Cross-species functional alignment reveals evolutionary hierarchy within the connectome
Authors: Karl-Heinz Nenning
Ernst Schwartz
Daniel S Margulies
Ting Xu
Joshua T Vogelstein
Charles E Schroeder
Damien A Fair
Georg Langs
Alexandros Goulas
Michael P Milham
Jonny Smallwood
Seok-Jun Hong
Journal: NeuroImage (2020)
Discipline: NEUROSCIENCE & BEHAVIOR
Keywords: Cross-species alignment; Default mode network; Evolution; Hierarchy; Joint embedding.
Affiliations: Center for the Developing Brain, Child Mind Institute, New York, NY, USA. Electronic address: ., Computational Imaging Research Lab, Department of Biomedical Imaging and Image-guided Therapy, Medical University of Vienna, Austria., Center for the Developing Brain, Child Mind Institute, New York, NY, USA., Department of Biomedical Engineering, Institute for Computational Medicine, Kavli Neuroscience Discovery Institute, Johns Hopkins University, MD, USA., Institute of Computational Neuroscience, University Medical Center Hamburg-Eppendorf, Hamburg University, Hamburg, Germany., Advanced Imaging Research Center, Oregon Health & Science University, Portland, OR, USA., Center for Biomedical Imaging and Neuromodulation, Nathan Kline Institute, Orangeburg, NY, USA; Departments of neurosurgery and Psychiatry, Columbia University College of Physicians and Surgeons, New York, NY, USA., Centre National de la Recherche Scientifique (CNRS) UMR 7225, Frontlab, Institut du Cerveau et de la Moelle Epini√®re, Paris, France., Department of Psychology, Queen's University, Kingston, Ontario, Canada; Psychology Department, University of York, York, UK., Center for the Developing Brain, Child Mind Institute, New York, NY, USA; Center for Biomedical Imaging and Neuromodulation, Nathan Kline Institute, Orangeburg, NY, USA., Computational Imaging Research Lab, Department of Biomedical Imaging and Image-guided Therapy, Medical University of Vienna, Austria; Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, Cambridge, MA, USA.

Abstract:  Evolution provides an important window into how cortical organization shapes function and vice versa. The complex mosaic of changes in brain morphology and functional organization that have shaped the mammalian cortex during evolution, complicates attempts to chart cortical differences across species. It limits our ability to fully appreciate how evolution has shaped our brain, especially in systems associated with unique human cognitive capabilities that lack anatomical homologues in other species. Here, we develop a function-based method for cross-species alignment that enables the quantification of homologous regions between humans and rhesus macaques, even when their location is decoupled from anatomical landmarks. Critically, we find cross-species similarity in functional organization reflects a gradient of evolutionary change that decreases from unimodal systems and culminates with the most pronounced changes in posterior regions of the default mode network (angular gyrus, posterior cingulate and middle temporal cortices). Our findings suggest that the establishment of the default mode network, as the apex of a cognitive hierarchy, has changed in a complex manner during human evolution - even within subnetworks. 

Retracted: No

PubPeer comments:
 In section 3.7, the text states:  We found that mean FCHI was negatively correlated with importance rank ( Fig. 4 C, Spearman r = u2212 0.648, p 0.001), suggesting that the most important DMN subregions in the human had the least functional homology between species. Specifically, **dorsal medial system components, which were previously identified as having relatively low importance, were found to have high FCHI**, **while medial temporal system components, which were identified as being of high importance, had low FCHI**. Consistent with prior work suggesting divisions within the core subsystem with respect to high versus low importance, we found that vMPFC and DLPFC exhibited a higher FCHI, while temporal parietal junction (TPJ) and PMC had a lower FCHI ( Patel et al., 2019 ). Together this analysis suggests that regions where the FCHI tends to be relatively lower, correspond to locations which in humans tend to be regions that are most important for reflecting global patterns of functional connectivity within the DMN ( Kernbach et al., 2018 ) . However, Figure 4B shows that the FCHI is actually higher in the medial temporal system than it is in the dorsal medial system, in direct contradiction to the text. Figure 4C also shows that medial temporal system regions have lower importance values than dorsal medial system regions. Both of these results shown in Figure 4 are in direct contradiction to the results reported in the text. Perhaps  medial temporal and  dorsal medial were swapped in the text? , 
 Dear Joseph, Thank you very much for pointing it out. Yes, you are correct. The  medial temporal and  dorsal medial were swapped in this sentence. This sentence should be,  Specifically, **medial temporal system** components, which were previously identified as having relatively low importance, were found to have high FCHI, while **dorsal medial system** components, which were identified as being of high importance, had low FCHI. Thank you again. I ll see if I can correct this. Best, Ting ,