Junctions in the meninges and marginal glia.
Abstract
The meninges of various mammals were prepared for examination with the electronmicroscope by thin sectioning or freeze-fracturing. Particular attention was given to the distribution of tight junctions in order to determine the basis for the meningeal barrier between the blood circulating in dural vessels and the cerebrospinal fluid in the subarachnoid space. While some dural blood vessels are fenestrated, those in the subarachnoid space are not and their component endothelial cells are joined by an extensive system of tight junctions. An extensive and continuous system of tight junctions was also found in a layer of specialized cells at the border of the arachnoid with the dura. This arachnoid barrier layer is apparently the only basis of the meningeal barrier because often cellular layers in the dura and arachnoid lack tight junctions although they are linked by gap junctions and desmosomes. In particular, tight junctions are lacking at the border of the "subdural space" which is actually a fascial plane within the dura. Tight junctions are also lacking between astrocytes at the surface of the brain but these cells are linked by gap junctions and a new type of intercellular junction. The distribution of these junctions, as well as assemblies of intramembranous particles at the astrocytic border, raises the question whether this layer might have a role in the exchange of certain substances between the brain and cerebrospinal fluid.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The pial vasculature has barrier properties and is part of the meninges blood-CSF barrier.
“Several studies show this vasculature has barrier properties and are therefore part of the meninges blood-CSF barrier.”
From Living on the Edge of the CNS: Meninges Cell Diversity in Health and Disease (2021) · cites this paper as Nabeshima et al., 1975
Arachnoid barrier cells are epithelial-like cells connected by tight and adherens junctions that regulate the movement of pathogens, molecules, and cells into and out of the CSF and brain parenchyma.
“Segregating the outer and inner meningeal compartments is the epithelial-like arachnoid barrier cells, connected by tight and adherens junctions, which regulate the movement of pathogens, molecules, and cells into and out of the cerebral spinal fluid (CSF) and brain parenchyma.”
From Living on the Edge of the CNS: Meninges Cell Diversity in Health and Disease (2021) · cites this paper as Nabeshima et al., 1975
Previous observations indicate that the arachnoid constitutes an impermeable barrier layer between CSF and dura mater.
“previous observations indicating that the arachnoid constitutes an impermeable barrier layer between the CSF and dura mater8,9”
From Cerebrospinal fluid tracer efflux to parasagittal dura in humans (2020) · cites this paper as [8]
Cites
JUNCTIONAL COMPLEXES IN VARIOUS EPITHELIA
Farquhar, M. G., & Palade, G. E. (1963) · The Journal of Cell Biology · doi:10.1083/jcb.17.2.375 · Cited by 3,637 · see citing works
FINE STRUCTURAL LOCALIZATION OF A BLOOD-BRAIN BARRIER TO EXOGENOUS PEROXIDASE
Reese, T. S., & Karnovsky, M. J. (1967) · The Journal of Cell Biology · doi:10.1083/jcb.34.1.207 · Cited by 2,629 · see citing works
JUNCTIONS BETWEEN INTIMATELY APPOSED CELL MEMBRANES IN THE VERTEBRATE BRAIN
Brightman, M., & Reese, T. S. (1969) · The Journal of Cell Biology · doi:10.1083/jcb.40.3.648 · Cited by 2,457 · see citing works
Bloom, W., & Fawcett, D. W. (1962) · Cited by 2,210 · see citing works
FRACTURE FACES OF ZONULAE OCCLUDENTES FROM "TIGHT" AND "LEAKY" EPITHELIA
Claude, P., & Goodenough, D. A. (1973) · The Journal of Cell Biology · doi:10.1083/jcb.58.2.390 · Cited by 1,094 · see citing works
Further observations on the fine structure of freeze-cleaved tight junctions
Staehelin, L. A. (1973) · Journal of Cell Science · doi:10.1242/jcs.13.3.763 · Cited by 512 · see citing works
McEwen, L. M. (1956) · The Journal of Physiology · doi:10.1113/jphysiol.1956.sp005493 · Cited by 395 · see citing works
ARRAYS OF PARTICLES IN FREEZE-FRACTURED ASTROCYTIC MEMBRANES
Landis, D. M. D., & Reese, T. S. (1974) · The Journal of Cell Biology · doi:10.1083/jcb.60.1.316 · Cited by 257 · see citing works
(1962) · PubMed · Cited by 173 · see citing works
ULTRASTRUCTURAL STUDIES ON THE PERMEABILITY OF THE MESOTHELIUM TO HORSERADISH PEROXIDASE
Cotran, R. S., & Karnovsky, M. J. (1968) · The Journal of Cell Biology · doi:10.1083/jcb.37.1.123 · Cited by 161 · see citing works
THE MEMBRANOUS COVERINGS OF NEURAL TISSUES: AN ELECTORN MICROSCOPY STUDY
WAGGENER, J. D., & BEGGS, J. (1967) · Journal of Neuropathology and Experimental Neurology · doi:10.1097/00005072-196707000-00005 · Cited by 154 · cited 4× · see citing works
“This layer has been recognized in the arachnoid near nerve roots (Shanthaveerappa and Bourne, ’63; Waggener and Beggs, ’67) but the present study shows that it can now be recognized consistently in both spinal and cerebral meninges in a variety of mammalian species.”
BackgroundInfluentialElectron microscopy of rat cranial meninges
Pease, D. C., & Schultz, R. L. (1958) · American Journal of Anatomy · doi:10.1002/aja.1001020207 · Cited by 142 · see citing works
The intercellular junctional complexes of retinal pigment epithelia.
Hudspeth, A. J., & Yee, A. G. (1973) · PubMed · Cited by 119 · see citing works
FINE STRUCTURE OF THE SURFACE OF THE CEREBRAL CORTEX OF HUMAN BRAIN
Ramsey, H. J. (1965) · The Journal of Cell Biology · doi:10.1083/jcb.26.2.323 · Cited by 117 · see citing works
[On the fine structure of the arachnoidea and dura mater of mammals].
Andres, K. H. (1967) · PubMed · Cited by 115 · see citing works
�ber die Feinstruktur der Arachnoidea und Dura mater von Mammalia
Andres, K. H. (1967) · Cell and Tissue Research · doi:10.1007/bf00369291 · Cited by 111 · see citing works
Meninges and Cerebrospinal Fluid.
Weed, L. H. (1938) · PubMed · Cited by 88 · see citing works
Ultrastructure of Meningeal Sheaths
Anderson, D. R. (1969) · Archives of Ophthalmology · doi:10.1001/archopht.1969.00990020653015 · Cited by 88 · see citing works
The fine structure of the pia mater of the rat
Morse, D. E., & Low, F. N. (1972) · American Journal of Anatomy · doi:10.1002/aja.1001330309 · Cited by 86 · see citing works
Scanning electron microscopy of the subarachnoid space in the dog. I. Spinal cord levels
Cloyd, M. W., & Low, F. N. (1974) · The Journal of Comparative Neurology · doi:10.1002/cne.901530402 · Cited by 77 · see citing works
THE SUBARACHNOID SPACE FOLLOWING THE INTRODUCTION OF A FOREIGN PROTEIN
Shabo, A. L., & Maxwell, D. S. (1971) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-197107000-00013 · Cited by 72 · see citing works
The fine structure of a lateral recess of the subarachnoid space in the rat
Himango, W. A., & Low, F. N. (1971) · The Anatomical Record · doi:10.1002/ar.1091710102 · Cited by 68 · see citing works
Nuclear Magnetic Resonance Studies of Sodium and Potassium in Etiolated Pea Stem
Magnuson, J. A., Magnuson, N. S., Hendrix, D. L., & Higinbotham, N. (1973) · Biophysical Journal · doi:10.1016/s0006-3495(73)86022-9 · Cited by 49 · see citing works
The role of the meningeal tissues in the hemato‐encephalic barrier
Rodriguez‐Peralta, L. A. (1957) · The Journal of Comparative Neurology · doi:10.1002/cne.901070308 · Cited by 40 · see citing works
Electrical impedance of brain surfaces
Bennett, M. V. L. (1969) · Brain Research · doi:10.1016/0006-8993(69)90191-7 · Cited by 28 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Tight junctions of the blood-brain barrier: development, composition and regulation.
Wolburg, H., & Lippoldt, A. (2002) · PubMed · doi:10.1016/s1537-1891(02)00200-8 · Cited by 1,184 · see citing works
Van Hove, H., Martens, L., Scheyltjens, I., De Vlaminck, K., Pombo Antunes, A. R., De Prijck, S., Vandamme, N., De Schepper, S., Van Isterdael, G., Scott, C. L., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0393-4 · Cited by 1,160 · see citing works
Nau, R., Sörgel, F., & Eiffert, H. (2010) · Clinical Microbiology Reviews · doi:10.1128/cmr.00007-10 · Cited by 1,031 · see citing works
Electrical resistance across the blood-brain barrier in anaesthetized rats: a developmental study.
Butt, A. M., Jones, H. C., & Abbott, N. J. (1990) · The Journal of Physiology · doi:10.1113/jphysiol.1990.sp018243 · Cited by 775 · see citing works
Ma, Q., Ineichen, B. V., Detmar, M., & Proulx, S. T. (2017) · Nature Communications · doi:10.1038/s41467-017-01484-6 · Cited by 690 · see citing works
Mechanisms of fluid movement into, through and out of the brain: evaluation of the evidence
Hladky, S. B., & Barrand, M. A. (2014) · Fluids and Barriers of the CNS · doi:10.1186/2045-8118-11-26 · Cited by 633 · see citing works
Stewart, P. A., & Wiley, M. J. (1981) · Developmental Biology · doi:10.1016/0012-1606(81)90382-1 · Cited by 684 · see citing works
Tight Junctions of the Blood–Brain Barrier
Kniesel, U., & Wolburg, H. (2000) · Cellular and Molecular Neurobiology · doi:10.1023/a:1006995910836 · Cited by 525 · see citing works
Ericsson, A., Liu, C., Hart, R. P., & Sawchenko, P. E. (1995) · Journal of Comparative Neurology · doi:10.1002/cne.903610410 · Cited by 471 · see citing works
Haines, D. E., Harkey, H. L., & Al‐Mefty, O. (1993) · Neurosurgery · doi:10.1227/00006123-199301000-00017 · Cited by 444 · see citing works
Drug delivery to the central nervous system: a review.
Misra, A. R., Ganesh, S. D., Shahiwala, A., & Shah, S. P. (2003) · PubMed · Cited by 434 · see citing works
Macrophages at CNS interfaces: Ontogeny and function in health and disease
Kierdorf, K., Masuda, T., Jordão, M. J. C., & Prinz, M. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-019-0201-x · Cited by 416 · see citing works
Proulx, S. T. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-020-03706-5 · Cited by 400 · see citing works
Balin, B. J., Broadwell, R. D., Salcman, M., & El‐Kalliny, M. (1986) · Journal of Comparative Neurology · doi:10.1002/cne.902510209 · Cited by 358 · see citing works
Recent research into the nature of cerebrospinal fluid formation and absorption
McComb, J. G. (1983) · Journal of neurosurgery · doi:10.3171/jns.1983.59.3.0369 · Cited by 337 · see citing works
Meningioma: A Review of Epidemiology, Pathology, Diagnosis, Treatment, and Future Directions
Ogasawara, C. T., Philbrick, B. D., & Adamson, D. C. (2021) · Biomedicines · doi:10.3390/biomedicines9030319 · Cited by 325 · see citing works
Syndrome of Orthostatic Headaches and Diffuse Pachymeningeal Gadolinium Enhancement
Mokri, B., Piepgras, D. G., & Miller, G. M. (1997) · Mayo Clinic Proceedings · doi:10.4065/72.5.400 · Cited by 312 · see citing works
Morphology of blood-brain interfaces
Brightman, M. (1977) · Experimental Eye Research · doi:10.1016/s0014-4835(77)80008-0 · Cited by 302 · see citing works
Cerebrospinal fluid tracer efflux to parasagittal dura in humans
Ringstad, G., & Eide, P. K. (2020) · Nature Communications · doi:10.1038/s41467-019-14195-x · Cited by 292 · see citing works
Blood-brain barrier permeability and physical exercise
Małkiewicz, M. A., Szarmach, A., Sabisz, A., Cubała, W. J., Szurowska, E., & Winklewski, P. J. (2019) · Journal of Neuroinflammation · doi:10.1186/s12974-019-1403-x · Cited by 276 · see citing works
Identification of direct connections between the dura and the brain
Smyth, L. C. D., Xu, D., Okar, S. V., Dykstra, T., Rustenhoven, J., Papadopoulos, Z., Bhasiin, K., Kim, M. W., Drieu, A., Mamuladze, T., et al. (2024) · Nature · doi:10.1038/s41586-023-06993-7 · Cited by 264 · see citing works
DeSisto, J., O’Rourke, R., Jones, H. E., Pawlikowski, B., Malek, A. D., Bonney, S., Guimiot, F., Jones, K. L., & Siegenthaler, J. A. (2020) · Developmental Cell · doi:10.1016/j.devcel.2020.06.009 · Cited by 241 · see citing works
Pizzo, M. E., Wolak, D. J., Kumar, N. N., Brunette, E., Brunnquell, C. L., Hannocks, M., Abbott, N. J., Meyerand, M. E., Sorokin, L., Stanimirovic, D. B., et al. (2018) · The Journal of Physiology · doi:10.1113/jp275105 · Cited by 272 · see citing works
The Cranial Arachnoid and Pia Mater in Man: Anatomical and Ultrastructural Observations
Alcolado, R., Weller, R. O., Parrish, E. P., & Garrod, D. R. (1988) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.1988.tb00862.x · Cited by 251 · see citing works
Recent insights into a new hydrodynamics of the cerebrospinal fluid
Bulat, M., & Klarica, M. (2010) · Brain Research Reviews · doi:10.1016/j.brainresrev.2010.08.002 · Cited by 255 · see citing works
Anatomy and development of the meninges: implications for subdural collections and CSF circulation
Mack, J., Squier, W., & Eastman, J. T. (2009) · Pediatric Radiology · doi:10.1007/s00247-008-1084-6 · Cited by 233 · see citing works
Weller, R. O., Sharp, M. M., Christodoulides, M., Carare, R. O., & Møllgård, K. (2018) · Acta Neuropathologica · doi:10.1007/s00401-018-1809-z · Cited by 222 · see citing works
“In the adult, an arachnoid blood–CSF barrier separates the fenestrated blood vessels in the dura from the CSF in the SAS by means of a cell layer joined by tight junctions (the arachnoid barrier layer) [65].”
BackgroundYamamoto, T., Ochalski, A., Hertzberg, E. L., & Nagy, J. I. (1990) · Journal of Comparative Neurology · doi:10.1002/cne.903020414 · Cited by 230 · see citing works
The origin of subdural neomembranes. I. Fine structure of the dura-arachnoid interface in man.
Schachenmayr, W., & Friede, R. L. (1978) · PubMed Central · Cited by 230 · see citing works
Nanoparticle transport across the blood brain barrier
Grabrucker, A. M., Ruozi, B., Belletti, D., Pederzoli, F., Forni, F., Vandelli, M. A., & Tosi, G. (2016) · Tissue Barriers · doi:10.1080/21688370.2016.1153568 · Cited by 217 · see citing works
Nagy, J. I., Li, X., Rempel, J., Stelmack, G. L., Patel, D., Staines, W. A., Yasumura, T., & Rash, J. E. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1414 · Cited by 212 · see citing works
Williams, R. W., Bastiani, M. J., Lia, B., & Chalupa, L. M. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902460104 · Cited by 206 · see citing works
Molecular characterization of perivascular drainage pathways in the murine brain
Hannocks, M.-J., Pizzo, M. E., Huppert, J., Deshpande, T., Abbott, N. J., Thorne, R. G., & Sorokin, L. (2018) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x17749689 · Cited by 201 · see citing works
Distribution of extracellular tracers in perivascular spaces of the rat brain
Ichimura, T., Fraser, P. A., & Cserr, H. F. (1991) · Brain Research · doi:10.1016/0006-8993(91)91275-6 · Cited by 215 · see citing works
On the question of a subdural space
Haines, D. E. (1991) · The Anatomical Record · doi:10.1002/ar.1092300103 · Cited by 200 · see citing works
Morii, S., Ngai, A. C., & Winn, H. R. (1986) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1986.5 · Cited by 195 · see citing works
Emerging roles for CNS fibroblasts in health, injury and disease
Dorrier, C., Jones, H. E., Pintarić, L., Siegenthaler, J. A., & Daneman, R. (2021) · Nature reviews. Neuroscience · doi:10.1038/s41583-021-00525-w · Cited by 194 · see citing works
CNS Drug Delivery Systems: Novel Approaches
Pathan, S., Iqbal, Z., Zaidi, S., Talegaonkar, S., Vohra, D., Jain, G., Azeem, A., Jain, N., Lalani, J., Khar, R., et al. (2009) · Recent Patents on Drug Delivery & Formulation · doi:10.2174/187221109787158355 · Cited by 193 · see citing works
The cranial dura mater: a review of its history, embryology, and anatomy
Adeeb, N., Mortazavi, M. M., Tubbs, R. S., & Cohen‐Gadol, A. (2012) · Child s Nervous System · doi:10.1007/s00381-012-1744-6 · Cited by 193 · see citing works
Permeability of blood-brain barrier to various sized molecules
Mayhan, W. G., & Heistad, D. D. (1985) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1985.248.5.h712 · Cited by 189 · see citing works
Microscopic morphology and histology of the human meninges
Weller, R. O. (2005) · Morphologie · doi:10.1016/s1286-0115(05)83235-7 · Cited by 176 · see citing works
The Choroid Plexuses and the Barriers Between the Blood and the Cerebrospinal Fluid
Segal, M. B. (2000) · Cellular and Molecular Neurobiology · doi:10.1023/a:1007045605751 · Cited by 174 · see citing works
THE DEVELOPMENT OF THE HUMAN BLOOD‐BRAIN AND BLOOD‐CSF BARRIERS
Møllgård, K., & Saunders, N. R. (1986) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.1986.tb00146.x · Cited by 171 · see citing works
Ultrastructure of the human spinal arachnoid mater and dura mater.
Vandenabeele, F., Creemers, J., & Lambrichts, I. (1996) · PubMed · Cited by 167 · see citing works
How Does the Immune System Enter the Brain?
Mapunda, J. A., Tibar, H., Regragui, W., & Engelhardt, B. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.805657 · Cited by 164 · see citing works
Proescholdt, M. G., Hutto, B., Brady, L. S., & Herkenham, M. A. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00417-0 · Cited by 165 · see citing works
Transport processes in the formation of the cerebrospinal fluid
Wright, E. M. (1978) · Reviews of physiology, biochemistry and pharmacology · doi:10.1007/3-540-08907-1_1 · Cited by 163 · see citing works
Ependym und Circumventriculäre Organe
Leonhardt, V. H. (1980) · Handbuch der mikroskopischen Anatomie des Menschen · doi:10.1007/978-3-642-81358-0_3 · Cited by 162 · see citing works
BARRIER MECHANISMS IN THE BRAIN, I. ADULT BRAIN
Saunders, N. R., Habgood, M., & Dzięgielewska, K. M. (1999) · Clinical and Experimental Pharmacology and Physiology · doi:10.1046/j.1440-1681.1999.02986.x · Cited by 161 · see citing works
van Deurs, B. (1980) · International review of cytology · doi:10.1016/s0074-7696(08)61960-9 · Cited by 159 · see citing works
Molecular anatomy of adult mouse leptomeninges
Pietilä, R., Del Gaudio, F., He, L., Vázquez-Liébanas, E., Vanlandewijck, M., Muhl, L., Mocci, G., Bjørnholm, K. D., Lindblad, C., Fletcher-Sandersjöö, A., et al. (2023) · Neuron · doi:10.1016/j.neuron.2023.09.002 · Cited by 145 · see citing works
Membrane organization and function of M1 and M23 isoforms of aquaporin-4 in epithelial cells
Silberstein, C., Bouley, R., Huang, Y. L., Fang, P.-K., Pastor‐Soler, N. M., Brown, D., & Hoek, A. N. V. (2004) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00439.2003 · Cited by 157 · see citing works
Structure and Junctional Complexes of Endothelial, Epithelial and Glial Brain Barriers
Dias, M. C., Mapunda, J. A., Vladymyrov, M., & Engelhardt, B. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20215372 · Cited by 152 · see citing works
The origin ofsubdural neomembranes. II. Fine structural of neomembranes.
Friede, R. L., & Schachenmayr, W. (1978) · PubMed Central · Cited by 157 · see citing works
B�ssow, H. (1980) · Cell and Tissue Research · doi:10.1007/bf00237966 · Cited by 156 · see citing works
Barriers in the Immature Brain
Saunders, N. R., Knott, G. W., & Dzięgielewska, K. M. (2000) · Cellular and Molecular Neurobiology · doi:10.1023/a:1006991809927 · Cited by 156 · see citing works
Brain cooling in humans ? anatomical considerations
Zenker, W., & Kubik, S. (1996) · Anatomy and Embryology · doi:10.1007/bf00186829 · Cited by 151 · see citing works
Ek, C. J., Dzięgielewska, K. M., Stolp, H. B., & Saunders, N. R. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.20885 · Cited by 150 · see citing works
The Origin of the Spinal Subdural Space: Ultrastructure Findings
Reina, M. Á., Casasola, O. D. L., López, A., Andrés, J. A. D., Mora, M., & Fernandez, A. L. (2002) · Anesthesia & Analgesia · doi:10.1097/00000539-200204000-00040 · Cited by 144 · see citing works
Saunders, N. R., Habgood, M. D., Møllgård, K., & Dziegielewska, K. M. (2016) · F1000Research · doi:10.12688/f1000research.7378.1 · Cited by 143 · see citing works
Supratentorial intracerebral epithelial (ependymal) cysts: review, case reports, and fine structure.
Friede, R. L., & Yasargil, M. G. (1977) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.40.2.127 · Cited by 141 · see citing works
The human brain intracerebral microvascular system: development and structure
Marín‐Padilla, M. (2012) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2012.00038 · Cited by 140 · see citing works
Living on the Edge of the CNS: Meninges Cell Diversity in Health and Disease
Derk, J., Jones, H. E., Como, C., Pawlikowski, B., & Siegenthaler, J. A. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.703944 · Cited by 120 · see citing works
“…have tight junctions, including expression of occludin and claudin proteins, as well as adherens junctions, that link to actin filaments (Nabeshima et al., 1975; Nakao, 1979; Cassella et al., 1997; Mazaud-Guittot et al., 2010; Zihni et al., 2016; Liebner et al., 2018; Rua and McGavern, 2018).”
BackgroundDeterminants of Passive Drug Entry into the Central Nervous System
Habgood, M. D., Begley, D. J., & Abbott, N. J. (2000) · Cellular and Molecular Neurobiology · doi:10.1023/a:1007001923498 · Cited by 129 · see citing works
Neuroanatomy of cranial dural vessels: implications for subdural hematoma embolization
Shapiro, M., Walker, M., Carroll, K. T., Levitt, M. R., Raz, E., Nossek, E. Z., Delavari, N., Mir, O., & Nelson, P. K. (2021) · Journal of NeuroInterventional Surgery · doi:10.1136/neurintsurg-2020-016798 · Cited by 128 · see citing works
The collagenic architecture of human dura mater
Protasoni, M., Sangiorgi, S., Cividini, A., Culuvaris, G. T., Tomei, G., Dell’Orbo, C., Raspanti, M., Balbi, S., & Reguzzoni, M. (2011) · Journal of neurosurgery · doi:10.3171/2010.12.jns101732 · Cited by 126 · see citing works
Coles, J. A., Myburgh, E., Brewer, J. M., & McMenamin, P. G. (2017) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2017.05.002 · Cited by 123 · see citing works
Selective retrograde labelling of the rat olivocerebellar climbing fiber system with d-[3h]aspartate
Wlklund, L., Toggenburger, G., & Cuénod, M. (1984) · Neuroscience · doi:10.1016/0306-4522(84)90242-2 · Cited by 120 · see citing works
Landis, D. M. D., & Reese, T. S. (1981) · Journal of Experimental Biology · doi:10.1242/jeb.95.1.35 · Cited by 120 · see citing works
Is the pial microvessel a good model for blood-brain barrier studies?
Allt, G., & Lawrenson, J. G. (1997) · Brain Research Reviews · doi:10.1016/s0165-0173(97)00011-8 · Cited by 118 · see citing works
Open pathways for cerebrospinal fluid outflow at the cribriform plate along the olfactory nerves
Spera, I., Cousin, N., Ries, M., Kedracka, A., Castillo, A., Aleandri, S., Vladymyrov, M., Mapunda, J. A., Engelhardt, B., Luciani, P., et al. (2023) · EBioMedicine · doi:10.1016/j.ebiom.2023.104558 · Cited by 117 · see citing works
Assemblies of particles in the cell membranes of developing, mature and reactive astrocytes
Anders, J. J., & Brightman, M. (1979) · Journal of Neurocytology · doi:10.1007/bf01206676 · Cited by 114 · see citing works
Understanding the physiology and pharmacology of epidural and intrathecal opioids
Bernards, C. M. (2002) · Best practice & research. Clinical anaesthesiology · doi:10.1053/bean.2002.0255 · Cited by 111 · see citing works
Boycott, B. B., & Hopkins, J. M. P. (1981) · Neuroscience · doi:10.1016/0306-4522(81)90151-2 · Cited by 110 · see citing works
The developing mouse coronal suture at single-cell resolution
Farmer, D. T., Mlčochová, H., Zhou, Y., Koelling, N., Wang, G., Ashley, N., Bugacov, H., Chen, H.-J., Parvez, R. K., Tseng, K.-C., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-24917-9 · Cited by 106 · see citing works
Shah, T., Leurgans, S. E., Mehta, R. I., Yang, J., Galloway, C. A., Bentley, K. L. D. M., Schneider, J. A., & Mehta, R. I. (2022) · The Journal of Experimental Medicine · doi:10.1084/jem.20220618 · Cited by 108 · see citing works
Outer brain barriers in rat and human development
Brøchner, C. B., Holst, C. B., & Møllgård, K. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00075 · Cited by 104 · see citing works
Kogan, M. J., Aguirre, M. V., Morales-Zavala, F., Toledo, E. G., Guerrero, S., Giralt, E., & Araya, E. (2015) · International Journal of Nanomedicine · doi:10.2147/ijn.s82310 · Cited by 105 · see citing works
Pharmacokinetic Optimisation of the Treatment of Bacterial Central Nervous System Infections
Nau, R., rgel, F. S., & Prange, H. W. (1998) · Clinical Pharmacokinetics · doi:10.2165/00003088-199835030-00005 · Cited by 101 · see citing works
Orlin, J. R., Osen, K. K., & Hovig, T. (1991) · The Anatomical Record · doi:10.1002/ar.1092300104 · Cited by 100 · see citing works
Ultrastructure of the cerebrospinal fluid outflow along the optic nerve into the lymphatic system
L�demann, W., von Rautenfeld, D. B., Samii, M., & Brinker, T. (2004) · Child s Nervous System · doi:10.1007/s00381-004-1040-1 · Cited by 100 · see citing works
Ahirrao, M., & Shrotriya, S. N. (2017) · Drug Development and Industrial Pharmacy · doi:10.1080/03639045.2017.1338721 · Cited by 98 · see citing works
Kumar, N. N., Lochhead, J. J., Pizzo, M. E., Nehra, G., Boroumand, S., Greene, G., & Thorne, R. G. (2018) · Journal of Controlled Release · doi:10.1016/j.jconrel.2018.08.006 · Cited by 95 · see citing works
The intracranial arachnoid mater
Adeeb, N., Deep, A., Griessenauer, C. J., Mortazavi, M. M., Watanabe, K., Loukas, M., Tubbs, R. S., & Cohen‐Gadol, A. (2012) · Child s Nervous System · doi:10.1007/s00381-012-1910-x · Cited by 94 · see citing works
Jahnke, K. (1980) · European Archives of Oto-Rhino-Laryngology · doi:10.1007/bf00455891 · Cited by 93 · see citing works
Morphology and Molecular Properties of Cellular Components of Normal Cerebral Vessels
Nag, S. (2003) · Humana Press eBooks · doi:10.1385/1-59259-419-0:3 · Cited by 94 · see citing works
Macdonald, R. L., & Weir, B. (2001) · Elsevier eBooks · doi:10.1016/b978-012464161-7/50006-8 · Cited by 93 · see citing works
A light and electron microscopic and immunohistochemical study of human arachnoid villi
Kida, S., Yamashima, T., Kubota, T., Ito, H., & Yamamoto, S. (1988) · Journal of neurosurgery · doi:10.3171/jns.1988.69.3.0429 · Cited by 93 · see citing works
Krisch, B., Leonhardt, H., & Buchheim, W. (1978) · Cell and Tissue Research · doi:10.1007/bf00233891 · Cited by 92 · see citing works
Redefining CNS immune privilege
Smyth, L. C. D., & Kipnis, J. (2025) · Nature Reviews Immunology · doi:10.1038/s41577-025-01175-0 · Cited by 80 · see citing works
Distribution of choline acetyltransferase-immunoreactive structures in the lamprey brain
Pombal, M. A., Marín, Ó., & Gonz�lez, A. (2001) · The Journal of Comparative Neurology · doi:10.1002/1096-9861(20010226)431:1 · Cited by 134 · see citing works
A new angle on blood–CNS interfaces: A role for connexins?
Bock, M. D., Vandenbroucke, R. E., Decrock, E., Culot, M., Cecchelli, R., & Leybaert, L. (2014) · FEBS Letters · doi:10.1016/j.febslet.2014.02.060 · Cited by 87 · see citing works
Blood‐brain barrier damage in vascular dementia
Ueno, M., Chiba, Y., Matsumoto, K., Murakami, R., Fujihara, R., Kawauchi, M., Miyanaka, H., & Nakagawa, T. (2015) · Neuropathology · doi:10.1111/neup.12262 · Cited by 87 · see citing works
Acute subdural hematoma from bridging vein rupture: a potential mechanism for growth
Miller, J. D., & Nader, R. (2013) · Journal of neurosurgery · doi:10.3171/2013.10.jns13272 · Cited by 84 · see citing works
Advances and controversies in meningeal biology
Betsholtz, C., Engelhardt, B., Koh, G. Y., McDonald, D. M., Proulx, S. T., & Siegenthaler, J. A. (2024) · Nature Neuroscience · doi:10.1038/s41593-024-01701-8 · Cited by 85 · see citing works
Comparative Physiology of the Blood-Brain Barrier
Abbott, N. J. (1992) · Handbook of experimental pharmacology · doi:10.1007/978-3-642-76894-1_15 · Cited by 83 · see citing works
Proulx, S. T., & Engelhardt, B. (2022) · Journal of Internal Medicine · doi:10.1111/joim.13469 · Cited by 83 · see citing works
Salahuddin, T. S., Kalimo, H., Johansson, B. B., & Olsson, Y. (1988) · Acta Neuropathologica · doi:10.1007/bf00687674 · Cited by 78 · see citing works
Iwaki, T., Fukui, M., Kondo, A., Matsushima, T., & Takeshita, I. (1987) · Acta Neuropathologica · doi:10.1007/bf00692844 · Cited by 76 · see citing works
Border-associated macrophages as gatekeepers of brain homeostasis and immunity
Vara‐Pérez, M., & Movahedi, K. (2025) · Immunity · doi:10.1016/j.immuni.2025.04.005 · Cited by 81 · see citing works
- Authors
- Nabeshima, S., Reese, T. S., Landis, D. M. D., & Brightman, M. W.
- Affiliations
- National Institutes of Health (US)
- Venue
- Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 1975-11-15
- Volume
- 164
- Issue
- 2
- Pages
- 127-169
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- OpenAlex
- W1975635783
- Cited by
- 444
- References
- 25
- Citations by year
- 2026: 15 · 2025: 16 · 2024: 25 · 2023: 14 · 2022: 27 · 2021: 12 · 2020: 11 · 2019: 12 · 2018: 12 · 2017: 20 · 2016: 9 · 2015: 7 · 2014: 8 · 2013: 13 · 2012: 7
- FWCI
- 7.65
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Comparative Neurology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Cerebrospinal fluid and hydrocephalus
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion Transport and Channel Regulation
- Keywords
- tight junctions, subarachnoid space, cerebrospinal fluid, gap junctions, desmosomes, astrocytes, subdural space, intercellular junctions, meninges
- MeSH terms
- Animals, Haplorhini, Arachnoid, Astrocytes, Cats, Chinchilla, Desmosomes, Dura Mater, Freeze Fracturing, Intercellular Junctions, Macaca, Meninges, Microscopy, Electron, Neuroglia, Pia Mater, Rabbits, Species Specificity, Mice, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review