Evolutionary changes leading to efficient glymphatic circulation in the mammalian brain

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Abstract

The functional significance of the morphological and genetic changes that occurred in the brain during evolution is not fully understood. Here we show the relationships between evolutionary changes of the brain and glymphatic circulation. We establish a mathematical model to simulate glymphatic circulation in the cerebral hemispheres, and our results show that cortical neurons accumulate in areas of the cerebral hemispheres where glymphatic circulation is highly efficient. We also find that cortical folds markedly enhance the efficiency of glymphatic circulation in the cerebral hemispheres. Furthermore, our in vivo study using ferrets reveals sulcus-dominant cerebrospinal fluid (CSF) influx, which enhances the efficiency of glymphatic circulation in the enlarged cerebral hemispheres of gyrencephalic brains. Sulcus-dominant CSF influx is mediated by preferential expression of aquaporin-4 in sulcal regions, and similar expression patterns of aquaporin-4 are also found in human cerebral hemispheres. These results indicate that evolutionary changes in the cerebral hemispheres are related to improved efficiency of glymphatic circulation. It seems plausible that the efficiency of glymphatic circulation is an important factor determining the evolutionary trajectory of the cerebral hemispheres.

Abstract

The functional consequences of the brain changes during evolution remain unclear. Here, the authors use mathematical modeling and experimental validation to demonstrate a relationship between evolutionary brain changes and glymphatic circulation.

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Most cited references 53

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A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β.

Jeffrey J. Iliff, Minghuan Wang, Yonghong Liao … (2012)

Because it lacks a lymphatic circulation, the brain must clear extracellular proteins by an alternative mechanism. The cerebrospinal fluid (CSF) functions as a sink for brain extracellular solutes, but it is not clear how solutes from the brain interstitium move from the parenchyma to the CSF. We demonstrate that a substantial portion of subarachnoid CSF cycles through the brain interstitial space. On the basis of in vivo two-photon imaging of small fluorescent tracers, we showed that CSF enters the parenchyma along paravascular spaces that surround penetrating arteries and that brain interstitial fluid is cleared along paravenous drainage pathways. Animals lacking the water channel aquaporin-4 (AQP4) in astrocytes exhibit slowed CSF influx through this system and a ~70% reduction in interstitial solute clearance, suggesting that the bulk fluid flow between these anatomical influx and efflux routes is supported by astrocytic water transport. Fluorescent-tagged amyloid β, a peptide thought to be pathogenic in Alzheimer's disease, was transported along this route, and deletion of the Aqp4 gene suppressed the clearance of soluble amyloid β, suggesting that this pathway may remove amyloid β from the central nervous system. Clearance through paravenous flow may also regulate extracellular levels of proteins involved with neurodegenerative conditions, its impairment perhaps contributing to the mis-accumulation of soluble proteins.

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Impairment of glymphatic pathway function promotes tau pathology after traumatic brain injury.

Jeffrey J. Iliff, Michael Chen, Benjamin A. Plog … (2014)

Traumatic brain injury (TBI) is an established risk factor for the early development of dementia, including Alzheimer's disease, and the post-traumatic brain frequently exhibits neurofibrillary tangles comprised of aggregates of the protein tau. We have recently defined a brain-wide network of paravascular channels, termed the "glymphatic" pathway, along which CSF moves into and through the brain parenchyma, facilitating the clearance of interstitial solutes, including amyloid-β, from the brain. Here we demonstrate in mice that extracellular tau is cleared from the brain along these paravascular pathways. After TBI, glymphatic pathway function was reduced by ∼60%, with this impairment persisting for at least 1 month post injury. Genetic knock-out of the gene encoding the astroglial water channel aquaporin-4, which is importantly involved in paravascular interstitial solute clearance, exacerbated glymphatic pathway dysfunction after TBI and promoted the development of neurofibrillary pathology and neurodegeneration in the post-traumatic brain. These findings suggest that chronic impairment of glymphatic pathway function after TBI may be a key factor that renders the post-traumatic brain vulnerable to tau aggregation and the onset of neurodegeneration.

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A developmental and genetic classification for malformations of cortical development: update 2012

A. Barkovich, Renzo Guerrini, Ruben I Kuzniecky … (2012)

Malformations of cerebral cortical development include a wide range of developmental disorders that are common causes of neurodevelopmental delay and epilepsy. In addition, study of these disorders contributes greatly to the understanding of normal brain development and its perturbations. The rapid recent evolution of molecular biology, genetics and imaging has resulted in an explosive increase in our knowledge of cerebral cortex development and in the number and types of malformations of cortical development that have been reported. These advances continue to modify our perception of these malformations. This review addresses recent changes in our perception of these disorders and proposes a modified classification based upon updates in our knowledge of cerebral cortical development.

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Author and article information

Contributors

Satoru Okuda:

ORCID: http://orcid.org/0000-0003-3792-8067

satokuda@staff.kanazawa-u.ac.jp

Hiroshi Kawasaki:

ORCID: http://orcid.org/0000-0002-2514-1497

kawasaki@med.kanazawa-u.ac.jp

Journal

Journal ID (nlm-ta): Nat Commun

Journal ID (iso-abbrev): Nat Commun

Title: Nature Communications

Publisher: Nature Publishing Group UK (London )

ISSN (Electronic): 2041-1723

Publication date (Electronic): 4 December 2024

Publication date PMC-release: 4 December 2024

Publication date Collection: 2024

Volume: 15

Electronic Location Identifier: 10048

Affiliations

[1 ]Department of Medical Neuroscience, Graduate School of Medical Sciences, Kanazawa University, ( https://ror.org/02hwp6a56) Ishikawa, Japan

[2 ]GRID grid.9707.9, ISNI 0000 0001 2308 3329, Nano Life Science Institute, , Kanazawa University, ; Ishikawa, Japan

[3 ]Sapiens Life Sciences, Evolution and Medicine Research Center, Kanazawa University, ( https://ror.org/02hwp6a56) Ishikawa, Japan

[4 ]Department of Neurosurgery, Graduate School of Medical Sciences, Kanazawa University, ( https://ror.org/02hwp6a56) Ishikawa, Japan

Author information

Narufumi Kameya http://orcid.org/0000-0002-9409-4364

Kengo Saito http://orcid.org/0000-0002-4520-3675

Mitsutoshi Nakada http://orcid.org/0000-0001-9419-6101

Satoru Okuda http://orcid.org/0000-0003-3792-8067

Hiroshi Kawasaki http://orcid.org/0000-0002-2514-1497

Article

Publisher ID: 54372

DOI: 10.1038/s41467-024-54372-1

PMC ID: 11618516

PubMed ID: 39632840

SO-VID: 989c38ae-1da7-4e9c-9892-bbc409cb6d08

License:

Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.

History

Date received : 9 December 2023

Date accepted : 5 November 2024

Funding

Funded by: FundRef https://doi.org/10.13039/100009619, Japan Agency for Medical Research and Development (AMED);

Award ID: JP24wm0625112

Award Recipient : Hiroshi Kawasaki

Funded by: FundRef https://doi.org/10.13039/501100001691, MEXT | Japan Society for the Promotion of Science (JSPS);

Funded by: FundRef https://doi.org/10.13039/100007449, Takeda Science Foundation;

Funded by: FundRef https://doi.org/10.13039/100008732, Uehara Memorial Foundation;

Funded by: FundRef https://doi.org/10.13039/501100002241, MEXT | Japan Science and Technology Agency (JST);

Funded by: the National Institute of Information and Communications Technology (NICT), Japan, Grant number 23001

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Keywords: neuroscience,evolution

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ScienceOpen disciplines: Uncategorized

Keywords: neuroscience, evolution

Evolutionary changes leading to efficient glymphatic circulation in the mammalian brain

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Crocodylian evolution

Most cited references 53

A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β.

Impairment of glymphatic pathway function promotes tau pathology after traumatic brain injury.

A developmental and genetic classification for malformations of cortical development: update 2012

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