Species -Shared and -Unique Gyral Peaks on Human and Macaque Brains

  1. Songyao Zhang
  2. Tuo Zhang
  3. Guannan Cao
  4. Jingchao Zhou
  5. Zhibin He
  6. Xiao Li
  7. Yudan Ren
  8. Xi Jiang
  9. Lei Guo
  10. Junwei Han
  11. Tianming Liu

  • Curated by eLife

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    eLife assessment

    This potentially important paper compares cross-species cortical folding patterns in human and non-human primates, showing that most gyral peaks shared across species are in lower-order cortical regions. The supporting evidence is currently incomplete, requiring the addition of multiple comparison corrections and further clarification and elaboration upon the statistical procedures used.

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Abstract

Cortical folding is an important feature of primate brains that plays a crucial role in various cognitive and behavioral processes. Extensive research has revealed both similarities and differences in folding morphology and brain function among primates including macaque and human. The folding morphology is the basis of brain function, making cross-species studies on folding morphology are important for understanding brain function and species evolution. However, prior studies on cross-species folding morphology mainly focused on partial regions of the cortex instead of the entire brain. Previously, we defined a whole-brain landmark based on folding morphology: the gyral peak. It was found to exist stably across individuals and ages in both human and macaque brains. In this study, we identified shared and unique gyral peaks in human and macaque, and investigated the similarities and differences in the spatial distribution, anatomical morphology, and functional connectivity of them.

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  1. eLife

    eLife assessment

    This potentially important paper compares cross-species cortical folding patterns in human and non-human primates, showing that most gyral peaks shared across species are in lower-order cortical regions. The supporting evidence is currently incomplete, requiring the addition of multiple comparison corrections and further clarification and elaboration upon the statistical procedures used.

  2. eLife

    Reviewer #1 (Public Review):

    Zhang et al. tackle the important topic of primate-specific structural features of the brain and the link with functional specialization. The authors explore and compare gyral peaks of the human and macaque cortex through non-invasive neuroimagery, using convincing techniques that have been previously validated elsewhere. They show that nearly 60% of the macaque peaks are shared with humans, and use a multi-modal parcellation scheme to describe the spatial distribution of shared and unique gyral peaks in both species.

    The claim is made that shared peaks are mainly located in lower-order cortical areas whereas unique peaks are located in higher-order regions, however, no systematic comparison is made. The authors then show that shared peaks are more consistently found across individuals than unique peaks, and show a positive but small and non-significant correlation between cross-individual counts of the shared peaks of the human and the macaque i.e. the authors show a non-significant trend for shared peaks that are more consistently found across humans to be those that are also more found across macaques.

    In order to identify if unique and shared peaks could be identified based on the structural features of the cortical regions containing them, the authors compared them with t-tests. A correction for multiple comparisons should be applied and t-values reported. Graph-theoretical measures were applied to functional connectivity datasets (resting-state fMRI) and compared between unique and shared peak regions for each species separately. Again the absence of multiple comparison correction and t-values make the results hard to interpret. The same comment applies to the analysis reporting that shared peaks are surrounded by a larger number of brain regions than unique peaks. Finally, the potentially extremely interesting results about differential human gene expression of shared and unique peaks regions are not systematically reported e.g. the 28 genes identified are not listed and the selection procedure of 7 genes is not fully reported.

    The paper is well written and the methods used for data processing are very compelling i.e. the peak cluster extraction pipeline and cross-species registration. However, the analysis and especially the reporting of statistics, as they stand now, constitutes the main weakness of the paper. Some aspects of the statistical analysis need to be clarified.

  3. eLife

    Reviewer #2 (Public Review):

    Summary:

    The authors compared the cortical folding of human brains with folding in macaque monkey brains to reveal shared and unique locations of gyral peaks. The shared gyral peaks were located in cortical regions that are functionally similar and less changed in humans from those in macaques, while the locations of unique peaks in humans are in regions that have changed or expanded functions. These findings are important in that they suggest where human brains have changed more than macaque brains in their subsequent evolution from a common ancestor. The massive analysis of comparative results provides evidence of where humans and macaques are similar or different in cortical markers, as well as noting some of the variations within each of the two primates.

    Strengths:

    The study includes massive detail.

    Weaknesses:

    The manuscript is too long and there is not enough focus on the main points. A brief listing of previous views on why fissures form and what factors are important would be helpful.

  4. Version 2 published on bioRxiv
  5. Version 1 published on bioRxiv