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Volume regulation of the brain tissue—a survey

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Summary

Though the brain bulk has been considered to be constant in several pressure homeostasis studies, the central nervous tissue may be responsible for the accommodation of extracerebral masses exceeding the volume regulation capacity of the cerebral blood and cerebrospinal fluid. Volume buffering of the nervous tissue may even be functioning in parallel, in conjunction with the “fluid” compartments. Of the existing volume regulatory models, the following are discussed:osmotic feedback (buffering) preventing major fluid shifts in osmotic or pressure disequilibrium at the blood brain barrier (BBB), and the4-compartment model, which under steady-state conditions can be regarded as an analogue of systemic tissue volume regulation, i.e. secretion of fluid at the BBB, bulk flow of interstitial space fluid (ISF) in the brain and absorption via the cerebrospinal fluid (CSF). The most recent data are presented, confirming that accommodation of space occupation by the nervous tissue is achieved via shrinkage of the extracerebral fluid (ECF), while the cell volume remains relatively constant. These findings confirm Hakim's classical hypothesis, based on biomechanical considerations, that the brain behaves like a sponge.

The data presented in this survey point to a more general hypothesis: the brain interstitial space can vary in volume according to physiological and pathological stress, within certain bounds this being a reversible process which does not affect brain function.

The potential role of the central neuro-endocrine system in brain volume regulation is discussed. Vasopressin (AVP) and atriopeptin (ANP) probably, function within the brain via a paracrine mechanism, as physiological regulators of brain cell and ISF volume. AVP and ANP are released in the central nervous system (CNS) independently from the periphery, and influence tissue water conservation and release directly. The future role of peptide analogues in the treatment of raised intracranial pressure and brain oedema are considered.

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References

  1. Abboud FM (1981) Special characteristics of the cerebral circulation. Federation Proc 40: 2296–2300

    Google Scholar 

  2. Agnati LF, Fuxe K, Zoli M, Zini I, Toffano G, Ferguti F (1986) A correlation analysis of the regional distribution of central encephalin and β-endorphin immunoreactive terminals and of opiate receptor in adult and old male rats. Evidence of the existence of two main types of communication in the central nervous system: the volume transmission and the wiring transmission. Acta Physiol Scand 128: 201–207

    PubMed  Google Scholar 

  3. Avezaat CJJ, van Eijdhoven JHM (1984) Cerebrospinal fluid pulse pressure and craniospinal dynamics. Jongbloed en Zoon, The Hague

    Google Scholar 

  4. Barzó P, Dóczi T, Csete K, Büza Z, Bodosi M (1991) Measurements of regional cerebral blood flow and blood flow velocity in experimental intracranial hypertension: infusion via the cisterna magna in rabbits. Neurosurgery 28: 821–825

    Google Scholar 

  5. Barzó P, Bari F, Dóczi T, Jancsó G, Bodosi M (1992) Significance of the rate of systemic blood pressure changes (mm of Mercury/sec) on short term autoregulatory response in normotensive and spontaneously hypertensive rats. Neurosurgery (submitted)

  6. Beaumont K, Tan PK (1990) Effects of atrial and brain natriuretic peptides upon cyclic GMP levels, potassium transport, and receptor binding in rat astrocytes. J Neurosci Res 25: 256–262

    PubMed  Google Scholar 

  7. Bradbury MWB (1979) The concept of a blood-brain barrier. Wiley, New York

    Google Scholar 

  8. Brownfield MS, Kozlowski GP (1977) The hypothalamochoroidal tract. Cell Tissue Res 178: 111–127

    PubMed  Google Scholar 

  9. Buijs RM, Swaab DF, Dogterom J, Van Leeuwen FW (1978) Intra- and extrahypothalamic vasopressin and oxytocin pathways in the cat. Cell Tissue Res 186: 423–433

    PubMed  Google Scholar 

  10. Changeux JP (1991) Concluding remarks. In: Fuxe K, Agnati LF (eds) Volume transmission in the brain: novel mechanisms for neural transmission. Raven, New York, pp 569–585

    Google Scholar 

  11. Cserr HF, DePasquale M, Patlak CS, Pullen RGL (1989) Convection of cerebral interstitial fluid and its role in brain volume regulation. Ann NY Acad Sci 481: 123–134

    Google Scholar 

  12. Cserr HF, DePasquale M, Nicholson C, Patlak CS, Pettigrew KD, Rice ME (1991) Extracellular volume decreases while cell volume is maintained by ion uptake in rat brain during acute hypernatraemia. J Physiol 442: 277–295

    PubMed  Google Scholar 

  13. Cserr HF, Patlak CS (1991) Regulation of brain volume under isosmotic and anisosmotic conditions. In: Gilles R (ed) Advances in comparative and environmental physiology, Vol 9. Springer, Berlin Heidelberg New York Tokyo, pp 62–80

    Google Scholar 

  14. Cserr HF, Latzkovits L (1992) A role for centrally-released vasopressin in brain ion and volume regulation: a hypothesis. Prog Brain Res 91: 1–6

    PubMed  Google Scholar 

  15. Del Bigio MR, Fedoroff S (1990) Swelling of astroglia in vitro and the effect of arginine vasopressin and atrial natriuretic peptide, Acta Neurochir [Suppl] (Wien) 51: 14–16

    Google Scholar 

  16. DePasquale M, Patlak CS, Cserr HF (1989) Brain ion and volume regulation during acute hypernatraemia in Brattleboro rats. Am J Physiol 256: F 1059-F 1066

    Google Scholar 

  17. Deyo SN, Shoemaker A, Ettenberg A, Bloom FE, Koob GF (1986) Subcutaneous administration of behaviourally effective doses of AVP change brain AVP content only in median eminence. Neuroendocrinology 42: 260–266

    PubMed  Google Scholar 

  18. Dóczi T, Szerdahelyi P, Gulya K, Kiss J (1982) Brain water accumulation after the central administration of vasopressin. Neurosurgery 11: 402–407

    PubMed  Google Scholar 

  19. Dóczi T, László FA, Szerdahelyi P, Joó F (1984) The role of vasopressin in brain oedema formation: further evidence obtained from the Brattleboro diabetes insipidus rat with subarachnoid haemorrhage. Neurosurgery 14: 436–440

    PubMed  Google Scholar 

  20. Dóczi T, Szerdahelyi P, Joó F (1984) 5-Hydroxytryptamine, injected intraventricularly, failed to increase brain water content. Neurosurgery 15: 165–169

    PubMed  Google Scholar 

  21. Dóczi T, Szerdahelyi P, Joó F, Bodosi M (1987) The effects of intraventricularly injected iso-osmolar glycerol on the brain water and electrolyte contents in rats. Neurosurgery 21: 182–185

    PubMed  Google Scholar 

  22. Dóczi T, Joó F, Szerdahelyi P, Bodosi M (1987) Regulation of brain water and electrolyte contents: the possible involvement of central atrial natriuretic factor (ANF). Neurosurgery 21: 454–458

    PubMed  Google Scholar 

  23. Dóczi T, Joó F, Szerdahelyi P, Bodosi M (1988) Regulation of brain water and electrolyte contents: the opposite actions of central vasopressin and atrial natriuretic factor (ANF). Acta Neurochir [Suppl] (Wien) 43: 186–188

    Google Scholar 

  24. Dóczi T, Joó F, Vecsernyés M, Bodosi M (1988) Increased concentration of atrial natriuretic factor in the cerebrospinal fluid of patients with aneurysmal subarachnoid haemorrhage and raised intracranial pressure. Neurosurgery 23: 16–19

    PubMed  Google Scholar 

  25. Dóczi T, Bodosi M (1989) The central neuroendocrine regulation of brain water and electrolytes, and resorption of cerebrospinal fluid (CSF). In: Gjerris F, Borgesen SE, Soelberg Sorensen P (eds) Outflow of cerebrospinal fluid. Alfred Benzon Symposium 27, Munksgaard, Copenhagen, pp 282–292

    Google Scholar 

  26. Dóczi T, Joó F, Bodosi M (1990) Central neuroendocrine control of the brain water, electrolyte and volume homeostasis. Acta Neurochir [Suppl] (Wien) 47: 122–126

    Google Scholar 

  27. Dytko G, Kintner LB (1986) Prevention of hyponatraemia in experimental Schwartz-Bartter syndrome with the vasopressin antagonist SK & F 101926. In: Cserr HF (ed) The neuronal microenvironment. Ann NY Acad Sci 481: 369–371

  28. Editorial (1991) Welcome to ouabain — a new steroid hormone. Lancet 338: 543–544

    Google Scholar 

  29. Fenstermacher JD, Rapoport SI (1984) Blood-brain barrier. In: Renkin EM, Michel CC (eds) Handbook of physiology. Sect. 2: The cardiovascular system. Am Phys Soc Bethesda, pp 969–1000

    Google Scholar 

  30. Fenstermacher JD (1984) Volume regulation of the central nervous system. In: Staub NC, Taylor AE (eds) Oedema. Raven, New York, pp 383–404

    Google Scholar 

  31. Flemming IFR, Sheppard RH, Turner V (1972) CSF scanning in the evaluation of hydrocephalus. In: Harbert JC, McCullough DC, Luessenhop AJ, DiChiro G (eds) Cisternography and hydrocephalus. Thomas, Springfield, Illinois, pp 261–284

    Google Scholar 

  32. Gardner DG, Vlasuk GP, Baxter JD, Fiddes A, Lewicki JA (1987) Identification of atrial natriuretic factor gene transcripts in the central nervous system of the rat. Proc Natl Acad Sci USA 84: 2175–2179

    PubMed  Google Scholar 

  33. Grubb RL, Raichle ME (1981) Intraventricular angiotensin II increases brain vascular permeability. Brain Res 210: 426–430

    PubMed  Google Scholar 

  34. Haddy FJ (1987) Endogenous digitalis-like factor or factors. N Engl J Med 316: 621–623

    PubMed  Google Scholar 

  35. Hakim S, Venegas JG, Burton JD (1976) The physics of the cranial cavity, hydrocephalus, and normal pressure hydrocephalus: mechanical interpretation and mathematical model. Surg Neurol 5: 187–210

    PubMed  Google Scholar 

  36. Holliday MA, Kakayci MN, Harrah J (1968) Factors that limit brain volume changes in response to acute hyper- and hyponatraemia. J Clin Invest 47: 1916–1922

    PubMed  Google Scholar 

  37. Heistad DD, Kontos HA (1983) Cerebral circulation. In: Shepherd JI, Abbound FM, Geiger SR (eds) Handbook of physiology. Sect. 2: The cardiovascular system. Am Phys Soc Bethesda, pp 137–183

    Google Scholar 

  38. Herkenham M (1991) Mismatches between neurotransmitter and receptor localisations: implications for endocrine functions in brain. In: Fuxe K, Agnati LF (eds) Volume transmission in the brain: novel mechanisms for neural transmission. Raven, New York, pp 63–87

    Google Scholar 

  39. Ibaragi M, Niwa M, Ozaki M (1989) Atrial natriuretic peptide modulates amiloride-sensitive Na-transport across the bloodbrain barrier. J Neurochem 53: 1802–1806

    PubMed  Google Scholar 

  40. Johnston H, Rowan JO, Park DM, Rennie MJ (1975) Raised intracranial pressure and cerebral blood flow. 5. Effects of episodic intracranial pressure waves in primates. J Neurol Neurosurg Psychiatry 38: 1076–1082

    PubMed  Google Scholar 

  41. Katzman R, Schimmel H (1969) Water movement. In: Lajtha A (ed) Handbook of neurochemistry, Vol 2. Plenum, New York, pp 11–22

    Google Scholar 

  42. Kuncz Á, Dóczi T, Bodosi M (1990) The effect of skull and dura on brain volume regulation after hypo- and hyperosmolar fluid treatment. Neurosurgery 27: 509–515

    PubMed  Google Scholar 

  43. Löfgren J, von Essen C, Zwetnow N (1973) The pressure volume curve of the cerebrospinal fluid space in dogs. Acta Neurol Scand 49: 557–574

    PubMed  Google Scholar 

  44. Marmarou A (1973) A theoretical and experimental evaluation of the cerebrospinal fluid system. PhD Thesis, Drexel University

  45. McGeer PE, Eccles JC, McGeer EG (1986) Molecular neurobiology of the mammalian brain. Plenum, New York

    Google Scholar 

  46. Miller JD, Stanek AE, Langfitt TW (1973) Cerebral blood flow regulation during experimental brain compression. J Neurosurg 39: 186–196

    Google Scholar 

  47. Nag S (1991) Effect of atrial natriuretic peptide on permeability of the blood-cerebrospinal fluid barrier. Acta Neuropathol (Berl) 82: 274–279

    Google Scholar 

  48. Nagy Z, Pappius HM, Mathieson G, Hüttner I (1979) Opening of tight junctions in cerebral endothelium. J Comp Neurol 185: 569–578

    PubMed  Google Scholar 

  49. Nakao N, Itakura T, Yokote H, Nakai K, Komai N (1990) Effect of atrial natriuretic peptide on ischaemic oedema. Changes in brain water and electrolytes. Neurosurgery 27: 39–44

    PubMed  Google Scholar 

  50. Naruse S, Aoki Y, Takei R, Horikawa Y, Ueda R (1991) Effects of atrial natriuretic peptide on ischaemic brain oedema in rats evaluated by proton magnetic resonance method. Stroke 22: 61–65

    PubMed  Google Scholar 

  51. Nicholson C, Rice ME (1991) Diffusion of ions and transmitters in the brain cell microenvironment. In: Fuxe K, Agnati LF (eds) Volume transmission in the brain: novel mechanisms for neural transmission. Raven, New York, pp 279–294

    Google Scholar 

  52. Niwa M, Ibaragi M, Tsutsumi K, Kurihara M, Himeno A, Mori K, Ozaki M (1988) Specific ANP binding sites in rat cerebral capillaries. Neurosci Lett 91: 89–94

    PubMed  Google Scholar 

  53. Needleman P (1986) The expanding physiological roles of atrial natriuretic factor. Nature 321: 199–200

    PubMed  Google Scholar 

  54. Paraicz E (ed) (1982) ICP in infancy and childhood. Karger, Basel

    Google Scholar 

  55. Pásztor E, Symon L, Drosch NWC, Branston NM (1973) The hydrogen clearance method in assessment of blood flow in cortex, white matter, and deep nuclei of baboons. Stroke 4: 556–567

    PubMed  Google Scholar 

  56. Pichon Y, Treherne JE (1976) Effect of osmotic stress on the electrical properties of the axons of a marine osmoconformer. J Exp Biol 65: 553–563

    PubMed  Google Scholar 

  57. Pollock AS, Arieff AJ (1980) Abnormalities of cell volume regulation and their functional consequences. Am J Physiol 239: F195-F205

    PubMed  Google Scholar 

  58. Prior DJ, Pierce SK (1981) Adaptation and tolerance of invertebrate nervous system to osmotic stress. J Exp Zool 215: 237–245

    Google Scholar 

  59. Raichle ME (1981) Hypothesis: a central neuroendocrine system regulates brain ion homeostasis and volume. In: Martin JB, Reichlin S, Bick KL (eds) Neurosecretion and brain peptides. Raven, New York, pp 329–336

    Google Scholar 

  60. Raichle ME, Grubb RL (1978) Regulation of brain water permeability by centrally released vasopressin. Brain Res 143: 191–194

    PubMed  Google Scholar 

  61. Reeder R, Nattie E, North W (1986) Effect of vasopressin on cold induced brain oedema. J Neurosurg 64: 941–950

    PubMed  Google Scholar 

  62. 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 a rapid distribution of tracer protein throughout the brain from subarachnoid space. Brain Res 326: 47–63

    PubMed  Google Scholar 

  63. Rodriguez EM (1976) The cerebrospinal fluid as a pathway in the neuroendocrine integration. J Endocrinol 71: 407–443

    PubMed  Google Scholar 

  64. Rosenberg AG, Kyner WT, Fenstermacher JD, Patlak CS (1986) Effects of vasopressin on ependymal and capillary permeability to tritiated water in cat. Am J Physiol 251: F485-F489

    PubMed  Google Scholar 

  65. Rosenberg AG, Estrada E, Kyner WT (1990) Vasopressin-induced brain oedema is mediated by the V1 receptor. Adv Neurol 52: 149–154

    PubMed  Google Scholar 

  66. Samson WK (1988) Central nervous system actions of atrial natriuretic factor. Brain Res Bull 20: 831–837

    PubMed  Google Scholar 

  67. Shapiro K, Takei F, Fried A, Kohn I (1985) Experimental feline hydrocephalus: the role of biomechanical changes in ventricular enlargement in cats. J Neurosurg 63: 82–87

    PubMed  Google Scholar 

  68. Steardo L, Nathanson JA (1987) Brain barrier tissues: end organs for atriopeptins. Science 235: 470–473

    PubMed  Google Scholar 

  69. Sudoh T, Kangawa K, Minamino M, Matsuo H (1988) Identification in porcine brain of a novel natriuretic peptide distinct from atrial natriuretic peptide. Nature (London) 332: 78–81

    Google Scholar 

  70. Tutsumi K, Niwa M, Himeno A, Kurihara M, Kawano T, Ibaragi M, Ozaki M, Mori K (1988) Alpha-atrial natriuretic peptide binding sites in the rat choroid plexus are increased in the presence of hydrocephalus. Neurosci Lett 87: 93–98

    PubMed  Google Scholar 

  71. Van Leeuwen FW (1987) Vasopressin receptors in the brain and pituitary. In: Gash DM, Boer GJ (eds) Vasopressin, principles, and properties. Plenum, New York, pp 477–496

    Google Scholar 

  72. Weinand M, O'Boynick P, Overman J (1987) The effect of central antidiuretic hormone (ADH) inhibition on vasogenic brain oedema. In: Proc 37th Congr Neurol Surg, Baltimore, MD, p 90

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Supported by Grants “OTKA I/3 2728” and “ETT T110/1990”.

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Dóczi, T. Volume regulation of the brain tissue—a survey. Acta neurochir 121, 1–8 (1993). https://doi.org/10.1007/BF01405174

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