Dual-format attentional template during preparation in human visual cortex

Reviewer #1 (Public review):

Summary:

The aim of the experiment reported in this paper is to examine the nature of the representation of a template of an upcoming target. To this end, participants were presented with compound gratings (consisting of tilted to the right and tilted to the left lines) and were cued to a particular orientation - red left tilt or blue right tilt (counterbalanced across participants). There are two directly compared conditions: (i) no ping: where there was a cue, that was followed by a 5.5-7.5s delay, then followed by a target grating in which the cued orientation deviated from the standard 45 degrees; and (ii) ping condition in which all aspects were the same with the only difference that a ping (visual impulse presented for 100ms) was presented after the 2.5 seconds following the cue. There was also a perception task in which only the 45 degrees to the right or to the left lines were presented. It was observed that during the delay, only in the ping condition, were the authors able to decode the orientation of the to-be-reported target using the cross-task generalization. Attention decoding, on the other hand, was decoded in both ping and non-ping conditions. It is concluded that the visual system has two different functional states associated with a template during preparation: a predominantly non-sensory representation for guidance and a latent sensory-like for prospective stimulus processing.

Strengths:

There is so much to be impressed with in this report. The writing of the manuscript is incredibly clear. The experimental design is clever and innovative. The analysis is sophisticated and also innovative - the cross-task decoding, the use of Mahalanobis distance as a function of representational similarity, the fact that the question is theoretically interesting, and the excellent figures.

Weaknesses:

While I think that this is an interesting study that addresses an important theoretical question, I have several concerns about the experimental paradigm and the subsequent conclusions that can be drawn.

(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.

(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.

(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?

(4) If I understand correctly, the only ROI that showed a significant difference for the cross-task 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.

(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.

(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?

(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).

Reviewer #2 (Public review):

Summary:

In the present study, the authors investigated the nature of attentional templates during the preparatory period of goal-directed attention. By combining the use of 'pinging' the neural activity with a visual impulse and fMRI-based multivariate decoding, the authors found that the nature of the neural representations of the prospective feature target during the preparatory period was contingent on the presence of the 'pinging' impulse. While the preparatory representations contained highly similar information content as the perceptual representations when the pinging impulse was introduced, they fundamentally differed from perceptual representations in the absence of the pinging impulse. Based on these findings, the authors proposed a dual-format mechanism in which both a "non-sensory" template and a latent "sensory" template coexisted during attentional preparation. The former actively guides activity in the preparatory state, and the latter is utilized for future stimulus processing.

Strengths:

Overall, I think this is an interesting study that introduced a novel perspective concerning the nature of neural representations during attentional processing. Methodologically, the present study combines an innovative utilization of the pinging technique in working memory studies and fMRI-based multivariate pattern analysis. The method is sound and the results are convincing. While I appreciate the conceptual elegance of the dual-format idea proposed by the authors, there are several questions that need to be addressed more thoroughly to clarify some of the potential ambiguities of the results and to increase the plausibility of the author's theory.

Weaknesses:

(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.

(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.

(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.

Reviewer #3 (Public review):

This paper discusses how non-sensory and latent, sensory-like attentional templates are represented during attentional preparation. Using multivariate pattern analysis, they found that visual impulses can enhance the decoding generalization from perception to attention tasks in the preparatory stage in the visual cortex. Furthermore, the emergence of the sensory-like template coincided with enhanced information connectivity between V1 and frontoparietal areas and was associated with improved behavioral performance. It is an interesting paper with supporting evidence for the latent, sensory-like attentional template, but several problems still need to be solved.

(1) The title is "Dual-format Attentional Template," yet the supporting evidence for the non-sensory 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.

(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 sensory-like 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.

(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.

(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.