Over 100 years ago, Ramon y Cajal hypothesized that two forces played a role in the evolution of mammalian brain connectivity: minimizing wiring costs and maximizing conductivity speed. Using diffusion MRI, we reconstructed the brain connectomes of 123 mammalian species. Network analysis revealed that both connectivity and the wiring cost are conserved across mammals. We describe a conservation principle that maintains the overall connectivity: species with fewer interhemispheric connections exhibit better intrahemispheric connectivity.
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The data that support the findings of this study are available from the corresponding author upon request.
All codes used in this study are part of Matlab’s (Mathworks) statistics and data analysis toolbox codes. The circular graphs were generated using P. Kassebaum’s (2020) circularGraph (https://www.github.com/paul-kassebaum-mathworks/circularGraph).
Krubitzer, L. A. & Seelke, A. M. Cortical evolution in mammals: the bane and beauty of phenotypic variability. Proc. Natl Acad. Sci. USA 109(Suppl 1), 10647–10654 (2012).
Herculano-Houzel, S. The human brain in numbers: a linearly scaled-up primate brain. Front Hum. Neurosci. 3, 31 (2009).
Thiebaut de Schotten, M., Croxson, P.L. & Mars, R.B. Large-scale comparative neuroimaging: where are we and what do we need? Cortex 118, 188–202 (2018).
Chklovskii, D. B. Synaptic connectivity and neuronal morphology: two sides of the same coin. Neuron 43, 609–617 (2004).
Wedeen, V. J. et al. The geometric structure of the brain fiber pathways. Science 335, 1628–1634 (2012).
Cherniak, C., Mokhtarzada, Z., Rodriguez-Esteban, R. & Changizi, K. Global optimization of cerebral cortex layout. Proc. Natl Acad. Sci. USA 101, 1081–1086 (2004).
Hagmann, P. et al. Mapping the structural core of human cerebral cortex. PLoS Biol. 6, e159 (2008).
Zhang, K. & Sejnowski, T. J. A universal scaling law between gray matter and white matter of cerebral cortex. Proc. Natl Acad. Sci. USA 97, 5621–5626 (2000).
Manger, P. R., Hemingway, J., Haagensen, M. & Gilissen, E. Cross-sectional area of the elephant corpus callosum: comparison to other eutherian mammals. Neuroscience 167, 815–824 (2010).
Sporns, O. From simple graphs to the connectome: networks in neuroimaging. Neuroimage 62, 881–886 (2012).
Bullmore, E. & Sporns, O. The economy of brain network organization. Nat. Rev. Neurosci. 13, 336–349 (2012).
Bassett, D. S. & Sporns, O. Network neuroscience. Nat. Neurosci. 20, 353–364 (2017).
Klyachko, V. A. & Stevens, C. F. Connectivity optimization and the positioning of cortical areas. Proc. Natl Acad. Sci. USA 100, 7937–7941 (2003).
Cuntz, H., Forstner, F., Borst, A. & Hausser, M. One rule to grow them all: a general theory of neuronal branching and its practical application. PLoS Comput. Biol. 6, e1000877 (2010).
Newman, M. E. J. Networks: An Introduction (Oxford Univ. Press, 2010).
Suarez, R. et al. A pan-mammalian map of interhemispheric brain connections predates the evolution of the corpus callosum. Proc. Natl Acad. Sci. USA 115, 9622–9627 (2018).
Thomas, C. et al. Anatomical accuracy of brain connections derived from diffusion MRI tractography is inherently limited. Proc. Natl Acad. Sci. USA 111, 16574–16579 (2014).
Maier-Hein, K. H. et al. The challenge of mapping the human connectome based on diffusion tractography. Nat. Commun. 8, 1349 (2017).
Owen, J. P. et al. The structural connectome of the human brain in agenesis of the corpus callosum. Neuroimage 70, 340–355 (2013).
Kliemann, D. et al. Intrinsic functional connectivity of the brain in adults with a single cerebral hemisphere. Cell Rep. 29(2398-2407), e2394 (2019).
van den Heuvel, M. P. & Sporns, O. Rich-club organization of the human connectome. J. Neurosci. 31, 1577586 (2011).
Oh, S. W. et al. A mesoscale connectome of the mouse brain. Nature 508, 207–214 (2014).
Leemans, A., Jeurissen, B., Sijbers, J. & Jones, D. K. ExploreDTI: a graphical toolbox for processing, analyzing, and visualizing diffusion MR data. Proc. Int. Soc. Magn. Reson. Med. 17, 3537 (2009).
Tournier, J. D., Calamante, F., Gadian, D. G. & Connelly, A. Direct estimation of the fiber orientation density function from diffusion-weighted MRI data using spherical deconvolution. Neuroimage 23, 1176–1185 (2004).
Smith, R. E., Tournier, J. D., Calamante, F. & Connelly, A. Anatomically-constrained tractography: improved diffusion MRI streamlines tractography through effective use of anatomical information. Neuroimage 62, 1924–1938 (2012).
Sotiropoulos, S. N. & Zalesky, A. Building connectomes using diffusion MRI: why, how and but. NMR Biomed. 32, e3752 (2019).
We thank K. Or, R. Elazari, S. Landau, A. Scheinin, D. Morik, N. Avni-Magen, N. Kornfeld-Schor, I. Horowitz and A. Kafri for help with brain collection. We also thank A. Leemans for help with the fiber-tracking procedures. Y.A. thanks the Strauss Center for Computational Neuroimaging for help in data acqusition.
The authors declare no competing interests.
Peer review information Nature Neuroscience thanks Daniel Alexander, Rogier Mars and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Assaf, Y., Bouznach, A., Zomet, O. et al. Conservation of brain connectivity and wiring across the mammalian class. Nat Neurosci 23, 805–808 (2020). https://doi.org/10.1038/s41593-020-0641-7
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