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Developmental mechanics of the primate cerebral cortex

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Abstract

The idea that the brain is shaped through the interplay of predetermined ontogenetic factors and mechanisms of self-organization has a long tradition in biology, going back to the late-nineteenth century. Here we illustrate the substantial impact of mechanical forces on the development, morphology, and functioning of the primate cerebral cortex. Based on the analysis of quantitative structural data for prefrontal cortices of the adult rhesus monkey, we demonstrate that (1) the characteristic shape of cortical convolutions can be explained by the global minimization of axonal tension in corticocortical projections; (2) mechanical forces resulting from cortical folding have a significant impact on the relative and absolute thickness of cortical layers in gyri and sulci; (3) folding forces may affect the cellular migration during cortical development, resulting in a significantly larger number of neurons in gyral compared to non-gyral regions; and (4) mechanically induced variations of morphology at the cellular level may result in different modes of neuronal functioning in gyri and sulci. These results underscore the significant contribution of mechanical forces during the self-organization of the primate cerebral cortex. Taking such factors into account within a framework of developmental mechanics can lead to a better understanding of how genetic specification, the layout of connections, brain shape as well as brain function are linked in normal and pathologically transformed brains.

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Acknowledgements

We thank Ms. Louise Hurst for carrying out the NEURON simulations depicted in Fig. 4, Mr. Oleg Gusyatin for reconstructing the rhesus monkey brain and globally calculating the thickness of gyral and sulcal cortex, as well as Dr. Basilis Zikopoulos for help with Fig. 3. The research was supported in part by NIH grants from NIMH and NINDS.

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Correspondence to Claus C. Hilgetag.

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Experiments involving animals were conducted according to the NIH guide for the Care and Use of Laboratory animals (NIH pub. 86–23, revised 1996), and experimental protocols were approved by the IACUC at Boston University School of Medicine., Harvard Medical School., and New England Primate Research Center

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Hilgetag, C.C., Barbas, H. Developmental mechanics of the primate cerebral cortex. Anat Embryol 210, 411–417 (2005). https://doi.org/10.1007/s00429-005-0041-5

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