Gold nanoparticle-enhanced X-ray microtomography of the rodent reveals region-specific cerebrospinal fluid circulation in the brain

Shelei Pan, Peter H. Yang, Dakota DeFreitas, Sruthi Ramagiri, Peter O. Bayguinov, Carl D. Hacker, Abraham Z. Snyder, Jackson Wilborn, Hengbo Huang, Gretchen M. Koller, Dhvanii K. Raval, Grace L. Halupnik, Sanja Sviben, Samuel Achilefu, Rui Tang, Gabriel Haller, James D. Quirk, James A. J. Fitzpatrick, Prabagaran Esakky and Jennifer M. Strahle ()
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Shelei Pan: Washington University in St. Louis
Peter H. Yang: Washington University in St. Louis
Dakota DeFreitas: Washington University in St. Louis
Sruthi Ramagiri: Washington University in St. Louis
Peter O. Bayguinov: Washington University in St. Louis
Carl D. Hacker: Washington University in St. Louis
Abraham Z. Snyder: Washington University in St. Louis
Jackson Wilborn: Washington University in St. Louis
Hengbo Huang: Washington University in St. Louis
Gretchen M. Koller: Washington University in St. Louis
Dhvanii K. Raval: Washington University in St. Louis
Grace L. Halupnik: Washington University in St. Louis
Sanja Sviben: Washington University in St. Louis
Samuel Achilefu: UT Southwestern Medical Center
Rui Tang: Washington University in St. Louis
Gabriel Haller: Washington University in St. Louis
James D. Quirk: Washington University in St. Louis
James A. J. Fitzpatrick: Washington University in St. Louis
Prabagaran Esakky: Washington University in St. Louis
Jennifer M. Strahle: Washington University in St. Louis

Nature Communications, 2023, vol. 14, issue 1, 1-16

Abstract: Abstract Cerebrospinal fluid (CSF) is essential for the development and function of the central nervous system (CNS). However, the brain and its interstitium have largely been thought of as a single entity through which CSF circulates, and it is not known whether specific cell populations within the CNS preferentially interact with the CSF. Here, we develop a technique for CSF tracking, gold nanoparticle-enhanced X-ray microtomography, to achieve micrometer-scale resolution visualization of CSF circulation patterns during development. Using this method and subsequent histological analysis in rodents, we identify previously uncharacterized CSF pathways from the subarachnoid space (particularly the basal cisterns) that mediate CSF-parenchymal interactions involving 24 functional-anatomic cell groupings in the brain and spinal cord. CSF distribution to these areas is largely restricted to early development and is altered in posthemorrhagic hydrocephalus. Our study also presents particle size-dependent CSF circulation patterns through the CNS including interaction between neurons and small CSF tracers, but not large CSF tracers. These findings have implications for understanding the biological basis of normal brain development and the pathogenesis of a broad range of disease states, including hydrocephalus.

Date: 2023
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DOI: 10.1038/s41467-023-36083-1

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