Orienting Gaze Toward a Visual Target: Neurophysiological Synthesis with Epistemological Considerations

Round 1

Reviewer 1 Report

Comments and Suggestions for Authors

Orienting gaze toward a visual target: Neurophysiological synthesis with epistemological considerations is a well written review article. The central line of argument is that most scholars of the visual system make an epistemological error in their interpretation of neual activation related to change in gaze direction, such that they interpret neural activity as a signal that encodes gaze position. The author argues this is inappropriate and marshsalls several lines of evidence in support of this critique. They then offer an alternative viewpoint, which is that the neural activation reflects a drive to return the visual system to a state of homeostasis in which visually related activitiy is distributed equally across the cerebral hemispheres. 

I found this to be a very thought provoking and well argued review that challenges the reader to consider the assumptions guiding thier beliefs about the functioning of the oculomotor system. However, it was not clear to me how latter part of the review (on orienting in  cats) related to the conceptual ideas outlined in the parts 1 to 3. This the biggest issue i saw with the review 

Other comments / suggestions 

Line 25- remove ‘entire’

Does the review refer only to reflexive orienting? (i.e orienting driven by external stimuli). It's not clear to me how an endogenously generated eye-movement to one of two equally salient objects that are equidistant from fixation but in opposite hemifields (for example, in the remote distractor paradigm) could be said to be restoring homeostasis. 

 P59” sufficient to symmetrize back the functional neuronal image of the stimulus 59 within the sensorimotor networks”: Is the argument here that the visual system seeks to have equal and symmetrical amounts of neural activation in the visual cortices? How does this work for higher level visuo-spatial representations which are biased towards the right hemisphere?

105 “notions that are foreign to the brain function” is unclear

 Line 136-162 – seems to make the argument that the brain does not contain an internal representation, topographical of external space. How can this be reconciled with the imaging and neurophysiological evidence for spatial maps throughout the dorsal visual system, and evidence that several brain areas maintain activation during delay period in memory guided saccade tasks. Perhaps i have misunderstood something here? 

Poly-equilibruim. An interesting idea, but doesn’t it imply that any disruption to the equilibrium of the visual system will lead to imbalance in the direction of gaze? This would seem to predict a very significant gaze offset in patients with lateralised brain lesions of the visual system. While some patients (e.g. with neglect) show this offset, others (e.g hemianopes) do not. In hemianopes, fixational errors are asymmetric towards the blind hemifield (Reinhard, Damm, Ivanov, & Trauzettel-Klosinski, 2014)

“Any suppression of activities within the set of commands participating to this poly-equilibrium alters the direction of gaze while fixating a target if it is not counterbalanced”

 Reinhard, J. I., Damm, I., Ivanov, I. V., & Trauzettel-Klosinski, S. (2014). Eye Movements During Saccadic and Fixation Tasks in Patients With Homonymous Hemianopia. Journal of Neuro-Ophthalmology, 34(4), 354-361. doi:10.1097/wno.0000000000000146

Line 406 “incitation to coordinate (in the metrological sense) the set of numerical values brought by behavioral measurements and neuronal activities”

I didn’t understand this sentence – could it be made more accessible?

416-422:  The line of argument was unclear to me here. The author seems to endorse a population coding view of oculomotor control. Is that the intention of this section?

I found the line of argument advanced in section 3.1 hard to follow . I think the section would benefit from a line or two at the end that summarized the arguments and main conclusion the author wishes to draw from this evidence

Line 565-566 was hard to understand

974- suggest amending  treasure’ to ‘treasure trove’

Section 4.3 seemed to digress away from the central line of argument that gaze control arises from a drive to maintain poly-equilibrium in the visual system. The key argument of this section seems to be that it is hard to study combined eye-head movements. It was not clear to me how this section advanced the main line of argument. This is a long and rather descriptive section and unless it can be convincingly linked to the main line of argument I would suggest removing it.

The quote in the conclusion seems unnecessary given it appears earlier in the article

Line 1146-1147 is not necessary.

It would be beneficial for the conclusion to briefly summarise the lines of argument in favour of the poly-equilibrium approach, as well as summarining the epistemological problems with idea that neural activity encodes gaze orientation

Comments on the Quality of English Language

The english is excellent. A couple of sentences were a bit dense and would benefit from a refdraft to make them more accessible 

Author Response

Please see the attachment. 

Author Response File: Author Response.pdf

Reviewer 2 Report

Comments and Suggestions for Authors

See attachment

Comments for author File: Comments.pdf

Comments on the Quality of English Language

I have worked on language.

Author Response

Please see the attachment.

Author Response File: Author Response.pdf

Reviewer 3 Report

Comments and Suggestions for Authors

This paper highlights the importance of understanding the neurophysiological mechanisms underlying gaze and head orientation in response to stimuli. The review addresses the distinction between behavioral and neurophysiological interpretations, emphasizing that gaze orientation involves complex intrinsic processes rather than a straightforward one-to-one correspondence with neural activity. Some comments follow.

 

The introduction and abstract are dense. Simplifying the language and summarizing the main objective and findings would make the text more accessible. Starting the introduction with a direct presentation of the critical problem would help capture the reader’s attention.

 

The paper could benefit from a critical literature analysis, highlighting any methodological limitations and potential inconsistencies in the cited studies. This would balance the discussion and allow for a better framing of the findings presented.

 

The conclusion should summarize the main points and suggest potential applications and directions for future research. Including pupillary dilation as a possible indicator of attentional orienting and saccade preparation (Dalmaso et al., 2020; Mathôt et al., 2013) could offer an exciting perspective for future studies and enhance the paper’s overall contribution.

 

References

Dalmaso, M., Castelli, L., & Galfano, G. (2020). Microsaccadic rate and pupil size dynamics in pro-/anti-saccade preparation: the impact of intermixed vs. blocked trial administration. Psychological Research, 84(5), 1320-1332.

Mathôt, S., Van der Linden, L., Grainger, J., & Vitu, F. (2013). The pupillary light response reveals the focus of covert visual attention. PloS one, 8(10), e78168.

Author Response

Please see the attachment.

Author Response File: Author Response.pdf

Round 2

Reviewer 1 Report

Comments and Suggestions for Authors

The author has done an excellent job revising the manuscript and has convincingly addressed all the issues i raised in the review

Author Response

The author thanks the reviewer #1 for taking the time to review his article and for raising issues that contributed to enhance its impact. He also thanks her/him for her/his appreciation of excellence and transmits his best regards.

 

Reviewer 2 Report

Comments and Suggestions for Authors

See attachment. Please, add all the files sent via e-mail. There are important notifications in there.

Comments for author File: Comments.zip

Comments on the Quality of English Language

A much-improved manuscript. But some crucial issues remain. 

Author Response

The author thanks the reviewer #2 for taking the time to review this article, for raising issues that contributed to improve its readability and for her/his numerous editorial corrections. 

The author thanks the reviewer #2 for sending links to videos and figures illustrating the pulling action of each extraocular muscle. The author already knew the figures, exception made of the photo showing the baby. He enjoyed watching the videos. However, the aim of Figure 4 is not to document the pulling action of each muscle separately but to illustrate the total configuration of muscles when gaze is directed to the right (A), upward (B) and downward (C). For each case, the readers can see the muscles whose contraction increases, those whose contraction does not change and those that relax. Small modifications have been made in the figure, but more modifications have been made in the text to remove some errors that possibly caused confusion.

Regarding the comment on the terminology, the author has followed the reviewer's advice and used the standard terminology throughout the text (intorsion instead of incycloduction and extorsion instead of excycloduction).

Finally, as suggested by the reviewer, the word "formidable" replaces the word "tremendous" in the abstract.

The author reiterates his gratitude for the reviewer's care to improve the article.

Reviewer 3 Report

Comments and Suggestions for Authors

I suggest publication

Author Response

The author thanks the reviewer 3 for taking the time to review this article and for raising issues that contributed to enhance its impact. He also thanks her/him for supporting its publication and transmit his best regards to her/him.

Round 3

Reviewer 2 Report

Comments and Suggestions for Authors

n/a

Comments on the Quality of English Language

Have the language editor go over the manuscript for minor adjustments.