Anatomical relationships of the pia mater to cerebral blood vessels in man

Margaret Hutchings B.M. 1 and Roy O. Weller M.D., Ph.D., F.R.C.Path. 1
View More View Less
  • 1 Department of Neuropathology, University of Southampton, Southampton, England
Restricted access

Purchase Now

USD  $45.00

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00
Print or Print + Online

✓ Using scanning and transmission electron microscopy and light microscopy, the authors studied the human pia mater and its relationship to the entry of blood vessels into the normal cerebral cortex. The purpose of this investigation was to examine the long-established concept that the subarachnoid space communicates directly with the perivascular spaces of the cerebral cortex. Brains obtained post mortem from subjects with recent subarachnoid hemorrhage (SAH) and purulent leptomeningitis were studied by light microscopy to determine the permeability of the pia mater to red blood cells and inflammatory cells. Scanning electron microscopy showed that the normal pia mater is a flat sheet of cells that is reflected from the surface of the brain to form the outer coating of the meningeal vessels in the subarachnoid space. Transmission electron microscopy confirmed that the cells of the pia mater are joined by junctional complexes and form a continuous sheet that separates the subarachnoid space on one side from the subpial and perivascular spaces on the other. Thus, neither the pia mater nor the subarachnoid space extends into the brain beside blood vessels as they enter the cerebral cortex. The perivascular spaces were, in fact, found to be confluent with the subpial space and not with the subarachnoid space. In cases of recent SAH, red blood cells did not enter the perivascular spaces from the subarachnoid space; neither did India ink injected post mortem into the subarachnoid space pass into the perivascular spaces. The results of these crude tracer studies suggest that the pia mater is an effective barrier to the passage of particulate matter. Histological examination of brains of patients who had died with purulent leptomeningitis showed that inflammatory cells were present in the cortical perivascular spaces and in the contiguous subpial spaces. The presence of a large number of inflammatory cells in the subarachnoid space suggests that inflammatory cells readily penetrate the pia mater that separates the perivascular spaces from the subarachnoid space. The permeability of the pia mater to small molecular weight substances is briefly discussed.

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00

Contributor Notes

Address reprint requests to: Roy O. Weller, M.D., Department of Pathology (Neuropathology), Level E, South Laboratory and Pathology Block, Southampton General Hospital, Southampton SO9 4XY, England.
  • 1.

    Aird RB: A study of intrathecal, cerebrospinal fluid-to-brain exchange. Exp Neurol 86:342358, 1984 Aird RB: A study of intrathecal, cerebrospinal fluid-to-brain exchange. Exp Neurol 86:342–358, 1984

    • Search Google Scholar
    • Export Citation
  • 2.

    Arutiunov AI, , Baron MA, & Majorova NA: The role of mechanical factors in the pathogenesis of short-term and prolonged spasm of the cerebral arteries. J Neurosurg 40:459472, 1974 Arutiunov AI, Baron MA, Majorova NA: The role of mechanical factors in the pathogenesis of short-term and prolonged spasm of the cerebral arteries. J Neurosurg 40:459–472, 1974

    • Search Google Scholar
    • Export Citation
  • 3.

    Bradbury MWB: The Concept of a Blood-Brain Barrier. Chichester: John Wiley & Sons, 1979, p 19 Bradbury MWB: The Concept of a Blood-Brain Barrier. Chichester: John Wiley & Sons, 1979, p 19

    • Search Google Scholar
    • Export Citation
  • 4.

    Brandt L, , Ljunggren B, & Andersson KE, et al: Vasoconstrictive effects of human post-hemorrhagic cerebrospinal fluid on cat pial arterioles in situ. J Neurosurg 54:351356, 1981 Brandt L, Ljunggren B, Andersson KE, et al: Vasoconstrictive effects of human post-hemorrhagic cerebrospinal fluid on cat pial arterioles in situ. J Neurosurg 54:351–356, 1981

    • Search Google Scholar
    • Export Citation
  • 5.

    Cloyd MW, & Low FN: Scanning electron microscopy of the subarachnoid space in the dog. I. Spinal cord levels. J Comp Neurol 153:325368, 1974 Cloyd MW, Low FN: Scanning electron microscopy of the subarachnoid space in the dog. I. Spinal cord levels. J Comp Neurol 153:325–368, 1974

    • Search Google Scholar
    • Export Citation
  • 6.

    Fisher CM, , Roberson GH, & Ojemann RG: Cerebral vasospasm with ruptured saccular aneurysm — the clinical manifestations. Neurosurgery 1:245248, 1977 Fisher CM, Roberson GH, Ojemann RG: Cerebral vasospasm with ruptured saccular aneurysm — the clinical manifestations. Neurosurgery 1:245–248, 1977

    • Search Google Scholar
    • Export Citation
  • 7.

    Frederickson RG, & Low FN: Blood vessels and tissue space associated with the brain of the rat. Am J Anat 125:123146, 1969 Frederickson RG, Low FN: Blood vessels and tissue space associated with the brain of the rat. Am J Anat 125:123–146, 1969

    • Search Google Scholar
    • Export Citation
  • 8.

    Graham RC Jr, & Karnovsky MJ: The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique. J Histochem Cytochem 14:291302, 1966 Graham RC Jr, Karnovsky MJ: The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique. J Histochem Cytochem 14:291–302, 1966

    • Search Google Scholar
    • Export Citation
  • 9.

    Harriman DGF: Bacterial infections of the central nervous system, in Adams JH, , Corsellis JAN, & Duchen LW (eds): Greenfield's Neuropathology, ed 4. London: Edward Arnold, 1984, pp 236259 Harriman DGF: Bacterial infections of the central nervous system, in Adams JH, Corsellis JAN, Duchen LW (eds): Greenfield's Neuropathology, ed 4. London: Edward Arnold, 1984, pp 236–259

    • Search Google Scholar
    • Export Citation
  • 10.

    Jones EG: On the mode of entry of blood vessels into the cerebral cortex. J Anat 106:507520, 1970 Jones EG: On the mode of entry of blood vessels into the cerebral cortex. J Anat 106:507–520, 1970

    • Search Google Scholar
    • Export Citation
  • 11.

    Krahn V: Leukodiapedesis and leukocyte migration in the leptomeninges and in the subarachnoid space. J Neurol 226:4352, 1981 Krahn V: Leukodiapedesis and leukocyte migration in the leptomeninges and in the subarachnoid space. J Neurol 226:43–52, 1981

    • Search Google Scholar
    • Export Citation
  • 12.

    Krahn V: The pia mater at the site of entry of blood vessels into the central nervous system. Anat Embryol 164:257263, 1982 Krahn V: The pia mater at the site of entry of blood vessels into the central nervous system. Anat Embryol 164:257–263, 1982

    • Search Google Scholar
    • Export Citation
  • 13.

    Malloy JJ, & Low FN: Scanning electron microscopy of the subarachnoid space in the dog. IV. Subarachnoid macrophages. J Comp Neurol 167:257283, 1976 Malloy JJ, Low FN: Scanning electron microscopy of the subarachnoid space in the dog. IV. Subarachnoid macrophages. J Comp Neurol 167:257–283, 1976

    • Search Google Scholar
    • Export Citation
  • 14.

    Millen JW, & Woollam DHM: The reticular perivascular tissue of the central nervous system. J Neurol Neurosurg Psychiatry 17:286294, 1954 Millen JW, Woollam DHM: The reticular perivascular tissue of the central nervous system. J Neurol Neurosurg Psychiatry 17:286–294, 1954

    • Search Google Scholar
    • Export Citation
  • 15.

    Morse DE, & Low FN: The fine structure of the pia mater of the rat. Am J Anat 133:349368, 1972 Morse DE, Low FN: The fine structure of the pia mater of the rat. Am J Anat 133:349–368, 1972

    • Search Google Scholar
    • Export Citation
  • 16.

    Nelson E, , Blinzinger K, & Hager H: Electron microscopic observations on subarachnoid and perivascular spaces of the Syrian hamster brain. Neurology 11:285295, 1961 Nelson E, Blinzinger K, Hager H: Electron microscopic observations on subarachnoid and perivascular spaces of the Syrian hamster brain. Neurology 11:285–295, 1961

    • Search Google Scholar
    • Export Citation
  • 17.

    Oda Y, & Nakanishi I: Ultrastructure of the mouse leptomeninx. J Comp Neurol 225:448457, 1984 Oda Y, Nakanishi I: Ultrastructure of the mouse leptomeninx. J Comp Neurol 225:448–457, 1984

    • Search Google Scholar
    • Export Citation
  • 18.

    Peters A, , Palay SL, & Webster HdeF: The Fine Structure of the Nervous System: The Neurons and Supporting Cells. Philadelphia: WB Saunders, 1976, pp 338340 Peters A, Palay SL, Webster HdeF: The Fine Structure of the Nervous System: The Neurons and Supporting Cells. Philadelphia: WB Saunders, 1976, pp 338–340

    • Search Google Scholar
    • Export Citation
  • 19.

    Ramsey HJ: Fine structure of the surface of the cerebral cortex of human brain. J Cell Biol 26:323333, 1965 Ramsey HJ: Fine structure of the surface of the cerebral cortex of human brain. J Cell Biol 26:323–333, 1965

    • Search Google Scholar
    • Export Citation
  • 20.

    Rennels ML, , Gregory TF, & Blaumanis OR, et al: Evidence for a “paravascular” fluid circulation in the mammalian central nervous system, provided by the rapid distribution of tracer protein throughout the brain from the subarachnoid space. Brain Res 326:4763, 1985 Rennels ML, Gregory TF, Blaumanis OR, et al: Evidence for a “paravascular” fluid circulation in the mammalian central nervous system, provided by the rapid distribution of tracer protein throughout the brain from the subarachnoid space. Brain Res 326:47–63, 1985

    • Search Google Scholar
    • Export Citation
  • 21.

    Sapsford I, , Buontempo J, & Weller RO: Basement membrane surfaces and perivascular compartments in normal human brain and glial tumours. A scanning electron microscope study. Neuropathol Appl Neurobiol 9:181194, 1983 Sapsford I, Buontempo J, Weller RO: Basement membrane surfaces and perivascular compartments in normal human brain and glial tumours. A scanning electron microscope study. Neuropathol Appl Neurobiol 9:181–194, 1983

    • Search Google Scholar
    • Export Citation
  • 22.

    Smith RR, , Clower BR, & Peeler DF Jr, et al: The angiopathy of subarachnoid hemorrhage: angiographic and morphological correlates. Stroke 14:240245, 1983 Smith RR, Clower BR, Peeler DF Jr, et al: The angiopathy of subarachnoid hemorrhage: angiographic and morphological correlates. Stroke 14:240–245, 1983

    • Search Google Scholar
    • Export Citation
  • 23.

    Torvik A, , Bhatia R, & Murthy VS: Transitory block of the arachnoid granulations following subarachnoid haemorrhage. A postmortem study. Acta Neurochir 41:137146, 1978 Torvik A, Bhatia R, Murthy VS: Transitory block of the arachnoid granulations following subarachnoid haemorrhage. A postmortem study. Acta Neurochir 41:137–146, 1978

    • Search Google Scholar
    • Export Citation
  • 24.

    Upton ML, & Weller RO: The morphology of cerebrospinal fluid drainage pathways in human arachnoid granulations. J Neurosurg 63:867875, 1985 Upton ML, Weller RO: The morphology of cerebrospinal fluid drainage pathways in human arachnoid granulations. J Neurosurg 63:867–875, 1985

    • Search Google Scholar
    • Export Citation
  • 25.

    Weed LH: The absorption of cerebrospinal fluid into the venous system. Am J Anat 31:191221, 1923 Weed LH: The absorption of cerebrospinal fluid into the venous system. Am J Anat 31:191–221, 1923

    • Search Google Scholar
    • Export Citation
  • 26.

    Weller RO: Spontaneous intracranial haemorrhage, in Adams JH, , Corsellis JAN, & Duchen LW (eds): Greenfield's Neuropathology, ed 4. London: Edward Arnold, 1984, pp 208235 Weller RO: Spontaneous intracranial haemorrhage, in Adams JH, Corsellis JAN, Duchen LW (eds): Greenfield's Neuropathology, ed 4. London: Edward Arnold, 1984, pp 208–235

    • Search Google Scholar
    • Export Citation
  • 27.

    Williams PL, & Warwick R (eds): Gray's Anatomy, ed 36. Edinburgh: Churchill Livingstone, 1980, pp 10511052 Williams PL, Warwick R (eds): Gray's Anatomy, ed 36. Edinburgh: Churchill Livingstone, 1980, pp 1051–1052

    • Search Google Scholar
    • Export Citation
  • 28.

    Woollam DHM, & Millen JW: Perivascular spaces of the mammalian central nervous system. Biol Rev 29:251283, 1954 Woollam DHM, Millen JW: Perivascular spaces of the mammalian central nervous system. Biol Rev 29:251–283, 1954

    • Search Google Scholar
    • Export Citation
  • 29.

    Woollam DHM, & Millen JW: The perivascular spaces of the mammalian central nervous system and their relation to the perineuronal and subarachnoid spaces. J Anat 89:193200, 1955 Woollam DHM, Millen JW: The perivascular spaces of the mammalian central nervous system and their relation to the perineuronal and subarachnoid spaces. J Anat 89:193–200, 1955

    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 1205 460 29
Full Text Views 399 71 3
PDF Downloads 300 43 3
EPUB Downloads 0 0 0