Plis de passage in the Superior Temporal Sulcus: Morphology and local connectivity

  1. C. Bodin
  2. A. Pron
  3. M. Le Mao
  4. J Régis
  5. P. Belin
  6. O. Coulon

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Abstract

While there is a profusion of functional investigations involving the superior temporal sulcus (STS), our knowledge of the anatomy of this sulcus is still limited by a large variability across individuals. Several “plis de passage” (PPs), annectant gyri buried inside the fold, can separate the STS into distinct segments and could explain part of the observed variability. However, an accurate characterization is lacking to properly extract and fully understand the nature of PPs. The aim of the present study is twofold: i. to characterize the STS PPs by directly identifying them within individual STS, using the geometry of the surrounding surface and considering both deep and superficial PPs. ii. to test the hypothesis that PPs constitute local increases of the short-range structural connectivity. Performed on 90 subjects from the Human Connectome Project database, our study revealed that PPs constitute surface landmarks that can be identified from the geometry of the STS walls and that they constitute critical pathways of the U-shaped white-matter connecting the two banks of the STS. Specifically, a larger amount of fibers was extracted at the location of PPs compared to other locations in the STS. This quantity was also larger for superficial PPs than for deep buried ones. These findings raise new hypotheses regarding the relation between the cortical surface geometry and structural connectivity, as well as the possible role of PPs in the functional organization of the STS.

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  1. eLife

    ###Reviewer #3:

    The paper "Morphology and local connectivity of the plis de passage in the superior temporal sulcus" is an interesting and thoughtful paper which uses modern tractography methods quite skillfully to examine whether the finer features of gyrification are related to connectivity patterns. This is an understudied area of research in human MRI because it deals with inter-individual variability, and so is time consuming, not well-suited to existing analysis pipelines, and requires a high level of neuroanatomical expertise. The methods, which included impressive inter-rater reliability and a nice control condition, were well-suited to the question. I also very much appreciated the discussion section, which covered anatomical, historical, evolutionary, and developmental considerations quite effectively and with clarity of language. Overall, the paper is well thought out and executed and a joy to read!

    Below are some comments that could improve clarity for the reader:

    -Figure 2 is a bit difficult to understand - to clarify that a and b are from the first brain, and b and c are from the second brain, the authors might consider labeling them or putting them in boxes. It might be helpful to add some arrows to help illustrate the "pinching" they describe.

    -End of results, p. 19, final paragraph. The authors write "Second, there was generally an increasing number of U-shape fibers from the anterior to the posterior part of the STS." I don't think the authors tested this, so I would rephrase this to say "on visual inspection, it appears that there was an increase in...". I would also replace the word "fibers" with "streamlines".

  2. eLife

    ###Reviewer #2:

    A new characterization of the "plis de passage"(PP) is proposed. The interest of this new definition is demonstrated in a cortical area where a huge amount of variability exists, hence it is very difficult to study. The results shown are convincing. The new connection established between PP and U-fibers contributes to the understanding of the link between gross anatomy and connectivity.

    Several questions for clarification:

    1. The distribution of the number of PP in STS is given in the results. Did you try to match the PP across the subjects, to try to define a stable model? In terms of the location of the PPs, is a model possible or their positions span the whole main branch of STS in a continuum? Did you try to study the relationships between PP and sulcal pits?

    2. Did you try to clarify whether all dense clusters of U-fibers correspond to PP across subjects? Due to the random selection of the extremities of the control PPs, such clusters with different trajectories (not necessarily facing each other) could be missed by your procedure in controls?

    3. Is there a link found between the superficiality of a PP and the extent of the shift of the two extremities along the sulcus (the S and C shapes)?

  3. eLife

    ###Reviewer #1:

    The study aims to improve the anatomical characterisation of STS plis de passage (PPs). Morphologically, the authors use the geometry of the surrounding surface to reveal deep PPs, which might be buried. Structurally, they explore associations with short-range u-shape connectivity across the two banks of the STS. This methodological advancements follow from previous work on the central sulcus (e.g. Zlatkina et al., 2016, European JNS; Catani et al., 2012, Cortex). The authors provide detailed characterisation of these anatomical features in 90 individuals from the HCP dataset, and focus their analysis in differences across the two hemispheres. But the study stops short of showing how this impacts functional organisation or behaviour. Overall, the methodological advancement offered here is incremental relative to other studies, and very little insight is provided about the impact of these morphological features and their variations on STS functional organisation. Considering the HCP offers high quality functional data, including tasks specifically relating to STS function, as well other highly related data (e.g. twins), I thought the present manuscript missed numerous precious opportunities to leverage the present findings into more significant impact and innovation.

    Major Comments:

    1. The abstract and introduction highlight the importance of studying inter-individual variability in PPs. But the results do not address this variability, as all the results are dedicated to inter-hemispheric differences. What is the significance of inter-individual structural variance, and how is it informed by experience (the introduction suggests that these folding patterns are determined in utero?)? For example, are they more similar in twins? Is there any clear evidence that it determines functional organisation and behaviour? Clinical symptoms? Also, are the inter-individual variations observed specific to the STS? Or do they reflect 'trait' like foldiness of the cortex? None of these questions are explored empirically, and as such, the present findings offer very little advancement to our understanding of STS function and functionality.

    2. I'm not sufficiently qualified to determine, but I have to wonder if the 'control PPs' are suitable, considering they are much smaller than the 'true PPs'? Considering the probabilistic nature of the analysis and the fact that the experimenters were not blinded as to which aspect of the sulcus was 'true' or 'control', some more consideration should be given to the appropriateness of this control.

    3. The u-shape analysis requires histological confirmation, as demonstrated by Catani et al. for the central sulcus.

    4. Nonsignificant results (e.g. between hemispheres) require further consideration - are the two hemispheres truly similar, or is the study underpowered to find such differences? Bayesian statistics can inform this question.

    5. I found the discussion to be overly speculative, and in particular the part relating to functional implications to be overly speculative, considering the very modest innovative contribution the current study offered.

  4. 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 very much appreciated the careful analysis, including very laborious manual segmentation. They agreed that the study provides a new level of detail of STS morphology that hasn’t been available to date. They also agreed that this characterisation has potential to support future research focusing on the inter-individual variability that is so common in this brain region. However, the study has not yet delivered on this promise, as the analysis is focused on inter-hemispheric differences across the group, without illuminating the impact of inter-individual morphological variability on the area's functional organisation or function.

  5. Version published to 10.1101/2020.05.26.116152 on bioRxiv