Connectome topology of mammalian brains and its relationship to taxonomy and phylogeny

Network models of anatomical connections allow for the extraction of quantitative features describing brain organization, and their comparison across brains from different species. Such comparisons can inform our understanding of between-species differences in brain architecture and can be compared...

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Main Authors: Joshua Faskowitz, Maria Grazia Puxeddu, Martijn P. van den Heuvel, Bratislav Mišić, Yossi Yovel, Yaniv Assaf, Richard F. Betzel, Olaf Sporns
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-01-01
Series:Frontiers in Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnins.2022.1044372/full
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author Joshua Faskowitz
Maria Grazia Puxeddu
Martijn P. van den Heuvel
Bratislav Mišić
Yossi Yovel
Yaniv Assaf
Richard F. Betzel
Richard F. Betzel
Richard F. Betzel
Richard F. Betzel
Olaf Sporns
Olaf Sporns
Olaf Sporns
Olaf Sporns
author_facet Joshua Faskowitz
Maria Grazia Puxeddu
Martijn P. van den Heuvel
Bratislav Mišić
Yossi Yovel
Yaniv Assaf
Richard F. Betzel
Richard F. Betzel
Richard F. Betzel
Richard F. Betzel
Olaf Sporns
Olaf Sporns
Olaf Sporns
Olaf Sporns
author_sort Joshua Faskowitz
collection DOAJ
description Network models of anatomical connections allow for the extraction of quantitative features describing brain organization, and their comparison across brains from different species. Such comparisons can inform our understanding of between-species differences in brain architecture and can be compared to existing taxonomies and phylogenies. Here we performed a quantitative comparative analysis using the MaMI database (Tel Aviv University), a collection of brain networks reconstructed from ex vivo diffusion MRI spanning 125 species and 12 taxonomic orders or superorders. We used a broad range of metrics to measure between-mammal distances and compare these estimates to the separation of species as derived from taxonomy and phylogeny. We found that within-taxonomy order network distances are significantly closer than between-taxonomy network distances, and this relation holds for several measures of network distance. Furthermore, to estimate the evolutionary divergence between species, we obtained phylogenetic distances across 10,000 plausible phylogenetic trees. The anatomical network distances were rank-correlated with phylogenetic distances 10,000 times, creating a distribution of coefficients that demonstrate significantly positive correlations between network and phylogenetic distances. Collectively, these analyses demonstrate species-level organization across scales and informational sources: we relate brain networks distances, derived from MRI, with evolutionary distances, derived from genotyping data.
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spelling doaj.art-e4a4901c43d94364b4d627d363303a852023-01-11T05:36:09ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2023-01-011610.3389/fnins.2022.10443721044372Connectome topology of mammalian brains and its relationship to taxonomy and phylogenyJoshua Faskowitz0Maria Grazia Puxeddu1Martijn P. van den Heuvel2Bratislav Mišić3Yossi Yovel4Yaniv Assaf5Richard F. Betzel6Richard F. Betzel7Richard F. Betzel8Richard F. Betzel9Olaf Sporns10Olaf Sporns11Olaf Sporns12Olaf Sporns13Department of Psychological and Brain Sciences, Indiana University Bloomington, Bloomington, IN, United StatesDepartment of Psychological and Brain Sciences, Indiana University Bloomington, Bloomington, IN, United StatesDepartment of Complex Trait Genetics, Center for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, Amsterdam, NetherlandsMontreal Neurological Institute, McGill University, Montreal, QC, CanadaSchool of Neurobiology, Biochemistry and Biophysics, Tel Aviv University, Tel Aviv-Yafo, IsraelSchool of Neurobiology, Biochemistry and Biophysics, Tel Aviv University, Tel Aviv-Yafo, IsraelDepartment of Psychological and Brain Sciences, Indiana University Bloomington, Bloomington, IN, United StatesProgram in Neuroscience, Indiana University Bloomington, Bloomington, IN, United StatesProgram in Cognitive Science, Indiana University Bloomington, Bloomington, IN, United StatesIndiana University Network Science Institute, Indiana University Bloomington, Bloomington, IN, United StatesDepartment of Psychological and Brain Sciences, Indiana University Bloomington, Bloomington, IN, United StatesProgram in Neuroscience, Indiana University Bloomington, Bloomington, IN, United StatesProgram in Cognitive Science, Indiana University Bloomington, Bloomington, IN, United StatesIndiana University Network Science Institute, Indiana University Bloomington, Bloomington, IN, United StatesNetwork models of anatomical connections allow for the extraction of quantitative features describing brain organization, and their comparison across brains from different species. Such comparisons can inform our understanding of between-species differences in brain architecture and can be compared to existing taxonomies and phylogenies. Here we performed a quantitative comparative analysis using the MaMI database (Tel Aviv University), a collection of brain networks reconstructed from ex vivo diffusion MRI spanning 125 species and 12 taxonomic orders or superorders. We used a broad range of metrics to measure between-mammal distances and compare these estimates to the separation of species as derived from taxonomy and phylogeny. We found that within-taxonomy order network distances are significantly closer than between-taxonomy network distances, and this relation holds for several measures of network distance. Furthermore, to estimate the evolutionary divergence between species, we obtained phylogenetic distances across 10,000 plausible phylogenetic trees. The anatomical network distances were rank-correlated with phylogenetic distances 10,000 times, creating a distribution of coefficients that demonstrate significantly positive correlations between network and phylogenetic distances. Collectively, these analyses demonstrate species-level organization across scales and informational sources: we relate brain networks distances, derived from MRI, with evolutionary distances, derived from genotyping data.https://www.frontiersin.org/articles/10.3389/fnins.2022.1044372/fullnetwork neuroscienceconnectomicsmammalsphylogenycomparative neuroanatomyconnectome analysis
spellingShingle Joshua Faskowitz
Maria Grazia Puxeddu
Martijn P. van den Heuvel
Bratislav Mišić
Yossi Yovel
Yaniv Assaf
Richard F. Betzel
Richard F. Betzel
Richard F. Betzel
Richard F. Betzel
Olaf Sporns
Olaf Sporns
Olaf Sporns
Olaf Sporns
Connectome topology of mammalian brains and its relationship to taxonomy and phylogeny
Frontiers in Neuroscience
network neuroscience
connectomics
mammals
phylogeny
comparative neuroanatomy
connectome analysis
title Connectome topology of mammalian brains and its relationship to taxonomy and phylogeny
title_full Connectome topology of mammalian brains and its relationship to taxonomy and phylogeny
title_fullStr Connectome topology of mammalian brains and its relationship to taxonomy and phylogeny
title_full_unstemmed Connectome topology of mammalian brains and its relationship to taxonomy and phylogeny
title_short Connectome topology of mammalian brains and its relationship to taxonomy and phylogeny
title_sort connectome topology of mammalian brains and its relationship to taxonomy and phylogeny
topic network neuroscience
connectomics
mammals
phylogeny
comparative neuroanatomy
connectome analysis
url https://www.frontiersin.org/articles/10.3389/fnins.2022.1044372/full
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