Abstract
There is evidence for lymphatic drainage of interstitial fluid from the brain along perivascular spaces in a number of mammalian species. Ultrastructural studies suggest that there are similar drainage pathways in the human cerebral cortex. Perivascular spaces in the basal ganglia, however, differ from those in the cortex in that they dilate to form lacunes and rarely accumulate beta-amyloid (amyloid angiopathy) in Alzheimer's disease; in the cortex, lacunes are rare but amyloid angiopathy is common. The aim of the present study is to compare the structure of perivascular spaces in the basal ganglia and at the anterior perforated substance with perivascular spaces in the cerebral cortex. Eight postmortem brains from patients aged 23–80 years (mean 68 y) were examined by light microscopy, by scanning and transmission electron microscopy and by direct visualisation of etched paraffin blocks. The results show that arteries in the basal ganglia are surrounded by 2 distinct coats of leptomeninges separated by a perivascular space which is continuous with the perivascular space around arteries in the subarachnoid space. The inner layer of leptomeninges closely invests the adventitia of the vessel wall and the outer layer is continuous with the pia mater on the surface of the brain at the anterior perforated substance. Veins in the basal ganglia have no outer layer of leptomeninges and thus the perivascular space is continuous with the subpial space. The anatomy of the periarterial spaces in the basal ganglia differs significantly from that in the cerebral cortex where there is only a single periarterial layer of leptomeninges. Differences in structure of perivascular spaces around arteries may reflect relative efficiencies in the drainage of interstitial fluid from different sites in the brain. Futhermore, the structure of the perivascular spaces may contribute to the relatively high frequency of lacunes in the basal ganglia, and the low frequency of amyloid angiopathy at this site in Alzheimer's disease.
Keywords: Vasculature, leptomeninges, interstitial fluid drainage, Alzheimer's disease
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- Alcolado R., Weller R. O., Parrish E. P., Garrod D. The cranial arachnoid and pia mater in man: anatomical and ultrastructural observations. Neuropathol Appl Neurobiol. 1988 Jan-Feb;14(1):1–17. doi: 10.1111/j.1365-2990.1988.tb00862.x. [DOI] [PubMed] [Google Scholar]
- Benhaïem-Sigaux N., Gray F., Gherardi R., Roucayrol A. M., Poirier J. Expanding cerebellar lacunes due to dilatation of the perivascular space associated with Binswanger's subcortical arteriosclerotic encephalopathy. Stroke. 1987 Nov-Dec;18(6):1087–1092. doi: 10.1161/01.str.18.6.1087. [DOI] [PubMed] [Google Scholar]
- Braak H., Braak E. Alzheimer's disease: striatal amyloid deposits and neurofibrillary changes. J Neuropathol Exp Neurol. 1990 May;49(3):215–224. [PubMed] [Google Scholar]
- Cserr H. F., Harling-Berg C. J., Knopf P. M. Drainage of brain extracellular fluid into blood and deep cervical lymph and its immunological significance. Brain Pathol. 1992 Oct;2(4):269–276. doi: 10.1111/j.1750-3639.1992.tb00703.x. [DOI] [PubMed] [Google Scholar]
- Feurer D. J., Weller R. O. Barrier functions of the leptomeninges: a study of normal meninges and meningiomas in tissue culture. Neuropathol Appl Neurobiol. 1991 Oct;17(5):391–405. doi: 10.1111/j.1365-2990.1991.tb00739.x. [DOI] [PubMed] [Google Scholar]
- González Cámpora R., Otal Salaverri C., Vázquez Ramirez F., Salguero Villadiego M., Galera Davidson H. Metastatic glioblastoma multiforme in cervical lymph nodes. Report of a case with diagnosis by fine needle aspiration. Acta Cytol. 1993 Nov-Dec;37(6):938–942. [PubMed] [Google Scholar]
- Harling-Berg C., Knopf P. M., Merriam J., Cserr H. F. Role of cervical lymph nodes in the systemic humoral immune response to human serum albumin microinfused into rat cerebrospinal fluid. J Neuroimmunol. 1989 Dec;25(2-3):185–193. doi: 10.1016/0165-5728(89)90136-7. [DOI] [PubMed] [Google Scholar]
- Hunter J. V., Batchelder K. F., Lo E. H., Wolf G. L. Imaging techniques for in vivo quantitation of extracranial lymphatic drainage of the brain. Neuropathol Appl Neurobiol. 1995 Jun;21(3):185–188. doi: 10.1111/j.1365-2990.1995.tb01049.x. [DOI] [PubMed] [Google Scholar]
- Hutchings M., Weller R. O. Anatomical relationships of the pia mater to cerebral blood vessels in man. J Neurosurg. 1986 Sep;65(3):316–325. doi: 10.3171/jns.1986.65.3.0316. [DOI] [PubMed] [Google Scholar]
- Kida S., Pantazis A., Weller R. O. CSF drains directly from the subarachnoid space into nasal lymphatics in the rat. Anatomy, histology and immunological significance. Neuropathol Appl Neurobiol. 1993 Dec;19(6):480–488. doi: 10.1111/j.1365-2990.1993.tb00476.x. [DOI] [PubMed] [Google Scholar]
- Kida S., Steart P. V., Zhang E. T., Weller R. O. Perivascular cells act as scavengers in the cerebral perivascular spaces and remain distinct from pericytes, microglia and macrophages. Acta Neuropathol. 1993;85(6):646–652. doi: 10.1007/BF00334675. [DOI] [PubMed] [Google Scholar]
- Kida S., Weller R. O., Zhang E. T., Phillips M. J., Iannotti F. Anatomical pathways for lymphatic drainage of the brain and their pathological significance. Neuropathol Appl Neurobiol. 1995 Jun;21(3):181–184. doi: 10.1111/j.1365-2990.1995.tb01048.x. [DOI] [PubMed] [Google Scholar]
- Knopf P. M., Cserr H. F., Nolan S. C., Wu T. Y., Harling-Berg C. J. Physiology and immunology of lymphatic drainage of interstitial and cerebrospinal fluid from the brain. Neuropathol Appl Neurobiol. 1995 Jun;21(3):175–180. doi: 10.1111/j.1365-2990.1995.tb01047.x. [DOI] [PubMed] [Google Scholar]
- Krahn V. The pia mater at the site of the entry of blood vessels into the central nervous system. Anat Embryol (Berl) 1982;164(2):257–263. doi: 10.1007/BF00318509. [DOI] [PubMed] [Google Scholar]
- Mandybur T. I. The incidence of cerebral amyloid angiopathy in Alzheimer's disease. Neurology. 1975 Feb;25(2):120–126. doi: 10.1212/wnl.25.2.120. [DOI] [PubMed] [Google Scholar]
- Nicholas D. S., Weller R. O. The fine anatomy of the human spinal meninges. A light and scanning electron microscopy study. J Neurosurg. 1988 Aug;69(2):276–282. doi: 10.3171/jns.1988.69.2.0276. [DOI] [PubMed] [Google Scholar]
- Phillips M. J., Weller R. O., Kida S., Iannotti F. Focal brain damage enhances experimental allergic encephalomyelitis in brain and spinal cord. Neuropathol Appl Neurobiol. 1995 Jun;21(3):189–200. doi: 10.1111/j.1365-2990.1995.tb01050.x. [DOI] [PubMed] [Google Scholar]
- Poirier J., Derouesné C. Le concept de lacune cérébrale de 1838 à nos jours. Rev Neurol (Paris) 1985;141(1):3–17. [PubMed] [Google Scholar]
- Weller R. O., Engelhardt B., Phillips M. J. Lymphocyte targeting of the central nervous system: a review of afferent and efferent CNS-immune pathways. Brain Pathol. 1996 Jul;6(3):275–288. doi: 10.1111/j.1750-3639.1996.tb00855.x. [DOI] [PubMed] [Google Scholar]
- Weller R. O., Kida S., Zhang E. T. Pathways of fluid drainage from the brain--morphological aspects and immunological significance in rat and man. Brain Pathol. 1992 Oct;2(4):277–284. doi: 10.1111/j.1750-3639.1992.tb00704.x. [DOI] [PubMed] [Google Scholar]
- Yamaguchi H., Yamazaki T., Lemere C. A., Frosch M. P., Selkoe D. J. Beta amyloid is focally deposited within the outer basement membrane in the amyloid angiopathy of Alzheimer's disease. An immunoelectron microscopic study. Am J Pathol. 1992 Jul;141(1):249–259. [PMC free article] [PubMed] [Google Scholar]
- Zhang E. T., Inman C. B., Weller R. O. Interrelationships of the pia mater and the perivascular (Virchow-Robin) spaces in the human cerebrum. J Anat. 1990 Jun;170:111–123. [PMC free article] [PubMed] [Google Scholar]
- Zhang E. T., Richards H. K., Kida S., Weller R. O. Directional and compartmentalised drainage of interstitial fluid and cerebrospinal fluid from the rat brain. Acta Neuropathol. 1992;83(3):233–239. doi: 10.1007/BF00296784. [DOI] [PubMed] [Google Scholar]