Difference between revisions of "Neural - Meninges Development"
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The meninges (singular meninx; Greek, meninx = membrane) are a complex connective tissue surrounding the central nervous system (brain and spinal cord). The 3 layers from the central nervous outward are: pia mater, arachnoid mater, and the dura mater. All three layers form from the meninx primitiva, a meningeal mesenchyme. The pia mater and the arachnoid can together be called called leptomeninx, and dura mater the pachymeninx.
There have been many theories to the embryonic origins of the three layers that form the meninges, as well as potential differences between species. The safest term would be mesenchymal in origin, but the actual source of this mesenchyme may also differ in the same species at different levels of the central nervous system. The space under the arachnoid layer (subarachnoid space) is filled with cerebrospinal fluid.
Recent studies also suggest that rather than acting as a passive connective tissue "neural container" during development, the meninges may also interact and regulate cranial skull and neural development.
See also the 1951 paper describing spinal cord meninges development.
Some Recent Findings
|More recent papers|
This table allows an automated computer search of the external PubMed database using the listed "Search term" text link.
Search term: Meninges Development
<pubmed limit=5>Meninges Development</pubmed>
Search term: Pia Development
<pubmed limit=5>Pia Development</pubmed>
Search term: Arachnoid Development
<pubmed limit=5>Arachnoid Development</pubmed>
Search term: Dura Development
<pubmed limit=5>Dura Development</pubmed>
A fine connective tissue covering of the central nervous system, forms innermost part of the meningial layers. Lies beneath the arachnoid mater and then tough outer dura mater layer. All three layers form from the meninx primitiva, a meningeal mesenchyme that is mesodermal and neural crest in origin. The space overlying the pia mater (subarachnoid space) is filled with cerebrospinal fluid. The pia mater has close contact with the spinal cord and brain, in the brain it follows down into the sulci and fissures of the cortex. This layer also fuses with the membranous lining of the ventricles (ependyma) forming the choroid plexus.
(Greek, arachne = spider + -oeides = form) A meshwork (spider web-like) connective tissue covering of the central nervous system, forms part of the meningial layers. Lies between tough outer dura mater layer and the inner fine pia mater layer. All three layers form from the meninx primitiva, a meningeal mesenchyme that is mesodermal and neural crest in origin. The space underlying the arachnoid mater (subarachnoid space) is filled with cerebrospinal fluid.
(Latin, dura mater = hard mother) The outer tough connective tissue meningial coat of the 3 layers that cover the central nervous system of 3 layers (overlays the arachnoid mater middle layer and pia mater inner layer). All three layers form from the meninx primitiva, a meningeal mesenchyme that is mesodermal and neural crest in origin.
At the level of the skull, the outer dura layer forms the inner periosteum of the skull and the inner dura layer forms the dural folds (falx and tentorium) that contains the dural sinuses. The dura mater also expresses osteogenic growth factors that may be required for ossification of cranial vault bones. At the level of the spinal cord, the dura is separated from the periosteum of the vertebral canal by an epidural space.
Dural Venous Sinuses
The dural venous sinuses form the major drainage of the brain to the internal jugular veins in the adult.
The dural venous sinuses:
- lie between the dura mater layers (endosteal layer and meningeal)
- run alone not parallel to arteries.
- are valveless allowing for bidirectional blood flow
Unpaired - superior sagittal sinus, inferior sagittal sinus, straight sinus, occipital sinus, intercavernous sinus Paired - transverse sinus, sigmoid sinus, superior petrosal sinus, inferior petrosal sinus, cavernous sinus, sphenoparietal sinus, basilar venous plexus
The following figures are from a 1915 study of the venous sinuses of the dura mater in the human embryo.
fig 1 embryo 4 mm No. 588
fig 2 embryo 13.8 mm No. 940
fig 3 embryo 18 mm No. 144
fig 4 embryo 21 mm No. 460
fig 5 embryo 24 mm No. 632
fig 6 embryo 50 mm No. 96
fig 7 embryo 13.8 mm No. 940
fig 8 embryo 20 mm No. 349
fig 9 fetus 54 mm No. 458
fig 11 embryo 14 mm No. 940
fig 12 embryo 18 mm No. 144
fig 13 embryo 21 mm No. 460
fig 14 embryo 35 mm No. 100
fig 15 fetus 50 mm No. 96
fig 16 fetus 80 mm No. 234a
CoupTFI Interacts with Retinoic Acid Signaling during Cortical Development
PLoS One. 2013;8(3):e58219. doi: 10.1371/journal.pone.0058219. Epub 2013 Mar 5.
Harrison-Uy SJ, Siegenthaler JA, Faedo A, Rubenstein JL, Pleasure SJ. Source Department of Neurology, University of California San Francisco, San Francisco, California, United States of America.
We examined the role of the orphan nuclear hormone receptor CoupTFI in mediating cortical development downstream of meningeal retinoic acid signaling. CoupTFI is a regulator of cortical development known to collaborate with retinoic acid (RA) signaling in other systems. To examine the interaction of CoupTFI and cortical RA signaling we utilized Foxc1-mutant mice in which defects in meningeal development lead to alterations in cortical development due to a reduction of RA signaling. By analyzing CoupTFI(-/-);Foxc1(H/L) double mutant mice we provide evidence that CoupTFI is required for RA rescue of the ventricular zone and the neurogenic phenotypes in Foxc1-mutants. We also found that overexpression of CoupTFI in Foxc1-mutants is sufficient to rescue the Foxc1-mutant cortical phenotype in part. These results suggest that CoupTFI collaborates with RA signaling to regulate both cortical ventricular zone progenitor cell behavior and cortical neurogenesis.
The cranial dura mater: a review of its history, embryology, and anatomy
Childs Nerv Syst. 2012 Jun;28(6):827-37. doi: 10.1007/s00381-012-1744-6. Epub 2012 Apr 15.
Adeeb N, Mortazavi MM, Tubbs RS, Cohen-Gadol AA. Abstract INTRODUCTION: The dura mater is important to the clinician as a barrier to the internal environment of the brain, and surgically, its anatomy should be well known to the neurosurgeon and clinician who interpret imaging. METHODS: The medical literature was reviewed in regard to the morphology and embryology of specifically, the intracranial dura mater. A historic review of this meningeal layer is also provided. CONCLUSIONS: Knowledge of the cranial dura mater has a rich history. The embryology is complex, and the surgical anatomy of this layer and its specializations are important to the neurosurgeon.
A cascade of morphogenic signaling initiated by the meninges controls corpus callosum formation
Neuron. 2012 Feb 23;73(4):698-712. doi: 10.1016/j.neuron.2011.11.036.
Choe Y, Siegenthaler JA, Pleasure SJ. Source Department of Neurology, University of California, San Francisco, San Francisco, CA 94158, USA.
The corpus callosum is the most prominent commissural connection between the cortical hemispheres, and numerous neurodevelopmental disorders are associated with callosal agenesis. By using mice either with meningeal overgrowth or selective loss of meninges, we have identified a cascade of morphogenic signals initiated by the meninges that regulates corpus callosum development. The meninges produce BMP7, an inhibitor of callosal axon outgrowth. This activity is overcome by the induction of expression of Wnt3 by the callosal pathfinding neurons, which antagonize the inhibitory effects of BMP7. Wnt3 expression in the cingulate callosal pathfinding axons is developmentally regulated by another BMP family member, GDF5, which is produced by the adjacent Cajal-Retzius neurons and turns on before outgrowth of the callosal axons. The effects of GDF5 are in turn under the control of a soluble GDF5 inhibitor, Dan, made by the meninges. Thus, the meninges and medial neocortex use a cascade of signals to regulate corpus callosum development. Copyright © 2012 Elsevier Inc. All rights reserved.
We have got you 'covered': how the meninges control brain development.
Curr Opin Genet Dev. 2011 Jun;21(3):249-55. doi: 10.1016/j.gde.2010.12.005. Epub 2011 Jan 20.
Siegenthaler JA, Pleasure SJ. Source Department of Neurology, Programs in Neuroscience and Developmental Biology, Institute for Regenerative Medicine, University of California, San Francisco, San Francisco, CA 94158, United States.
The meninges have traditionally been viewed as specialized membranes surrounding and protecting the adult brain from injury. However, there is increasing evidence that the fetal meninges play important roles during brain development. Through the release of diffusible factors, the meninges influence the proliferative and migratory behaviors of neural progenitors and neurons in the forebrain and hindbrain. Meningeal cells also secrete and organize the pial basement membrane (BM), a critical anchor point for the radially oriented fibers of neuroepithelial stem cells. With its emerging role in brain development, the potential that defects in meningeal development may underlie certain congenital brain abnormalities in humans should be considered. In this review, we will discuss what is known about assembly of the fetal meninges and review the role of meningeal-derived proteins in mouse and human brain development. Copyright © 2011 Elsevier Ltd. All rights reserved.
Tissue origins and interactions in the mammalian skull vault
Dev Biol. 2002 Jan 1;241(1):106-16. Jiang X, Iseki S, Maxson RE, Sucov HM, Morriss-Kay GM. Source Institute for Genetic Medicine, University of Southern California Keck School of Medicine, Los Angeles, California 90033, USA.
During mammalian evolution, expansion of the cerebral hemispheres was accompanied by expansion of the frontal and parietal bones of the skull vault and deployment of the coronal (fronto-parietal) and sagittal (parietal-parietal) sutures as major growth centres. Using a transgenic mouse with a permanent neural crest cell lineage marker, Wnt1-Cre/R26R, we show that both sutures are formed at a neural crest-mesoderm interface: the frontal bones are neural crest-derived and the parietal bones mesodermal, with a tongue of neural crest between the two parietal bones. By detailed analysis of neural crest migration pathways using X-gal staining, and mesodermal tracing by DiI labelling, we show that the neural crest-mesodermal tissue juxtaposition that later forms the coronal suture is established at E9.5 as the caudal boundary of the frontonasal mesenchyme. As the cerebral hemispheres expand, they extend caudally, passing beneath the neural crest-mesodermal interface within the dermis, carrying with them a layer of neural crest cells that forms their meningeal covering. Exposure of embryos to retinoic acid at E10.0 reduces this meningeal neural crest and inhibits parietal ossification, suggesting that intramembranous ossification of this mesodermal bone requires interaction with neural crest-derived meninges, whereas ossification of the neural crest-derived frontal bone is autonomous. These observations provide new perspectives on skull evolution and on human genetic abnormalities of skull growth and ossification.
The meninges in human development
J Neuropathol Exp Neurol. 1986 Sep;45(5):588-608.
O'Rahilly R, Müller F.
The brain and cranial meninges were studied in 61 serially sectioned embryos of stages 8-23. Much earlier stages than those examined by previous authors provided a more comprehensive view of meningeal development. As a result, the possible and probable sources of the cranial and spinal meninges are believed to be: (a) prechordal plate, (b) unsegmented paraxial (parachordal) mesoderm, (c) segmented paraxial (somitic) mesoderm, (d) mesectoderm (neural crest), (e) neurilemmal cells (neural crest), and (f) neural tube. Some of these sources (a, b, d) pertain to the cranial meninges, others (c, d, e) to the spinal coverings. The first of the future dural processes to develop is the tentorium cerebelli, which, at the end of the embryonic period proper, differs considerably in shape and composition from the later fetal and postnatal tentorium. The embryonic dural limiting layer (Duragrenzschicht) probably corresponds to the interface layer of the adult meninges. The appropriate literature was reviewed and summarized.
- Sensenig EC. The early development of the meninges of the spinal cord in human embryos. (1951) Contrib. Embryol., Carnegie Inst. Wash. Publ. 611.
- Izen RM, Yamazaki T, Nishinaka-Arai Y, Hong YK & Mukouyama YS. (2018). Postnatal development of lymphatic vasculature in the brain meninges. Dev. Dyn. , , . PMID: 29493038 DOI.
- Yay A, Ozdamar S, Canoz O, Baran M, Tucer B & Sonmez MF. (2014). Intermediate filament protein nestin is expressed in developing meninges. Bratisl Lek Listy , 115, 718-22. PMID: 25428542
- Streeter GL. The development of the venous sinuses of the dura mater in the human embryo. (1915) Amer. J Anat.18: 145-178.
Weller RO, Sharp MM, Christodoulides M, Carare RO & Møllgård K. (2018). The meninges as barriers and facilitators for the movement of fluid, cells and pathogens related to the rodent and human CNS. Acta Neuropathol. , 135, 363-385. PMID: 29368214 DOI.
Mortazavi MM, Quadri SA, Khan MA, Gustin A, Suriya SS, Hassanzadeh T, Fahimdanesh KM, Adl FH, Fard SA, Taqi MA, Armstrong I, Martin BA & Tubbs RS. (2018). Subarachnoid Trabeculae: A Comprehensive Review of Their Embryology, Histology, Morphology, and Surgical Significance. World Neurosurg , 111, 279-290. PMID: 29269062 DOI.
Adeeb N, Mortazavi MM, Deep A, Griessenauer CJ, Watanabe K, Shoja MM, Loukas M & Tubbs RS. (2013). The pia mater: a comprehensive review of literature. Childs Nerv Syst , 29, 1803-10. PMID: 23381008 DOI.
Patel N & Kirmi O. (2009). Anatomy and imaging of the normal meninges. Semin. Ultrasound CT MR , 30, 559-64. PMID: 20099639
Yokogawa N, Murakami H, Demura S, Kato S, Yoshioka K, Yamamoto M, Iseki S & Tsuchiya H. (2015). Effects of Radiation on Spinal Dura Mater and Surrounding Tissue in Mice. PLoS ONE , 10, e0133806. PMID: 26214850 DOI.
Baltsavias G, Parthasarathi V, Aydin E, Al Schameri RA, Roth P & Valavanis A. (2015). Cranial dural arteriovenous shunts. Part 1. Anatomy and embryology of the bridging and emissary veins. Neurosurg Rev , 38, 253-63; discussion 263-4. PMID: 25468011 DOI.
Tochitani S & Kondo S. (2013). Immunoreactivity for GABA, GAD65, GAD67 and Bestrophin-1 in the meninges and the choroid plexus: implications for non-neuronal sources for GABA in the developing mouse brain. PLoS ONE , 8, e56901. PMID: 23437266 DOI.
Search Pubmed: Development Meninges Development
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Cite this page: Hill, M.A. (2021, June 24) Embryology Neural - Meninges Development. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Neural_-_Meninges_Development
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