Feedback of peripheral saccade targets to early foveal cortex

Reviewer #1 (Public review):

Summary:

The main contributions of this paper are: (1) a replication of the surprising prior finding that information about peripherally-presented stimuli can be decoded from foveal V1 (Williams et al 2008), (2) a new demonstration of cross-decoding between stimuli presented in the periphery and stimuli presented at the fovea, (3) a demonstration that the information present in the fovea is based on shape not semantic category, and (4) a demonstration that the strength of foveal information about peripheral targets is correlated with the univariate response in the same block in IPS.

Strengths:

The design and methods appear sound, and finding (2) above is new, and importantly constrains our understanding of this surprising phenomenon. The basic effect investigated here is so surprising that even though it has been replicated several times since it was first reported in 2008, it is useful to replicate it again.

Weaknesses:

(1) The paper, including in the title ("Feedback of peripheral saccade targets to early foveal cortex") seems to assume that the feedback to foveal cortex occurs in conjunction with saccade preparation. However, participants in the original Williams et al (2008) paper never made saccades to the peripheral stimuli. So, saccade preparation is not necessary for this effect to occur. Some acknowledgement and discussion of this prior evidence against the interpretation of the effect as due to saccade preparation would be useful. (e.g., one might argue that saccade preparation is automatic when attending to peripheral stimuli.)

(2) The most important new finding from this paper is the cross-decodability between stimuli presented in the fovea and stimuli presented in the periphery. This finding should be related to the prior behavioral finding (Yu & Shim, 2016) that when a foveal foil stimulus identical to a peripheral target is presented 150 ms after the onset of the peripheral target, visual discrimination of the peripheral target is improved, and this congruency effect occurred even though participants did not consciously perceive the foveal stimulus (Yu, Q., & Shim, W. M., 2016). Modulating foveal representation can influence visual discrimination in the periphery (Journal of Vision, 16(3), 15-15).

(3) The prior literature should be laid out more clearly. For example, most readers will not realize that the basic effect of decodability of peripherally-presented stimuli in the fovea was first reported in 2008, and that that original paper already showed that the effect cannot arise from spillover effects from peripheral retinotopic cortex because it was not present in a retinotopic location between the cortical locus corresponding to the peripheral target and the fovea. (For example, this claim on lines 56-57 is not correct: "it remains unknown 1) whether information is fed back all the way to early visual areas".) What is needed is a clear presentation of the prior findings in one place in the introduction to the paper, followed by an articulation and motivation of the new questions addressed in this paper. If I were writing the paper, I would focus on the cross-decodability between foveal and peripheral stimuli, as I think that is the most revealing finding.

Reviewer #2 (Public review):

Summary:

This study investigated whether the identity of a peripheral saccade target object is predictively fed back to the foveal retinotopic cortex during saccade preparation, a critical prediction of the foveal prediction hypothesis proposed by Kroell & Rolfs (2022). To achieve this, the authors leveraged a gaze-contingent fMRI paradigm, where the peripheral saccade target was removed before the eyes landed near it, and used multivariate decoding analysis to quantify identity information in the foveal cortex. The results showed that the identity of the saccade target object can be decoded based on foveal cortex activity, despite the fovea never directly viewing the object, and that the foveal feedback representation was similar to passive viewing and not explained by spillover effects. Additionally, exploratory analysis suggested IPS as a candidate region mediating such foveal decodability. Overall, these findings provide neural evidence for the foveal cortex processing the features of the saccade target object, potentially supporting the maintenance of perceptual stability across saccadic eye movements.

Strengths:

This study is well-motivated by previous theoretical findings (Kroell & Rolfs, 2022), aiming to provide neural evidence for a potential neural mechanism of trans-saccadic perceptual stability. The question is important, and the gaze-contingent fMRI paradigm is a solid methodological choice for the research goal. The use of stimuli allowing orthogonal decoding of stimulus category vs stimulus shape is a nice strength, and the resulting distinctions in decoded information by brain region are clean. The results will be of interest to readers in the field, and they fill in some untested questions regarding pre-saccadic remapping and foveal feedback.

Weaknesses:

The conclusions feel a bit over-reaching; some strong theoretical claims are not fully supported, and the framing of prior literature is currently too narrow. A critical weakness lies in the inability to test a distinction between these findings (claiming to demonstrate that "feedback during saccade preparation must underlie this effect") and foveal feedback previously found during passive fixation (Williams et al., 2008). Discussions (and perhaps control analysis/experiments) about how these findings are specific to the saccade target and the temporal constraints on these effects are lacking. The relationship between the concepts of foveal prediction, foveal feedback, and predictive remapping needs more thorough treatment. The choice to use only 4 stimuli is justified in the manuscript, but remains an important limitation. The IPS results are intriguing but could be strengthened by additional control analysis. Finally, the manuscript claims the study was pre-registered ("detailing the hypotheses, methodology, and planned analyses prior to data collection"), but on the OSF link provided, there is just a brief summary paragraph, and the website says "there have been no completed registrations of this project".

Specifics:

(1) In the eccentricity-dependent decoding results (Figure 2B), are there any statistical tests to support the results being a U-shaped curve? The dip isn't especially pronounced. Is 4 degrees lower than the further ones? Are there alternative methods of quantifying this (e.g., fitting it to a linear and quadratic function)?

(2) In the parametric modulation analysis, the evidence for IPS being the only region showing stronger fovea vs peripheral beta values was weak, especially given the exploratory nature of this analysis. The raw beta value can reflect other things, such as global brain fluctuations or signal-to-noise ratio. I would also want to see the results of the same analysis performed on the control condition decoding results.

(3) Many of the claims feel overstated. There is an emphasis throughout the manuscript (including claims in the abstract) that these findings demonstrate foveal prediction, specifically that "image-specific feedback during saccade preparation must underlie this effect." To my understanding, one of the key aspects of the foveal prediction phenomenon that ties it closely to trans-saccadic stability is its specificity to the saccade target but not to other objects in the environment. However, it is not clear to what degree the observed findings are specific to saccade preparation and the peripheral saccade target. Should the observers be asked to make a saccade to another fixation location, or simply maintain passive fixation, will foveal retinotopic cortex similarly contain the object's identity information? Without these control conditions, the results are consistent with foveal prediction, but do not definitively demonstrate that as the cause, so claims need to be toned down.

(4) Another critical aspect is the temporal locus of the feedback signal. In the paradigm, the authors ensured that the saccade target object was never foveated via the gaze-contingent procedure and a conservative data exclusion criterion, thus enabling the test of feedback signals to foveal retinotopic cortex. However, due to the temporal sluggishness of fMRI BOLD signals, it is unclear when the feedback signal arrives at the foveal retinotopic cortex. In other words, it is possible that the feedback signal arrives after the eyes land at the saccade target location. This possibility is also bolstered by Chambers et al. (2013)'s TMS study, where they found that TMS to the foveal cortex at 350-400 ms SOA interrupts the peripheral discrimination task. The authors should qualify their claims of the results occurring "during saccade preparation" (e.g., pg 1 ln 22) throughout the manuscript, and discuss the importance of temporal dynamics of the effect in supporting stability across saccades.

(5) Relatedly, the claims that result in this paradigm reflect "activity exclusively related to predictive feedback" and "must originate from predictive rather than direct visual processes" (e.g., lines 60-65 and throughout) need to be toned down. The experimental design nicely rules out direct visual foveal stimulation, but predictive feedback is not the only alternative to that. The activation could also reflect mental imagery, visual working memory, attention, etc. Importantly, the experiment uses a block design, where the same exact image is presented multiple times over the block, and the activation is taken for the block as a whole. Thus, while at no point was the image presented at the fovea, there could still be more going on than temporally-specific and saccade-specific predictive feedback.

(6) The authors should avoid using the terms foveal feedback and foveal prediction interchangeably. To me, foveal feedback refers to the findings of Williams et al. (2008), where participants maintained passive fixation and discriminated objects in the periphery (see also Fan et al., 2016), whereas foveal prediction refers to the neural mechanism hypothesized by Kroell & Rolfs (2022), occurring before a saccade to the target object and contains task irrelevant feature information.

(7) More broadly, the treatment of how foveal prediction relates to saccadic remapping is overly simplistic. The authors seem to be taking the perspective that remapping is an attentional phenomenon marked by remapping of only attentional/spatial pointers, but this is not the classic or widely accepted definition of remapping. Within the field of saccadic remapping, it is an ongoing debate whether (/how/where/when) information about stimulus content is remapped alongside spatial location (and also whether the attentional pointer concept is even neurophysiologically viable). This relationship between saccadic remapping and foveal prediction needs clarification and deeper treatment, in both the introduction and discussion.

(8) As part of this enhanced discussion, the findings should be better integrated with prior studies. E.g., there is some evidence for predictive remapping inducing integration of non-spatial features (some by the authors themselves; Harrison et al., 2013; Szinte et al., 2015). How do these findings relate to the observed results? Can the results simply be a special case of non-spatial feature integration between the currently attended and remapped location (fovea)? How are the results different from neurophysiological evidence for facilitation of the saccade target object's feature across the visual field (Burrow et al., 2014)? How might the results be reconciled with a prior fMRI study that failed to find decoding of stimulus content in remapped responses (Lescroart et al, 2016)? Might this reflect a difference between peripheral-to-peripheral vs peripheral-to-foveal remapping? A recent study by Chiu & Golomb (2025) provided supporting evidence for peripheral-to-fovea remapping (but not peripheral-to-peripheral remapping) of object-location binding (though in the post-saccadic time window), and suggested foveal prediction as the underlying mechanism.

Reviewer #3 (Public review):

Summary:

In this paper, the authors used fMRI to determine whether peripherally viewed objects could be decoded from the foveal cortex, even when the objects themselves were never viewed foveally. Specifically, they investigated whether pre-saccadic target attributes (shape, semantic category) could be decoded from the foveal cortex. They found that object shape, but not semantic category, could be decoded, providing evidence that foveal feedback relies on low-mid-level information. The authors claim that this provides evidence for a mechanism underlying visual stability and object recognition across saccades.

Strengths:

I think this is another nice demonstration that peripheral information can be decoded from / is processed in the foveal cortex - the methods seem appropriate, and the experiments and analyses are carefully conducted, and the main results seem convincing. The paper itself was very clear and well-written.

Weaknesses:

There are a couple of reasons why I think the main theoretical conclusions drawn from the study might not be supported, and why a more thorough investigation might be needed to draw these conclusions.

(1) The authors used a blocked design, with each object being shown repeatedly in the same block. This meant that the stimulus was entirely predictable on each block, which weakens the authors' claims about this being a predictive mechanism that facilitates object recognition - if the stimulus is 100% predictable, there is no aspect of recognition or discrimination actually being tested. I think to strengthen these claims, an experiment would need to have unpredictable stimuli, and potentially combine behavioural reports with decoding to see whether this mechanism can be linked to facilitating object recognition across saccades.

(2) Given that foveal feedback has been found in previous studies that don't incorporate saccades, how is this a mechanism that might specifically contribute to stability across saccades, rather than just being a general mechanism that aids the processing/discrimination of peripherally-viewed stimuli? I don't think this paper addresses this point, which would seem to be crucial to differentiate the results from those of previous studies.