both V1 and EVC (ps < 0.001), significantly higher than that in the No-Ping session for V1 (independent t-test: t(38) = 3.145, p = 0.003; Cohen’s d = 0.995) and EVC (independent t-test: t(38) = 2.153, p = 0.038, Cohen’s d = 0.681) (Page 10; Line 194-196). While both areas maintained similar representations, additional measures (Mahalanobis distance, neural-behavior relationship and connectivity changes) showed more robust ping-evoked changes in V1 compared to EVC. This differential pattern likely reflects the primary role of V1 in orientation processing, with EVC showing a similar but weaker response profile. We have revised the text to clarity this point (Page 16; Line 327-329).
(5) My primary concern about the interpretation of the finding is that the result, differences in cross-task decoding within V1 between the ping and no-ping condition might simply be explained by the fact that the ping condition refocuses attention during the long delay thus "resharpening" the template. In the no-ping condition during the 5.5 to 7.5 seconds long delay, attention for orientation might start getting less "crisp." In the ping condition, however, the ping itself might simply serve to refocus attention. So, the result is not showing the difference between the latent and non-latent stages, rather it is the difference between a decaying template representation and a representation during the refocused attentional state. It is important to address this point. Would a simple tone during the delay do the same? If so, the interpretation of the results will be different.
We thank the reviewer for this comment. The reviewer proposed an alternative account suggesting that visual pings may function to refocus attention, rather than reactivate latent information during the preparatory period. If this account holds (i.e., attention became weaker in the no-ping condition and it was strengthened by the ping due to re-focusing), we would expect to observe a general enhancement of attentional decoding during the preparatory period. However, our data reveal no significant differences in overall attention decoding between two conditions during this period (ps > 0.519; BFexcl > 3.247), arguing against such a possibility.
The reviewer also raised an interesting question about whether an auditory tone during preparation could produce effects similar to those observed with visual pings. Although our study did not directly test this possibility, existing literature provides some relevant evidence. In particular, prior studies have shown that latent visual working memory contents are selectively reactivated by visual impulses, but not by auditory stimuli (Wolff et al., 2020). This finding supports the modality-specificity for visually encoded contents, suggesting that sensory impulses must match the representational domain to effectively access latent visual information, which also argues against the refocusing hypothesis above. However, we do think that this is an important question that merits direct investigation in future studies. We now added the related discussion on this point in the revised texts (Page 10, Line 202-203; Page 19, Line 392395).
(6) The neural pattern distances measured using Mahalanobis values are really great! Have the authors tried to use all of the data, rather than the high AMI and low AMI to possibly show a linear relationship between response times and AMI?
We thank the reviewer for this comment. We took the reviewer’s suggestion to explore the relationship between attentional modulation index (AMI) and RTs across participants for each session (see Figure 3). In the No-Ping session, we observed no significant correlation between AMI and RT (r = -0.366, p = 0.113). By contrast, the same analysis in the Ping condition revealed a significantly negative correlation (r = -0.518, p = 0.019). These results indicate that the attentional modulations evoked by visual impulse was associated with faster RTs, supporting the functional relevance of activating sensory-like representations during preparation. We have now included these inter-subject correlations in the main texts (Page 13, Line 258-264; Fig 3D and 3E) along with within-subject correlations in the Supplementary Information (Page 6, Line, 85-98; S3 Fig).
(7) After reading the whole manuscript I still don't understand what the authors think the ping is actually doing, mechanistically. I would have liked a more thorough discussion, rather than referencing previous papers (all by the co-author).
We thank the reviewer for this comment regarding the mechanistic basis of visual pings. We agree that this warrants deeper discussion. One possibility, as informed by theoretical studies of working memory, is that the sensory-like template could be maintained via an “activity-silent” mechanism through short-term changes in synaptic weights (Mongillo et al., 2008). In this framework, a visual impulse may function as nonspecific inputs that momentarily convert latent traces into detectable activity patterns (Rademaker & Serences, 2017). Related to our findings, it is unlikely that the orientation-specific templates observed during the Ping session emerged from purely non-sensory representations and were entirely induced by an exogenous ping, which was devoid of any orientation signal. Instead, the more parsimonious explanation is that visual impulse reactivated pre-existing latent sensory signals. To our knowledge, the detailed circuit-level mechanism of such reactivation is still unclear; existing evidence only suggests a relationship between ping-evoked inputs and the neural output (Wolff et al., 2017; Fan et al., 2021; Duncan et al., 2023). We now included the discussion on this point in the main texts (Page 19, Line 383-401).
Reviewer #2 (Public review):
(1) The origin of the latent sensory-like representation. By 'pinging' the neural activity with a high-contrast, task-irrelevant visual stimulus during the preparation period, the authors identified the representation of the attentional feature target that contains the same information as perceptual representations. The authors interpreted this finding as a 'sensory-like' template is inherently hosted in a latent form in the visual system, which is revealed by the pinging impulse. However, I am not sure whether such a sensory-like template is essentially created, rather than revealed, by the pinging impulses. First, unlike the classical employment of the pinging technique in working memory studies, the (latent) representation of the memoranda during the maintenance period is undisputed because participants could not have performed well in the subsequent memory test otherwise. However, this appears not to be the case in the present study. As shown in Figure 1C, there was no significant difference in behavioral performance between the ping and the no-ping sessions (see also lines 110-125, pg. 5-6). In other words, it seems to me that the subsequent attentional task performance does not necessarily rely on the generation of such sensory-like representations in the preparatory period and that the emergence of such sensory-like representations does not facilitate subsequent attentional performance either. In such a case, one might wonder whether such sensory-like templates are really created, hosted, and eventually utilized during the attentional process. Second, because the reference orientations (i.e. 45 degrees and 135 degrees) have remained unchanged throughout the experiment, it is highly possible that participants implicitly memorized these two orientations as they completed more and more trials. In such a case, one might wonder whether the 'sensory-like' templates are essentially latent working memory representations activated by the pinging as was reported in Wolff et al. (2017), rather than a functional signature of the attentional process.
We thank the reviewer for this comment. We agree that the question of whether the sensory-like template is created or merely revealed by visual pinging is crucial for the understanding our findings. First, we acknowledge that our task may not be optimized for detecting changes in accuracy, as the task difficulty was controlled using individually adjusted thresholds (i.e., angular difference). Nevertheless, we observed some evidence supporting the neural-behavioral relationships. In particular, the impulse-driven sensory-like template in V1 contributed to facilitated faster RTs during stimulus selection (Page 12, Fig. 3D and 3E in the main texts; also see our response to R1, Point 6).
Second, the reviewer raised an important concern about whether the attended feature might be stored in the memory system due to the trial-by-trial repetition of attention conditions (attend 45º or attend 135º). Although this is plausible, we don’t think it is likely. We note that neuroimaging evidence shows that attended working memory contents maintain sensory-like representations in visual cortex (Harrison & Tong, 2009; Serences et al., 2009; Rademaker et al., 2019), with generalizable neural activity patterns from perception to working memory delay-period, whereas unattended items in multi-item working memory tasks are stored in a latent state for prospective use (Wolff et al., 2017). Importantly, our task only required maintaining a single attentional template at a time. Thus, there was no need to store it via latent representations, if participants simply used a working memory mechanism for preparatory attention. Had they done so, we should expect to find evidence for a sensory template, i.e., generalizable neural pattern between perception and preparation in the No-Ping condition, which was not what we found. We have mentioned this point in the main texts (Page 18, Line 367-372).
(2) The coexistence of the two types of attentional templates. The authors interpreted their findings as the outcome of a dual-format mechanism in which 'a non-sensory template' and a latent 'sensory-like' template coexist (e.g. lines 103-106, pg. 5). While I find this interpretation interesting and conceptually elegant, I am not sure whether it is appropriate to term it 'coexistence'. First, it is theoretically possible that there is only one representation in either session (i.e. a non-sensory template in the no-ping session and a sensory-like template in the ping session) in any of the brain regions considered. Second, it seems that there is no direct evidence concerning the temporal relationship between these two types of templates, provided that they commonly emerge in both sessions. Besides, due to the sluggish nature of fMRI data, it is difficult to tell whether the two types of templates temporally overlap.
We thank the reviewer for the comment regarding our interpretation of the ‘coexistence’ of non-sensory and sensory-like attentional template. While we acknowledge the limitations of fMRI in resolving temporal relationships between these two types of templates, several aspects of our data support a dual-format interpretation.
First, our key findings remained consistent for the subset of participants (N=14) who completed both No-Ping and Ping sessions in counterbalanced order. It thus seems improbable that participants systematically switched cognitive strategies (e.g., using non-sensory templates in the No-Ping session versus sensory-like templates in the Ping session) in response to the task-irrelevant, uninformative visual impulse. Second, while we agree with the reviewer that the temporal dynamics between these two templates remain unclear, it is difficult to imagine that orientation-specific templates observed during the Ping session emerged de novo from a purely non-sensory templates and an exogenous ping. In other words, if there is no orientation information at all to begin with, how does it come into being from an orientation-less external ping? It seems to us that the more parsimonious explanation is that there was already some orientation signal in a latent format, and it was activated by the ping, in line with the models of “activity-silent” working memory. To address these concerns, we have added the related discussion of these alternative interpretations in the main texts (Page 19, Line 387-391)
(3) The representational distance. The authors used Mahalanobis distance to quantify the similarity of neural representation between different conditions. According to the authors' hypothesis, one would expect greater pattern similarity between 'attend leftward' and 'perceived leftward' in the ping session in comparison to the no-ping session. However, this appears not to be the case. As shown in Figures 3B and C, there was no major difference in Mahalanobis distance between the two sessions in either ROI and the authors did not report a significant main effect of the session in any of the ANOVAs. Besides, in all the ANOVAs, the authors reported only the statistic term corresponding to the interaction effect without showing the descriptive statistics related to the interaction effect. It is strongly advised that these descriptive statistics related to the interaction effect should be included to facilitate a more effective and intuitive understanding of their data.
We thank the reviewer for this comment. We expected greater pattern similarity between 'attend leftward' and 'perceived leftward' in the Ping session in comparison to the Noping session. This prediction was supported by a significant three-way interaction effect between session × attended orientation × perceived orientation (F(1,38) = 5.00, p = 0.031, ηp2 = 0.116). In particular, there was a significant interaction between attended orientation × perceived orientation (F(1,19) = 9.335, p = 0.007, ηp2 = 0.329) in the Ping session, but not in the No-Ping session (F(1,19) = 0.017, p = 0.898, ηp2 = 0.001). These above-mentioned statistical results were reported in the original texts. In addition, this three-way mixed ANOVA (session × attended orientation × perceived orientation) on Mahalanobis distance in V1 revealed no significant main effects (session: F(1,38) = 0.009, p = 0.923, ηp2 < 0.001; attended orientation: F(1,38) = 0.116, p = 0.735, ηp2 = 0.003; perceived orientation: (F(1,38) = 1.106, p = 0.300, ηp2 = 0.028). We agree with the reviewer that a complete reporting of analyses enhances understanding of the data. Therefore, we have now included the main effects in the main texts (Page 11, Line 233).
We thank the reviewer for the suggestion regarding the inclusion of descriptive statistics for interaction effects. However, since the data were already visualized in Fig. 3B and 3C in the main texts, to maintain conciseness and consistency with the reporting style of other analyses in the texts, we have opted to include these statistics in the Supplementary Information (Page 5, Table 1).
Reviewer #3 (Public review):
(1) The title is "Dual-format Attentional Template," yet the supporting evidence for the nonsensory format and its guiding function is quite weak. The author could consider conducting further generalization analysis from stimulus selection to preparation stages to explore whether additional information emerges.
We thank the reviewer for this comment. Our approach to investigate whether preparatory attention is encoded in sensory or non-sensory format - by training classifier using separate runs of perception task – closely followed methods from previous studies (Stokes et al., 2009; Peelen et al., 2011; Kok et al., 2017). Following the reviewer’s suggestion, we performed generalization analyses by training classifiers on activity during the stimulus selection period and testing them preparatory activity. However, we observed no significant generalization effects in either No-Ping and Ping sessions (ps > 0.780). This null result may stem from a key difference in the neural representations: classifiers trained on neural activity from stimulus selection period necessarily encode both target and distractor information, thus relying on somewhat different information than classifier trained exclusively on isolated target information in the perception task.
(2) In Figure 2, the author did not find any decodable sensory-like coding in IPS and PFC, even during the impulse-driven session, indicating that these regions do not represent sensory-like information. However, in the final section, the author claimed that the impulse-driven sensorylike template strengthens informational connectivity between sensory and frontoparietal areas. This raises a question: how can we reconcile the lack of decodable coding in these frontoparietal regions with the reported enhancement in network communication? It would be helpful if the author provided a clearer explanation or additional evidence to bridge this gap.
We thank the reviewer for this comment. We would like to clarity that although we did not observe sensory-like coding during preparation in frontoparietal areas, we did observe attentional signals in these regions, as evidenced by the above-chance within-task attention decoding performance (Fig. 2 in the main texts). This could reflect different neural codes in different areas, and suggests that inter-regional communication does not necessarily require identical representational formats. It seems plausible that the representation of a non-sensory attentional template in frontoparietal areas supports top-down attentional control, consistent with theories suggesting increasing abstraction as the cortical hierarchy ascends (Badre, 2008; Brincat et al., 2018), and their interaction with the sensory representation in the visual areas is enhanced by the visual impulse.
(3) Given that the impulse-driven sensory-like template facilitated behavior, the author proposed that it might also enhance network communication. Indeed, they observed changes in informational connectivity. However, it remains unclear whether these changes in network communication have a direct and robust relationship with behavioral improvements.
We thank the reviewer for the suggestion. To examine how network communication relates to behavior, we performed a correlation analysis between information connectivity (IC) and RTs across participants (see Figure S5). We observed a trend of correlations between V1-PFC connectivity and RTs in the Ping session (r = -0.394, p = 0.086), but not in the NoPing session (r = -0.046, <i.p = 0.846). No significant correlations were found between V1-IPS and RTs (ps > 0.400) or between ICs and accuracy (ps > 0.399). These results suggests that ping-enhanced connectivity might contributed to facilitated responses. Although we may not have sufficient statistical power to warrant a strong conclusion, we think this result is still highly suggestive, so we now added the texts in the Supplementary Information (Page 8, Line 116121; S5 Fig) and mentioned this result in the main texts (Page 14, Line 292-293).
(4) I'm uncertain about the definition of the sensory-like template in this paper. Is it referring to the Ping impulse-driven condition or the decodable performance in the early visual cortex? If it is the former, even in working memory, whether pinging identifies an activity-silent mechanism is currently debated. If it's the latter, the authors should consider whether a causal relationship - such as "activating the sensory-like template strengthens the informational connectivity between sensory and frontoparietal areas" - is reasonable.
We apologize for the confusions. The sensory-like template by itself does not directly refer to representations under Ping session or the attentional decoding in early visual cortex. Instead, it pertains to the representational format of attentional signals during preparation. Specifically, its existence is inferred from cross-task generalization, where neural patterns from a perception task (perceive 45º or perceive 135º) generalize to an attention task (attend 45 º or attend 135º). We think this is a reasonable and accepted operational definition of the representational format. Our findings suggest that the sensory-like template likely existed in a latent state and was reactivated by visual pings, aligning more closely with the first account raised by the reviewer.
We agree with the reviewer that whether ping identifies an activity-silent mechanism is currently debated (Schneegans & Bays, 2017; Barbosa et al., 2021). It is possible that visual impulse amplified a subtle but active representation of the sensory template during attentional preparation and resulted in decodable performance in visual cortex. Distinguishing between these two accounts likely requires neurophysiological measurements, which are beyond the scope of the current study. We have explicitly addressed this limitation in our Discussion (Page 19, Line 395-399).
Nevertheless, the latent sensory-like template account remains plausible for three reasons. First, our interpretation aligns with theoretical framework proposing that the brain maintains more veridical, detailed target templates than those typically utilized for guiding attention (Wolfe, 2021; Yu et al., 2023). Second, this explanation is consistent with the proposed utility of latent working memory for prospective use, as maintaining a latent sensory-like template during preparation would be useful for subsequent stimulus selection. The latter point was further supported by the reviewer’s suggestion about whether “activating the sensory-like template strengthens the informational connectivity between sensory and frontoparietal areas is reasonable”. Our additional analyses (also refer to our response to Reviewer 3, Point 3) suggested that impulse-enhanced V1-PFC connectivity was associated with a trend of faster behavioral responses (r = -0.394, p = 0.086; see Supplementary Information, Page 8, Line 116-121; S5 Fig). Considering these findings in totality, we think it is reasonable to suggest that visual impulse may strengthen information flow among areas to enhance attentional control.
Recommendation for the Authors:
Reviewer #1 (Recommendation for the authors):
I hate to suggest another fMRI experiment, but in order to make strong claims about two states, I would want to see the methodological and interpretation confounds addressed. Ping condition - would a tone lead to the same result of sharpening the template? If so, then why? Can a ping be manipulated in its effectiveness? That would be an excellent manipulation condition.
We thank the reviewer for the comments. Please refer to our reply to Reviewer 1, Point 5 for detailed explanation.
Reviewer #2 (Recommendation for the authors):
It is strongly advised that these descriptive statistics related to the interaction effect should be included to facilitate a more effective understanding of their data.
We thank the reviewer for the comments. We now included the relevant descriptive statistics in the Supplementary Information, Table 1.
Reviewer #3 (Recommendation for the authors):
In addition to p-values, I see many instances of 'ps'. Does this indicate the plural form of p?
We used ‘ps’ to denote the minimal p-value across multiple statistical analyses, such as when applying identical tests to different region groups.
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