Skip to main content
Log in

Directional and compartmentalised drainage of interstitial fluid and cerebrospinal fluid from the rat brain

  • Regular Papers
  • Published:
Acta Neuropathologica Aims and scope Submit manuscript

Summary

Pathways for drainage of interstitial fluid and cerebrospinal fluid from the rat brain were investigated by the injection of 2–5 μl Indian ink into cerebral white and grey matter and into the subarachnoid space over the vertex of the left frontal lobe. Animals were killed by formalin or glutaraldehyde perfusion 5 min-2 years after injection, and the distribution of ink over the surface of the brain, in 2-mm slices of brain cleared in cedar wood oil, in paraffin sections and by electron microscopy was documented. These investigations showed that carbon particles were distributed diffusely through the interstitial spaces of the white matter whereas they spread selectively along perivascular spaces in the grey matter outlining both arteries and veins and extending to surround capillaries within 1 h. Carbon particles were rapidly ingested by perivascular cells and, to some extent, by meningeal cells surrounding the larger vessels. Very little movement of carbon-labelled perivascular cells and perivascular macrophages was seen after 2 years. Carbon particles entering the subarachnoid space over the vertex of the cerebral hemispheres drained along selected paravascular and subfrontal pathways in the subarachnoid space to the cribriform plate and thence into nasal lymphatics and cervical lymph nodes. These studies demonstrate the diffuse spread of fluidborne tracers through cerebral white matter in the rat, the perivascular spread of tracer in grey matter and the compartmentalised directional flow or tracer through the subarachnoid space to the cribriform plate and nasal lymphatics. Furthermore, particulate matter selectively injected into perivascular spaces in rat grey matter is rapidly and efficiently ingested by perivascular cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Alcolado R, Weller RO, Parrish EP, Garrod D (1988) The cranial arachnoid and pia mater in man: anatomical and ultrastructural observations. Neuropathol Appl Neurobiol 14:1–17

    Google Scholar 

  2. Bradbury MWB, Cserr HF, Westrop RJ (1981) Drainage of cerebral interstitial fluid into deep cervical lymph of the rabbit. Am J Physiol 240:F329-F336

    Google Scholar 

  3. Casley-Smith JR, Földi-Börcsök E, Földi M (1976) The prelymphatic pathways of the brain as revealed by cervical lymphatic obstruction and the passage of particles. Br J Exp Pathol 57:179–188

    Google Scholar 

  4. Clark RG, Milhorat TH (1970) Experimental hydrocephalus. III. Light microscopic findings in acute and subacute obstructive hydrocephalus in the monkey. J Neurosurg 32:400–413

    Google Scholar 

  5. Cross AH, Cannella B, Brosnan CF, Raine CS (1990) Homing to central nervous system vasculature by antigen-specific lymphocytes. I. Localization of 14C-labelled cells during acute, chronic, and relapsing experimental allergic encephalomyelitis. Lab Invest 63:162–170

    Google Scholar 

  6. Cserr HF, Ostrach LH (1974) Bulk flow of interstitial fluid after intracranial injection of Blue Dextran 2000. Exp Neurol 45:50–60

    Google Scholar 

  7. Cserr HF, Harling-Berg C, Ichimura T, Knopf PM, Yamada S (1990) Drainage of cerebral extracellular fluids into cervical lymph: an afferent limb in brain/immune system interactions. In: Johansson BB, Owman C, Widner H (eds) Pathophysiology of the blood-brain barrier. Elsevier Science Publishers (Biomedical Division), Amsterdam, pp 413–420

    Google Scholar 

  8. Erlich SS, McComb JG, Hyman S, Weiss MH (1986) Ultrastructural morphology of the olfactory pathway for cerebrospinal fluid drainage in the rabbit. J Neurosurg 64:466–473

    Google Scholar 

  9. Esiri MM, Gay D (1990) Immunological and neuropathological significance of the Virchow-Robin space. J Neurol Sci 100:3–8

    Google Scholar 

  10. Feuer D, Weller RO (1991) Barrier functions of the leptomeninges: a study of normal meninges and meningiomas in tissue culture. Neuropathol Appl Neurobiol 17:391–405

    Google Scholar 

  11. Graeber MB, Streit WJ, Kreutzberg GW (1989) Identity of ED2-positive perivascular cells in rat brain. J Neurosci Res 22:103–106

    Google Scholar 

  12. Graeber MB, Streit WJ, Kiefer R, Schoen SW, Kreutzberg GW (1990) New expression of myelomonocytic antigen by microglia and perivascular cells following lethal motor neuron injury. J Neuroimmunol 27:121–132

    Google Scholar 

  13. Harling-Berg C, Knopf PM, Merriam J, Cserr HF (1989) Role of cervical lymph nodes in the systemic humoral immune response to human serum albumin microinfused into rat cerebrospinal fluid. J Neuroimmunol 25:185–193

    Google Scholar 

  14. Hutchings M, Weller RO (1986) Anatomical relationships of the pia mater to cerebral blood vessels in man. J Neurosurg 65:316–325

    Google Scholar 

  15. Ichimura T, Fraser PA, Cserr HF (1991) Distribution of extracellular tracers in perivascular spaces of the rat brain. Brain Res 545:103–113

    Google Scholar 

  16. Kalimo H, Fredricksson K, Nordborg C, Auer RN, Olsson Y, Johansson B (1986) The spread of brain oedema in hypertensive brain injury. Med Biol 64:133–137

    Google Scholar 

  17. Krisch B, Leonhardt H, Oksche A (1984) Compartments and perivascular arrangement of the meninges covering the cerebral cortex of the rat. Cell Tissue Res 238:459–474

    Google Scholar 

  18. McComb JG, Hyman S, Weiss MH (1984) Lymphatic drainage of cerebrospinal fluid in cat. In: Shapiro K, Marmarou A, Portnoy H (eds) Hydrocephalus. Raven Press, New York, pp 83–98

    Google Scholar 

  19. McKeever PE, Balentine JD (1978) Macrophage migration through the brain parenchyma to the perivascular space following particle ingestion. Am J Pathol 93:153–164

    Google Scholar 

  20. Nicholas DS, Weller RO (1988) The fine anatomy of the human spinal meninges. A light and scanning electron microscopy study. J Neurosurg 69:276–282

    Google Scholar 

  21. Ohata K, Marmarou A, Povlishock JT (1990) An immunocytochemical study of protein clearance in brain infusion edema. Acta Neuropathol 81:162–177

    Google Scholar 

  22. Rennels ML, Gregory TF, Blaumanis OR, Fujimoto K, Grady PA (1985) 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

    Google Scholar 

  23. Streit WJ, Graeber MB, Kreutzberg GW (1989) Expression of Ia antigen on perivascular and microglial cells after sublethal and lethal motor neuron injury. Exp Neurol 105:115–126

    Google Scholar 

  24. Szentistvanyi I, Patlak CS, Ellis RA, Cserr HF (1984) Drainage of intertitial fluid from different regions of rat brain. Am J Physiol 246:F835-F844

    Google Scholar 

  25. Weller RO, Wisniewski H (1969) Histological and ultrastructural changes in experimental hydrocephalus. I. Adult Rabbit. Brain 92:819–828

    Google Scholar 

  26. Weller RO, Wisniewski H, Shulman K, Terry RD (1971) Experimental hydrocephalus in young dogs: histological and ultrastructural study of the brain tissue damage. J Neuropathol Exp Neurol 30:613–627

    Google Scholar 

  27. Weller RO, Shulman K (1972) Infantile hydrocephalus: clinical, histological and ultrastructural study of brain damage. J Neurosurg 36:255–265

    Google Scholar 

  28. Yamazumi H (1989) Infiltration of Indian ink from subarachnoid space to nasal mucosa along olfactory nerves in rabbits. Nippon Jibiinkoka Gakkai Kaiho 92:608–616

    Google Scholar 

  29. Zhang ET, Inman CBE, Weller RO (1990) Interrelationships of the pia mater and the perivascular (Virchow-Robin) spaces in the human cerebrum. J Anat 170:111–123

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

E. T. Z. supported by the James Gibson Fund, the Wessex Medical Trust, the Wessex Neurological Centre Research Trust, and the Sino-British Society

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, E.T., Richards, H.K., Kida, S. et al. Directional and compartmentalised drainage of interstitial fluid and cerebrospinal fluid from the rat brain. Acta Neuropathol 83, 233–239 (1992). https://doi.org/10.1007/BF00296784

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00296784

Key words

Navigation