Anatomical basis and physiological role of cerebrospinal fluid transport through the murine cribriform plate

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Abstract

Cerebrospinal fluid (CSF) flows through the brain, transporting chemical signals and removing waste. CSF production in the brain is balanced by a constant outflow of CSF, the anatomical basis of which is poorly understood. Here, we characterized the anatomy and physiological function of the CSF outflow pathway along the olfactory sensory nerves through the cribriform plate, and into the nasal epithelia. Chemical ablation of olfactory sensory nerves greatly reduced outflow of CSF through the cribriform plate. The reduction in CSF outflow did not cause an increase in intracranial pressure (ICP), consistent with an alteration in the pattern of CSF drainage or production. Our results suggest that damage to olfactory sensory neurons (such as from air pollution) could contribute to altered CSF turnover and flow, providing a potential mechanism for neurological diseases.

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Intranasal delivery of biologics to the central nervous system.

Jeffrey J. Lochhead, Robert Thorne (2012)

Treatment of central nervous system (CNS) diseases is very difficult due to the blood-brain barrier's (BBB) ability to severely restrict entry of all but small, non-polar compounds. Intranasal administration is a non-invasive method of drug delivery which may bypass the BBB to allow therapeutic substances direct access to the CNS. Intranasal delivery of large molecular weight biologics such as proteins, gene vectors, and stem cells is a potentially useful strategy to treat a variety of diseases/disorders of the CNS including stroke, Parkinson's disease, multiple sclerosis, Alzheimer's disease, epilepsy, and psychiatric disorders. Here we give an overview of relevant nasal anatomy and physiology and discuss the pathways and mechanisms likely involved in drug transport from the nasal epithelium to the CNS. Finally we review both pre-clinical and clinical studies involving intranasal delivery of biologics to the CNS. Copyright © 2011 Elsevier B.V. All rights reserved.

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SeeDB: a simple and morphology-preserving optical clearing agent for neuronal circuit reconstruction.

Meng-Tsen Ke, Satoshi Fujimoto, Takeshi Imai (2013)

We report a water-based optical clearing agent, SeeDB, which clears fixed brain samples in a few days without quenching many types of fluorescent dyes, including fluorescent proteins and lipophilic neuronal tracers. Our method maintained a constant sample volume during the clearing procedure, an important factor for keeping cellular morphology intact, and facilitated the quantitative reconstruction of neuronal circuits. Combined with two-photon microscopy and an optimized objective lens, we were able to image the mouse brain from the dorsal to the ventral side. We used SeeDB to describe the near-complete wiring diagram of sister mitral cells associated with a common glomerulus in the mouse olfactory bulb. We found the diversity of dendrite wiring patterns among sister mitral cells, and our results provide an anatomical basis for non-redundant odor coding by these neurons. Our simple and efficient method is useful for imaging intact morphological architecture at large scales in both the adult and developing brains.

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Correlations of neuronal and microvascular densities in murine cortex revealed by direct counting and colocalization of nuclei and vessels.

Philbert S. Tsai, John Kaufhold, Pablo Blinder … (2009)

It is well known that the density of neurons varies within the adult brain. In neocortex, this includes variations in neuronal density between different lamina as well as between different regions. Yet the concomitant variation of the microvessels is largely uncharted. Here, we present automated histological, imaging, and analysis tools to simultaneously map the locations of all neuronal and non-neuronal nuclei and the centerlines and diameters of all blood vessels within thick slabs of neocortex from mice. Based on total inventory measurements of different cortical regions ( approximately 10(7) cells vectorized across brains), these methods revealed: (1) In three dimensions, the mean distance of the center of neuronal somata to the closest microvessel was 15 mum. (2) Volume samples within lamina of a given region show that the density of microvessels does not match the strong laminar variation in neuronal density. This holds for both agranular and granular cortex. (3) Volume samples in successive radii from the midline to the ventral-lateral edge, where each volume summed the number of cells and microvessels from the pia to the white matter, show a significant correlation between neuronal and microvessel densities. These data show that while neuronal and vascular densities do not track each other on the 100 mum scale of cortical lamina, they do track each other on the 1-10 mm scale of the cortical mantle. The absence of a disproportionate density of blood vessels in granular lamina is argued to be consistent with the initial locus of functional brain imaging signals.

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Author and article information

Contributors

Jordan N Norwood:

ORCID: http://orcid.org/0000-0001-8093-5938

Patrick J Drew:

ORCID: https://orcid.org/0000-0002-7483-7378

Ronald L Calabrese: Role: Reviewing Editor

Ronald L Calabrese: Role: Senior Editor

Journal

Journal ID (nlm-ta): eLife

Journal ID (iso-abbrev): Elife

Journal ID (publisher-id): eLife

Title: eLife

Publisher: eLife Sciences Publications, Ltd

ISSN (Electronic): 2050-084X

Publication date (Electronic, pub): 07 May 2019

Publication date Collection: 2019

Volume: 8

Electronic Location Identifier: e44278

Affiliations

[1 ]deptCellular and Developmental Biology Graduate Program Pennsylvania State University University ParkUnited States

[2 ]deptDepartment of Engineering Science and Mechanics Pennsylvania State University University ParkUnited States

[3 ]deptDepartment of Physics Pennsylvania State University University ParkUnited States

[4 ]deptDepartment of Biomedical Engineering Pennsylvania State University University ParkUnited States

[5 ]deptDepartment of Anthropology Pennsylvania State University University ParkUnited States

[6 ]deptDepartment of Neurosurgery Pennsylvania State University University ParkUnited States

Emory University United States

University of Southampton United Kingdom

University of Wisconsin-Madison United States

OHSU United States

Author information

Jordan N Norwood http://orcid.org/0000-0001-8093-5938

Qingguang Zhang http://orcid.org/0000-0003-4500-813X

Patrick J Drew https://orcid.org/0000-0002-7483-7378

Article

Publisher ID: 44278

DOI: 10.7554/eLife.44278

PMC ID: 6524970

PubMed ID: 31063132

SO-VID: ec91be1e-2f0d-417d-9e8a-8d3cfbf50cff

License:

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

History

Date received : 10 December 2018

Date accepted : 06 May 2019

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;

Award ID: F31NS105461

Award Recipient : Jordan N Norwood

Funded by: FundRef http://dx.doi.org/10.13039/100008321, Pennsylvania State University;

Award ID: Huck Graduate Enrichment Grant

Award Recipient : Jordan N Norwood

Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;

Award ID: CBET1705854

Award Recipient : Patrick J Drew

Funded by: FundRef http://dx.doi.org/10.13039/100000872, McKnight Endowment Fund for Neuroscience;

Award Recipient : Patrick J Drew

Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;

Award ID: R01NS078168

Award Recipient : Patrick J Drew

Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;

Award ID: P01HD078233

Award Recipient : Patrick J Drew

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Custom metadata

Author impact statement Chemical ablation of olfactory sensory neurons blocks cerebrospinal fluid outflow into the nasal epithelium, leading to alterations of cerebrospinal fluid dynamics.

ScienceOpen disciplines: Life sciences

Keywords: cribriform,olfatory nerve,cerebrospinal fluid,intracranial pressure,anosmia,mouse

Data availability:

ScienceOpen disciplines: Life sciences

Keywords: cribriform, olfatory nerve, cerebrospinal fluid, intracranial pressure, anosmia, mouse

Anatomical basis and physiological role of cerebrospinal fluid transport through the murine cribriform plate

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GLUT4 biology

Most cited references 105

Intranasal delivery of biologics to the central nervous system.

SeeDB: a simple and morphology-preserving optical clearing agent for neuronal circuit reconstruction.

Correlations of neuronal and microvascular densities in murine cortex revealed by direct counting and colocalization of nuclei and vessels.

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