Anatomical correlates of face patches in macaque inferotemporal cortex

  1. Michael J. Arcaro
  2. Theodora Mautz
  3. Vladimir K. Berezovskii
  4. Margaret S. Livingstone

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Abstract

This study reports the discovery that buried gyral folds along the superior temporal sulcus in macaque lateral temporal cortex predict the locations of regions selectively responsive to faces. These findings demonstrate a link between cortical topology and the functional organization of higher-order visual cortex in macaques. We show that these anatomical landmarks are established prenatally and are likely the result of general developmental mechanisms such as molecular signaling gradients, topographic maps, and the formation of cortical areas. These folds are found across primate species. Identification of such anatomical landmarks may provide insight into evolutionary changes in the functional organization of high-level visual cortex.

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  1. Version published to 10.1073/pnas.2018780117
  2. eLife

    ###Reviewer #3:

    In this paper, Arcaro and colleagues investigate the relationship between bumps along the macaque STS and functional selectivity for faces. Through a series of analyses, they convincingly demonstrate a strong structural-functional relationship between face patches and these small sulcal bumps. They show that this correspondence outperforms functional probabilistic atlases, and does not result from functional specialization per se, as visually-deprived monkeys show similar anatomical folding patterns. As someone familiar with the field of vision and cognitive neuroscience, I can say that this paper is thorough, employs careful single-subject analyses, and I honestly do not have much to add to improve what is already a great paper.

    Points:

    For clarification, were the borders of each bump drawn by hand on the cortical surface (e.g. what's show in Figure 2B)? Saying so in the text will help future researchers replicate the identification process.

    Monkey M3 looks odd; what do you think is going on there? I know there is individual variability, but the AL patch in that monkey seems atypical in its position in both hemispheres. For most monkeys it almost looks like you could mirror their STS from one hemisphere and predict relatively well their other hemisphere, but in M3 the AL patch doesn't look symmetric.

    The previous point got me thinking, was data across hemispheres within a monkey collapsed before statistical testing? Are there hemispheric differences in bump volume or spacing? Apologies if I missed that in the text.

    In the visually-deprived monkeys, were there any anatomical differences at all within the bumps? Volume differences? Thickness of the cortex that comprises a bump? If this is the topic of another paper and the authors excluded it purposely, I understand, but it might speak to how functional emergence interacts with existing structure (in this case the bumps).

    Did I miss something, or is there really a reference to Julius Caesar's Gaul in the discussion? Is that what "Gallia" is referring to? I appreciate a deep historical reference (if that's what this is) but I'm worried that this will go over most readers' heads. Happy to leave it for poetic purposes, but just noting that it will likely be confusing.

  3. eLife

    ###Reviewer #2:

    Summary:

    Neuroimaging and electrophysiological experiments demonstrate a series of face-selective regions in the macaque superior temporal sulcus (STS). In normalised space, these regions partially align across individuals. The present report demonstrates that for some of these regions, local surface properties ("bumps") provide additional reliable information about the likely location of face-selective patches (in fMRI) and cells (in intracranial recordings). That pre-cursors of these bumps are identified both pre-natally, and in macaques reared with abnormal visual experience of faces, indicates that these bumps do not arise due to the normal development of face-selective cortical activity. Similar bumps are found in some other primates, although much of the relevant imaging and electrophysiology data that would help to assess homologies is not yet available.

    General assessment:

    This is a well-presented study that addresses a topic of ongoing interest with highly rigorous methods. On a narrow reading that holds close to the data, the paper offers an interesting observation that would seem to have mainly practical implications (e.g. in informing localisation for future electrophysiological work). In contrast, the effort to draw wider theoretical implications for understanding the visual organisation of STS seems to rely on unpicking the main observation that prompted the report in the first place, and on inferences and speculations that extend too far beyond the data that are reported.

    Substantive points:

    If "bumps" are the relevant physiological markers -- and demonstrating this is the thrust of most of the paper -- then it seems important to understand what a "bump" is. That is, what underlying properties or developmental processes are implied by the presence of a cortical bump, in contrast to regions with less prominent local curvature? The authors only very briefly review some possible mechanisms in the Discussion, and I felt more a complete exploration of this issue would have been useful.

    However, having established a structure-function correlation empirically, at the same time the paper provides many indirect lines of evidence to suggest that this relationship may be tangential at best. As the authors note, "STS bumps are not sufficient to produce face selectivity in the absence of face experience". Nor are bumps necessary to produce face selectivity, given the apparent absence of bumps related to MF and AF. Further, the overlap between bumps and faces patches is variable over individuals, and incomplete: the bumps are large, and not entirely comprised of face-selective populations. The authors also note studies that reveal broadly similar tri-partite STS organisation of retinotopic responses, and of body and colour-selective patches. For example, images of bodies tend (in macaque fMRI) to activate regions that are adjacent to face patches, suggesting that there would be a similar anatomy/function relationship for this visual category too. Finally, the authors note that the kinds of physiological processes that are likely to produce bumps are too generic to produce a face-specific mechanism. The authors' speculation, in light of such considerations, is that anatomical bumps in STS are in fact the indirect signals of three distinct, coherent, and complex visual areas that may contribute to a range of visual processes. The main difficulty with the manuscript, as I see it, is that while these wider possibilities are what give the paper the potential to engage a broad neuroscience audience, they are simply too far removed from the actual observations that are reported here. Substantial additional evidence would need to be mustered to support the (admittedly interesting) picture of arealisation in STS that the authors paint. Without such evidence, what remains is mainly a structure-function observation that is interesting, and perhaps practically useful for further studies, but with uncertain theoretical implications.

  4. eLife

    ###Reviewer #1:

    This paper reports a correspondence between structural markers, convexities ("bumps") along the superior temporal sulcus (STS), and face-selective patches in the macaque inferior temporal cortex. They localized three face patches with fMRI and each of these face patches overlapped with one of three bumps. These bumps were also present in monkeys that lacked face patches because of being reared without exposure to faces. These data provide some evidence for a correspondence between structure and function in inferior temporal cortex in macaques, in line with recent evidence for a link between structure and function in the temporal lobe of humans. This is interesting work showing novel data on a potential correspondence between structure and function in macaque temporal cortex. They examined, for monkey studies, a relatively large number of subjects and employed two functional measurements, fMRI and multi-unit recordings. However, I have some concerns regarding the correspondence between the face patches and the anatomical structure that need to be addressed.

    Main comments:

    1. The authors employed an automatic procedure to compute the convexity of the pial/white matter, which is excellent because it is objective. However, I found it difficult to differentiate neighboring bumps in some of the animals (Figure 2 S1). One reason for this is the way Figure2 S1 was made, showing the bumps with different colors that occlude to some extent the underlying convexity map. The authors should show the convexity map for each monkey and then in a separate panel show the identified bumps, so that one can judge the correspondence between the convexity map and the bumps. Also, the group average data shown in Figure 2C look not very convincing to me: I find it difficult to differentiate the posterior from the middle bump: it looks like one long continuous convexity instead of two with a clear border in between. This could be due to the averaging across monkeys. That is why Figure 2S1, that shows the data of the individual monkeys, is important but that figure needs to be improved by showing the convexity maps alone (see above).

    2. The overlap between the bump surfaces and the patches depend on how the two are defined. As said above, I found it difficult to identify the individual bumps. The surface area/size of a face patch depends on the statistical threshold (and number of runs etc) that is used to define it and thus is arbitrary to some extent. These two factors make it difficult to evaluate the degree of overlap between patches and bumps and to interpret the DICE overlap analysis. The authors should address this by using several thresholds to define the face patch surface and examine how this affects the DICE outcome and analyses using centroids.

    3. Because the face patches appear to be a (in some cases) small part of a bump and its location can vary within the bump, how predictive is the bump then about the location of the face patch? The correspondence between structure and function appears to be rather coarse: I have the impression from the comparison of the centroids of the bumps and face patches (Figure 4) that there is a reasonable correspondence between ML and the middle bump, but that it is weaker for PL and AL. Furthermore, it is highly variable amongst animals. For instance, in M3, face patch AL appears to lie in between the middle and anterior bump. This suggests that the bumps might not determine the presence of a face patch but that perhaps the presence of a bump and a face patch are unrelated mechanistically.

    4. The authors' work ignores the most anterior face patch, AM, which is located outside the STS (as in fact also PL typically is (in fact, also in the present study)). It has been suggested that AM is important for face identification, having a high tolerance for identity-preserving transformations such as viewpoint (see the work by Freiwald and Tsao), and thus is difficult to ignore. How does AM fit into the proposed correspondence between STS bumps and face patches?

  5. eLife

    ##Preprint Review

    This preprint was reviewed using eLife’s Preprint Review service, which provides public peer reviews of manuscripts posted on bioRxiv for the benefit of the authors, readers, potential readers, and others interested in our assessment of the work. This review applies only to version 1 of the manuscript.

    ###Summary:

    The reviewers agreed that the paper reports an interesting finding: a potential correspondence between structure and function in macaque temporal cortex. However, they also noted that this correspondence was only partial and variable across individuals. Furthermore, the reviewers were unsure of the broader theoretical implications of this finding.

  6. Version published to 10.1101/2020.06.10.144600 on bioRxiv