Glia limitans

Glia limitans
Glia limitans
	The glia limitans (in dark blue) lies between the pia mater and the cerebral cortex
Details
Parts	Astrocyte, Basal lamina
Identifiers
Latin	Glia limitans
NeuroLex ID	nlx_subcell_100209
	Anatomical terms of neuroanatomy [ edit on Wikidata]

Last updated July 17, 2021

The glia limitans, or the glial limiting membrane, is a thin barrier of astrocyte foot processes associated with the parenchymal basal lamina surrounding the brain and spinal cord. It is the outermost layer of neural tissue, and among its responsibilities is the prevention of the over-migration of neurons and neuroglia, the supporting cells of the nervous system, into the meninges. The glia limitans also plays an important role in regulating the movement of small molecules and cells into the brain tissue by working in concert with other components of the central nervous system (CNS) such as the blood–brain barrier (BBB).^[1]

Location and structure

The perivascular feet of astrocytes form a close association with the basal lamina of the brain parenchyma ^[2] to create the glia limitans. This membrane lies deep to the pia mater and the subpial space and surrounds the perivascular spaces (Virchow-Robin spaces). Any substance entering the central nervous system from the blood or cerebrospinal fluid (CSF) must cross the glia limitans.

The two different classifications of glial limiting membrane, the glia limitans perivascularis and the glia limitans superficialis, have nearly identical structures, however, they can be distinguished from each other by their location within the brain. The glia limitans perivascularis abuts the perivascular space surrounding the parenchymal blood vessels and functions as a supportive constituent of the blood–brain barrier. In contrast, the non-parenchymal blood vessels present in the subarachnoid space are not covered by the glia limitans. Instead, the entire subarachnoid space is sealed towards the nervous tissue by the glia limitans superficialis.^[3] These two parts of the glia limitans are continuous; however, convention dictates that the part that covers the surface of the brain is referred to as the superficialis, and the part that encloses the blood vessels within the brain is called the perivascularis.

Function

Physical barrier

The main role of the glia limitans is to act as a physical barrier against unwanted cells or molecules attempting to enter the CNS. The glia limitans compartmentalizes the brain to insulate the parenchyma from the vascular and subarachnoid compartments.^[4] Within the brain, the glial limiting membrane is an important constituent of the blood–brain barrier. Experiments using electron-dense markers have discovered that functional components of the blood–brain barrier are the endothelial cells that compose the vessel itself. These endothelial cells contain highly impermeable tight junctions that cause the blood vessels of the brain to exhibit none of the “leakiness” found in arteries and veins elsewhere in the body.^[5] Through both in vivo and in vitro experiments the astrocytic foot processes of the glia limitans were shown to induce the formation of the tight junctions of the endothelial cells during brain development.^[6] The in vivo experiment involved harvested rat astrocytes that were placed into the anterior chamber of a chick-eye or on the chorioallantois. Permeable blood vessels from either the iris or chorioallantois became impermeable to blue-albumin once they had entered the transplanted bolus of astrocytes. In the in vitro experiment, endothelial cells were first cultured alone and the tight junctions were observed in freeze-fracture replicas to be discontinuous and riddled with gap junctions. Then, the brain endothelial cells were cultured with astroctytes resulting in enhanced tight junctions and a reduced frequency of gap junctions.

The glia limitans also acts as a second line of defense against anything that passes the blood–brain barrier. However, because the astrocytes surrounding the vessels are connected by gap junctions, it is not considered part of the BBB and material can readily pass between the foot processes.

Immunological barrier

The astrocytes of the glia limitans are responsible for separating the brain into two primary compartments. The first compartment is the immune-privileged brain and spinal cord parenchyma. This compartment contains multiple immunosuppressive cell surface proteins such as CD200 and CD95L and it allows for the release of anti-inflammatory factors. The second compartment is that of the non-immune-privileged subarachnoid, subpial, and perivascular spaces. This area is filled with pro-inflammatory factors such as antibodies, complement proteins, cytokines, and chemokines. The astrocytes of the glia limitans are believed to be the component of the brain that secretes the pro- and anti-inflammatory factors.^[1]

Development

The development of the long astrocyte cellular processes that are integral to the glia limitans structure has been linked to the presence of meningeal cells in the pia mater.^[7] Meningeal cells are specialized fibroblast-like cells that surround the CNS and major blood vessels. They have been found to co-operate with astrocytes in the initial formation of the glia limitans during development and participate in its continued maintenance throughout life. Artificially induced destruction of meningeal cells during CNS development have been found to result in the alteration of subpial extracellular matrix and a disruption of the glia limitans.^[8]

The glia limitans has also proven to be important in the recovery of the CNS after injuries. When lesions are made on the brain surface, meningeal cells will divide and migrate into the lesion, eventually lining the entire injury cavity. If the injury has significantly reduced the density of astrocytes and created space within the tissue, the meningeal cells will invade even more diffusely. As invading meningeal cells make contact with astrocytes, they can induce the formation of a new, functional glia limitans. The new glia limitans formed after CNS injury usually presents itself as a barrier to regenerating axons.^[9]

Clinical relevance

There are a number of diseases associated with problems or abnormalities with the glia limitans. Many diseases can arise from a breach to the glia limitans in which it will no longer be able to fulfill its functional role as a barrier. Two of the more common diseases resulting from a breach to the glia limitans are described below.

Fukuyama-type congenital muscular dystrophy (FCMD)

Breaches in the glia limitans-basal lamina complex have been associated with Fukuyama-type congenital muscular dystrophy (FCMD), which is thought to be the result of micropolygyri, or small protrusions of nervous tissue.^[10] Although the underlying mechanism for the formation of these breaches is largely unknown, recent research has indicated that the protein fukutin is directly linked to the developing lesions. Mutations in the fukutin protein lead to a depressed level of its expression in the brain and spinal cord of neonatal subjects, which in turn has been found to contribute to the weakening of the structural integrity of the glia limitans. Neuronal and glial cells migrate through the weakened barrier resulting in the accumulation of neural tissue in the subarachnoid space. This abnormal migration, known as cortical dysplasia, is theorized to be one of the primary causes for FCMD.^[11]

Experimental autoimmune encephalomyelitis (EAE)

It has been demonstrated that the clinical signs of experimental autoimmune encephalomyelitis (EAE) are only evident after the penetration of inflammatory cells across the glia limitans and upon entrance into the CNS parenchyma. The activity of matrix metalloproteinases, specifically MMP-2 and MMP-9, are required for the penetration of the glia limitans by inflammatory cells. This is most likely due to the biochemistry of the parenchymal basement membrane and the astrocytic foot processes. MMP-2 and MMP-9 are both produced by myeloid cells, which surround T cells in the perivascular space. These metalloproteinases allow immune cells to breach the glia limitans and reach the CNS parenchyma to attack the CNS parenchymal cells. Once the immune cells have reached the CNS parenchyma and the immune attack is underway, the CNS parenchymal cells are sacrificed in order to battle the infection. The autoimmune response to EAE leads to chronic attack of oligodendrocytes and neurons, which promotes demyelination and axonal loss. This can ultimately result in the loss of CNS neurons.^[3]

Comparative anatomy

Because the glia limitans serves such an important structural and physiological function in human beings, it is unsurprising that evolutionary precursors of the glial limiting membrane can be found in many other animals.

Insects have an open circulatory system, so there are no blood vessels found within their ganglia. However, they do have a sheath of perineurial glial cells that envelops the nervous system and exhibit the same tight occluding junctions that are induced by the glia limitans in humans. These cells act as a barrier and are responsible for establishing permeability gradients.

In certain molluscs, a glial-interstitial fluid barrier is observed without the presence of tight junctions. Cephalopod molluscs, in particular, have cerebral ganglia that have microcirculation, often seen in the composition of higher organisms. Often, the glial cells will form a seamless sheath completely around the blood space. The barrier consists of zonular intercellular junctions, rather than tight junctions, with clefts formed by extracellular fibrils. In addition to protection from the blood, these barriers are thought to exhibit local control of the microenvironment around specific neuron groups, a function required for complex nervous systems.^[6]

Monkeys and other primates have been found to have a glial limiting membrane extremely similar to humans. Studies on these animals have revealed that the thickness of the glia limitans not only varies greatly among different species, but also within different regions of the central nervous system of the same organism. Further observations of young and old monkeys have proven that the younger subjects have thinner membranes with fewer layers of astrocytic processes while the older monkeys possess much thicker membranes.^[12]

Current research

As of 2011, research is focused on the two-way communication between neurons and glial cells. Communication between these two types of cells allows for axonal conduction, synaptic transmission, as well as the processing of information to regulate and better control the processes of the central nervous system. The various forms of communication include neurotransmission, ion fluxes and signaling molecules. As recently as 2002, new information on the process of neuron-glia communication was published by R. Douglas Fields and Beth Stevens-Graham. They used advanced imaging methods to explain that the ion channels seen in glial cells did not contribute to action potentials but rather allowed the glia to determine the level of neuronal activity within proximity. Glial cells were determined to communicate with one another solely with chemical signals and even had specialized glial-glial and neuron-glial neurotransmitter signaling systems. Additionally, neurons were found to release chemical messengers in extrasynaptic regions, suggesting that the neuron-glial relationship includes functions beyond synaptic transmission. Glia have been known to assist in synapse formation, regulating synapse strength, and information processing as mentioned above. The process for adenosine triphosphate (ATP), glutamate, and other chemical messenger release from glia is debated and is seen as a direction for future research.^[13]

Related Research Articles

The blood–brain barrier (BBB) is a highly selective semipermeable border of endothelial cells that prevents solutes in the circulating blood from non-selectively crossing into the extracellular fluid of the central nervous system where neurons reside. The blood–brain barrier is formed by endothelial cells of the capillary wall, astrocyte end-feet ensheathing the capillary, and pericytes embedded in the capillary basement membrane. This system allows the passage of some molecules by passive diffusion, as well as the selective and active transport of various nutrients, ions, organic anions, and macromolecules such as glucose, water and amino acids that are crucial to neural function.

Nervous tissue, also called neural tissue, is the main tissue component of the nervous system. The nervous system regulates and controls bodily functions and activity. It consists of two parts: the central nervous system (CNS) comprising the brain and spinal cord, and the peripheral nervous system (PNS) comprising the branching peripheral nerves. It is composed of neurons, also known as nerve cells, which receive and transmit impulses, and neuroglia, also known as glial cells or glia, which assist the propagation of the nerve impulse as well as provide nutrients to the neurons.

In anatomy, the meninges are the three membranes that envelop the brain and spinal cord. In mammals, the meninges are the dura mater, the arachnoid mater, and the pia mater. Cerebrospinal fluid is located in the subarachnoid space between the arachnoid mater and the pia mater. The primary function of the meninges is to protect the central nervous system.

Pia mater Delicate innermost layer of the meninges, the membranes surrounding the brain and spinal cord

Pia mater, often referred to as simply the pia, is the delicate innermost layer of the meninges, the membranes surrounding the brain and spinal cord. Pia mater is medieval Latin meaning "tender mother". The other two meningeal membranes are the dura mater and the arachnoid mater. Both the pia and arachnoid mater are derivatives of the neural crest while the dura is derived from embryonic mesoderm. The pia mater is a thin fibrous tissue that is permeable to water and small solutes. The pia mater allows blood vessels to pass through and nourish the brain. The perivascular space between blood vessels and pia mater is proposed to be part of a pseudolymphatic system for the brain. When the pia mater becomes irritated and inflamed the result is meningitis.

Glia, also called glial cells or neuroglia, are non-neuronal cells in the central nervous system and the peripheral nervous system that do not produce electrical impulses. They maintain homeostasis, form myelin in the peripheral nervous system, and provide support and protection for neurons. In the central nervous system, glial cells include oligodendrocytes, astrocytes, ependymal cells, and microglia, and in the peripheral nervous system glial cells include Schwann cells and satellite cells. They have four main functions: (1) to surround neurons and hold them in place; (2) to supply nutrients and oxygen to neurons; (3) to insulate one neuron from another; (4) to destroy pathogens and remove dead neurons. They also play a role in neurotransmission and synaptic connections, and in physiological processes like breathing. While glia were thought to outnumber neurons by a ratio of 10:1, recent studies using newer methods and reappraisal of historical quantitative evidence suggests an overall ratio of less than 1:1, with substantial variation between different brain tissues.

Astrocytes, also known collectively as astroglia, are characteristic star-shaped glial cells in the brain and spinal cord. They perform many functions, including biochemical support of endothelial cells that form the blood–brain barrier, provision of nutrients to the nervous tissue, maintenance of extracellular ion balance, regulation of cerebral blood flow, and a role in the repair and scarring process of the brain and spinal cord following infection and traumatic injuries. The proportion of astrocytes in the brain is not well defined; depending on the counting technique used, studies have found that the astrocyte proportion varies by region and ranges from 20% to 40% of all glia. Another study reports that astrocytes are the most numerous cell type in the brain. Astrocytes are the major source of cholesterol in the central nervous system. Apolipoprotein E transports cholesterol from astrocytes to neurons and other glial cells, regulating cell signaling in the brain. Astrocytes in humans are more than twenty times larger than in rodent brains, and make contact with more than ten times the number of synapses.

Astrogliosis is an abnormal increase in the number of astrocytes due to the destruction of nearby neurons from central nervous system (CNS) trauma, infection, ischemia, stroke, autoimmune responses or neurodegenerative disease. In healthy neural tissue, astrocytes play critical roles in energy provision, regulation of blood flow, homeostasis of extracellular fluid, homeostasis of ions and transmitters, regulation of synapse function and synaptic remodeling. Astrogliosis changes the molecular expression and morphology of astrocytes, in response to infection for example, in severe cases causing glial scar formation that may inhibit axon regeneration.

Microglia are a type of neuroglia located throughout the brain and spinal cord. Microglia account for 10–15% of all cells found within the brain. As the resident macrophage cells, they act as the first and main form of active immune defense in the central nervous system (CNS). Microglia are distributed in large non-overlapping regions throughout the CNS. Microglia are key cells in overall brain maintenance—they are constantly scavenging the CNS for plaques, damaged or unnecessary neurons and synapses, and infectious agents. Since these processes must be efficient to prevent potentially fatal damage, microglia are extremely sensitive to even small pathological changes in the CNS. This sensitivity is achieved in part by the presence of unique potassium channels that respond to even small changes in extracellular potassium. Recent evidence shows that microglia are also key players in the sustainment of normal brain functions under healthy conditions. Microglia also constantly monitor neuronal functions through direct somatic contacts and exert neuroprotective effects when needed.

Pericyte Contractile cells that wrap around the endothelial cells of capillaries and venules throughout the body

Pericytes are multi-functional mural cells of the microcirculation that wrap around the endothelial cells that line the capillaries and venules throughout the body. Pericytes are embedded in basement membrane, where they communicate with endothelial cells of the body's smallest blood vessels by means of both direct physical contact and paracrine signaling. Pericytes help to maintain homeostatic and hemostatic functions in the brain and also sustain the blood–brain barrier. These cells are also a key component of the neurovascular unit, which includes endothelial cells, astrocytes, and neurons. Pericytes regulate capillary blood flow, the clearance and phagocytosis of cellular debris, and the permeability of the blood–brain barrier. Pericytes stabilize and monitor the maturation of endothelial cells by means of direct communication between the cell membrane as well as through paracrine signaling. A deficiency of pericytes in the central nervous system can cause the blood–brain barrier to break down.

A perivascular space, also known as a Virchow–Robin space, is a fluid-filled space surrounding certain blood vessels in several organs, including the brain, potentially having an immunological function, but more broadly a dispersive role for neural and blood-derived messengers. The brain pia mater is reflected from the surface of the brain onto the surface of blood vessels in the subarachnoid space. In the brain, perivascular cuffs are regions of leukocyte aggregation in the perivascular spaces, usually found in patients with viral encephalitis.

The neuroimmune system is a system of structures and processes involving the biochemical and electrophysiological interactions between the nervous system and immune system which protect neurons from pathogens. It serves to protect neurons against disease by maintaining selectively permeable barriers, mediating neuroinflammation and wound healing in damaged neurons, and mobilizing host defenses against pathogens.

Gliosis is a nonspecific reactive change of glial cells in response to damage to the central nervous system (CNS). In most cases, gliosis involves the proliferation or hypertrophy of several different types of glial cells, including astrocytes, microglia, and oligodendrocytes. In its most extreme form, the proliferation associated with gliosis leads to the formation of a glial scar.

Tanycytes are special ependymal cells found in the third ventricle of the brain, and on the floor of the fourth ventricle and have processes extending deep into the hypothalamus. It is possible that their function is to transfer chemical signals from the cerebrospinal fluid to the central nervous system.

Glial scar formation (gliosis) is a reactive cellular process involving astrogliosis that occurs after injury to the central nervous system. As with scarring in other organs and tissues, the glial scar is the body's mechanism to protect and begin the healing process in the nervous system.

Leptomeningeal cancer is a rare complication of cancer in which the disease spreads from the original tumor site to the meninges surrounding the brain and spinal cord. This leads to an inflammatory response, hence the alternative names neoplastic meningitis (NM), malignant meningitis, or carcinomatous meningitis. The term leptomeningeal describes the thin meninges, the arachnoid and the pia mater, between which the cerebrospinal fluid is located. The disorder was originally reported by Eberth in 1870.

Potassium spatial buffering is a mechanism for the regulation of extracellular potassium concentration by astrocytes. Other mechanisms for astrocytic potassium clearance are carrier-operated or channel-operated potassium chloride uptake. The repolarization of neurons tends to raise potassium concentration in the extracellular fluid. If a significant rise occurs, it will interfere with neuronal signaling by depolarizing neurons. Astrocytes have large numbers of potassium ion channels facilitating removal of potassium ions from the extracellular fluid. They are taken up at one region of the astrocyte and then distributed throughout the cytoplasm of the cell, and further to its neighbors via gap junctions. This keeps extracellular potassium at levels that prevent interference with normal propagation of an action potential.

Drug delivery to the brain is the process of passing therapeutically active molecules across the blood–brain barrier for the purpose of treating brain maladies. This is a complex process that must take into account the complex anatomy of the brain as well as the restrictions imposed by the special junctions of the blood–brain barrier.

The glymphatic system was described and named in 2013 as a system for waste clearance in the central nervous system (CNS) of vertebrates. According to this model, cerebrospinal fluid (CSF) flows into the paravascular space around cerebral arteries, combining with interstitial fluid (ISF) and parenchymal solutes, and exiting down venous paravascular spaces. The pathway consists of a para-arterial influx route for cerebrospinal fluid (CSF) to enter the brain parenchyma, coupled to a clearance mechanism for the removal of interstitial fluid (ISF) and extracellular solutes from the interstitial compartments of the brain and spinal cord. Exchange of solutes between CSF and ISF is driven primarily by arterial pulsation and regulated during sleep by the expansion and contraction of brain extracellular space. Clearance of soluble proteins, waste products, and excess extracellular fluid is accomplished through convective bulk flow of ISF, facilitated by astrocytic aquaporin 4 (AQP4) water channels.

Neuroinflammation is inflammation of the nervous tissue. It may be initiated in response to a variety of cues, including infection, traumatic brain injury, toxic metabolites, or autoimmunity. In the central nervous system (CNS), including the brain and spinal cord, microglia are the resident innate immune cells that are activated in response to these cues. The CNS is typically an immunologically privileged site because peripheral immune cells are generally blocked by the blood–brain barrier (BBB), a specialized structure composed of astrocytes and endothelial cells. However, circulating peripheral immune cells may surpass a compromised BBB and encounter neurons and glial cells expressing major histocompatibility complex molecules, perpetuating the immune response. Although the response is initiated to protect the central nervous system from the infectious agent, the effect may be toxic and widespread inflammation as well as further migration of leukocytes through the blood–brain barrier.

The blood-spinal cord barrier (BSCB) is a semipermeable anatomical interface that consists of the specialized small blood vessels that surround the spinal cord. While similar to the blood-brain barrier in function and morphology, it is physiologically independent and has several distinct characteristics. The BSCB is involved in many disorders affecting the central nervous system, including neurodegenerative diseases, pain disorders, and traumatic spinal cord injury. In conjunction with the blood-brain barrier, the BSCB contributes to the difficulty in delivering drugs to the central nervous system, which makes drug targeting of the BSCB an important goal in pharmaceutical research.

References

1 2 Helmut Kettenmann; Bruce R. Ransom (2005). Neuroglia. Oxford University Press US. pp. 303–305. ISBN 978-0-19-515222-7 . Retrieved 20 March 2011.
↑ Saladin, Kenneth S. (2011). Human Anatomy. p. 358. ISBN 9780071222075.
1 2 Engelhardt B, Coisne C (2011). "Fluids and barriers of the CNS establish immune privilege by confining immune surveillance to a two-walled castle moat surrounding the CNS castle". Fluids Barriers CNS. 8 (1): 4. doi:10.1186/2045-8118-8-4. PMC 3039833 . PMID 21349152.
↑ Alekseǐ Nestorovich Verkhratskiǐ; Arthur Butt (2007). Glial neurobiology: a textbook. John Wiley and Sons. p. 24. ISBN 978-0-470-01564-3 . Retrieved 20 March 2011.
↑ Alan Peters; Sanford L. Palay; Henry deF. Webster (1991). The fine structure of the nervous system: neurons and their supporting cells. Oxford University Press. pp. 292–293. ISBN 978-0-19-506571-8 . Retrieved 25 March 2011.
1 2 Brightman, Milton (1991). "Implication of Astroglia in the Blood–Brain Barrier". In Abbot, N.J. (ed.). Glial-Neuronal Interaction. New York Academy of Sciences. p. 633. ISBN 0-89766-680-1.
↑ Struckhoff, Gernot (1995). "Cocultures of Meningeal and Astrocytic Cells- A Mode for the Formation of the Glial-Limiting Membrane". Int. J. Devl Neuroscience. 13.6 (6): 595–606. doi:10.1016/0736-5748(95)00040-N.
↑ B. Castellano López; Bernardo Castellano; Manuel Nieto-Sampedro (15 September 2003). Glial cell function. Gulf Professional Publishing. p. 18. ISBN 978-0-444-51486-8 . Retrieved 25 March 2011.
↑ Mathias Bähr (2006). Brain repair. Gulf Professional Publishing. p. 19. ISBN 978-0-306-47859-8 . Retrieved 25 March 2011.
↑ Saito Y, Murayama S, Kawai M, Nakano I (October 1999). "Breached cerebral glia limitans-basal lamina complex in Fukuyama-type congenital muscular dystrophy". Acta Neuropathol. 98 (4): 330–6. doi:10.1007/s004010051089. PMID 10502035.
↑ Nakano, Imaharu; Funahashi, M; Takada, K; Toda, T (1996). "Are breaches in the glia limitans the primary cause of the micropolygyria in Fukuyama-type congenital muscular dystrophy (FCMD)? - Pathological study of the cerebral cortex of an FCMD fetus". Acta Neuropathologica. 91 (3): 313–321. doi:10.1007/s004010050431. PMID 8834545.
↑ Ennio Pannese (1994). Neurocytology: fine structure of neurons, nerve processes, and neuroglial cells. Thieme. pp. 173–175. ISBN 978-0-86577-456-8 . Retrieved 25 March 2011.
↑ Fields, Douglas; Stevens-Graham, B (2002). "New Insights into Neuron-Glia Communication". Science. 298 (5593): 556–562. Bibcode:2002Sci...298..556F. doi:10.1126/science.298.5593.556. PMC 1226318 . PMID 12386325.

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[KettenmannRansom2005-1] 1 2 Helmut Kettenmann; Bruce R. Ransom (2005). Neuroglia. Oxford University Press US. pp. 303–305. ISBN 978-0-19-515222-7 . Retrieved 20 March 2011.

[Saladin-2] Saladin, Kenneth S. (2011). Human Anatomy. p. 358. ISBN 9780071222075.

[pmcid3039833-3] 1 2 Engelhardt B, Coisne C (2011). "Fluids and barriers of the CNS establish immune privilege by confining immune surveillance to a two-walled castle moat surrounding the CNS castle". Fluids Barriers CNS. 8 (1): 4. doi:10.1186/2045-8118-8-4. PMC 3039833 . PMID 21349152.

[VerkhratskiǐButt2007-4] Alekseǐ Nestorovich Verkhratskiǐ; Arthur Butt (2007). Glial neurobiology: a textbook. John Wiley and Sons. p. 24. ISBN 978-0-470-01564-3 . Retrieved 20 March 2011.

[PetersPalay1991-5] Alan Peters; Sanford L. Palay; Henry deF. Webster (1991). The fine structure of the nervous system: neurons and their supporting cells. Oxford University Press. pp. 292–293. ISBN 978-0-19-506571-8 . Retrieved 25 March 2011.

[Implication-6] 1 2 Brightman, Milton (1991). "Implication of Astroglia in the Blood–Brain Barrier". In Abbot, N.J. (ed.). Glial-Neuronal Interaction. New York Academy of Sciences. p. 633. ISBN 0-89766-680-1.

[7] Struckhoff, Gernot (1995). "Cocultures of Meningeal and Astrocytic Cells- A Mode for the Formation of the Glial-Limiting Membrane". Int. J. Devl Neuroscience. 13.6 (6): 595–606. doi:10.1016/0736-5748(95)00040-N.

[LópezCastellano2003-8] B. Castellano López; Bernardo Castellano; Manuel Nieto-Sampedro (15 September 2003). Glial cell function. Gulf Professional Publishing. p. 18. ISBN 978-0-444-51486-8 . Retrieved 25 March 2011.

[Bähr2006-9] Mathias Bähr (2006). Brain repair. Gulf Professional Publishing. p. 19. ISBN 978-0-306-47859-8 . Retrieved 25 March 2011.

[10] Saito Y, Murayama S, Kawai M, Nakano I (October 1999). "Breached cerebral glia limitans-basal lamina complex in Fukuyama-type congenital muscular dystrophy". Acta Neuropathol. 98 (4): 330–6. doi:10.1007/s004010051089. PMID 10502035.

[11] Nakano, Imaharu; Funahashi, M; Takada, K; Toda, T (1996). "Are breaches in the glia limitans the primary cause of the micropolygyria in Fukuyama-type congenital muscular dystrophy (FCMD)? - Pathological study of the cerebral cortex of an FCMD fetus". Acta Neuropathologica. 91 (3): 313–321. doi:10.1007/s004010050431. PMID 8834545.

[Pannese1994-12] Ennio Pannese (1994). Neurocytology: fine structure of neurons, nerve processes, and neuroglial cells. Thieme. pp. 173–175. ISBN 978-0-86577-456-8 . Retrieved 25 March 2011.

[13] Fields, Douglas; Stevens-Graham, B (2002). "New Insights into Neuron-Glia Communication". Science. 298 (5593): 556–562. Bibcode:2002Sci...298..556F. doi:10.1126/science.298.5593.556. PMC 1226318 . PMID 12386325.

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