Skip to main content

Advertisement

SpringerLink
Log in

Influence of electrical stimulation of locus coeruleus on the rat blood-brain barrier permeability to sodium fluorescein

  • Published:
Acta Neurochirurgica Aims and scope Submit manuscript

Summary

The role of central adrenergic innervation of the brain capillaries is still a matter of discussion. The hypothesis that these nerves control the blood-brain barrier permeability was tested by electrically stimulating the locus coeruleus, the major central adrenergic nucleus, in the anaesthetized rat. Frequencies of 5, 15, and 30 Hz were used. A frequency dependent increase in blood-brain barrier permeability to sodium fluorescein was verified. Prior administration of the α-adrenoceptor antagonist phenoxybenzamine (10 mg/kg i.p., 24 h before electrical stimulation) totally blocked the effect of 15 Hz stimulation. The same dose of pindolol (a β-adrenoceptor antagonist) given 1 h before electrical stimulation potentiated the effect of 5 Hz stimulation. Thus, blood-brain barrier permeability is increased, in a frequency dependent manner, by electrical stimulation of the locus coeruleus. The results obtained with phenoxybenzamine and pindolol suggest an opposite effect of α and β-adrenoceptors on the control of sodium fluorescein transport through the blood-brain barrier.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Baba H, Oishi R, Saeki K (1988) Enhancement of blood-brain barrier permeability to sodium fluorescein by stimulation of μ opioid receptors in mice. Naunyn-Schmiedebergs Arch Pharmacol 337: 423–428

    PubMed  Google Scholar 

  2. Bandler R, Carrive P, Zhang SP (1991) Integration of somatic and autonomic reactions within the midbrain periaqueductal gray: viscerotopic, somatotopic and functional organization. Prog Brain Res 87: 269–305

    PubMed  Google Scholar 

  3. Bolwig TG, Hertz MM, Paulsen OB (1977) The permeability of blood-brain barrier during electrically induced seizures in man. Eur J Clin Invest 7: 87–93

    PubMed  Google Scholar 

  4. Corrodi H, Fuxe K, Kokfelt T (1968) The effect of imobilization stress on the activity of central monoamine neurons. Life Sci 7: 107–112

    Google Scholar 

  5. Dahlstrom A, Fuxe K (1964) Evidence for the existence of monoamine-containing neurons in the central nervous system. 1. Demonstration of monoamines in the cell bodies of brain stem neurons. Acta Physiol Scand 62 [Suppl 232]: 1–55

    Google Scholar 

  6. Donovick PJ (1974) A metachromatic stain for neural tissue. Stain Technol 49: 49–51

    PubMed  Google Scholar 

  7. Dóczi T (1993) Volume regulation of the brain tissue — a survey. Acta Neurochir (Wien) 121: 1–8

    Google Scholar 

  8. Edvinsson L, Lindvall O, Nielsen K, Owman C (1973) Are brain vessels innervated by central (non-sympathetic) adrenergic neurons? Brain Res 63: 496–499

    PubMed  Google Scholar 

  9. Edvinsson L, Owman CH, Siesjo B (1976) Physiological role of cerebrovascular sympathetic nerves in the autorregulation of cerebral blood flow. Brain Res 117: 519–523

    PubMed  Google Scholar 

  10. Harik SI, Sharma VK, Weatherbae JR, Warren RH, Banergee SP (1980) Adrenergic receptors of cerebral microvessles. Eur J Pharmacol 61: 207–208

    PubMed  Google Scholar 

  11. Harper CM, McCulloch J (1985) Cerebral blood flow and cerebrovascular disease. In: Swash M, Kennard C (eds) Scientific basis of clinical neurology. Churchill Livingstone, Edinburg, pp 518–532

    Google Scholar 

  12. Hartman BK (1973) The innervation of cerebral blood vessels by central noradrenergic neurons. In: Usdin E, Snyder SH (eds) Frontiers in catecholamine reasearch. Pergamon, New York, pp 91–96

    Google Scholar 

  13. Johansson BB, Aver LM, Linder LE (1982) Phenothiazine-medited protection of the blood-brain barrier during acute hypertension. Evidence of a modification of the endothelial cell membrane. Stroke 13: 220–225

    PubMed  Google Scholar 

  14. Kobayashi H, Cazzaniga A, Spano PF, Trabucchi M (1982) Ontogenesis of alpha and beta receptors located on cerebral microvessels. Brain Res 242: 358–360

    PubMed  Google Scholar 

  15. Korf J, Aghajanian GK, Roth RH (1973 a) Increased turnover of norepinephrine in the rat cerebral cortex during stress; role of the locus coeruleus. Neuropharmacology 12: 933–938

    PubMed  Google Scholar 

  16. Korf J, Aghajanian GK, Roth RH (1973 b) Stimulation and destruction of the locus coeruleus: opposite effects on 3-methoxy-4-hydroxyphenylglycol sulfate levels in the rat cerebral cortex. Eur J Pharmacol 21: 305–310

    PubMed  Google Scholar 

  17. Korf J, Aghajanian GK, Roth RH (1973 c) Alterations and endogenous levels of noradrenaline in cerebral cortex following electrical stimulation and acute axotomy of cerebral noradrenergic pathways. Eur J Pharmacol 23: 276–282

    PubMed  Google Scholar 

  18. Loizou LA (1969) Projections of the locus coeruleus in the albino rat. Brain Res 15: 563–566

    PubMed  Google Scholar 

  19. Lorenzo AV, Shiarahige JA, Liang M, Barlow CF (1972) Temporary alterations of cerebrovascular permeability during drug induced seizures. Am J Physiol 223: 268–277

    PubMed  Google Scholar 

  20. Menzies SA, Betz AL, Hoff JT (1993) Contributions of ions and albumin to the formation and resolution of ischemic brain edema. J Neurosurg 78: 257–266

    PubMed  Google Scholar 

  21. Mraovitch S, Iadecola C, Ruggiero DA, Reis DJ (1985) Widespread reductions in cerebral blood flow and metabolism elicited by electrical stimulation of the parabrachial nucleus in rat. Brain Res 341: 283–296

    PubMed  Google Scholar 

  22. Mraovitch S, Kumada M, Reis DJ (1982) Role of the nucleus parabrachialis in cardiovascular regulation in cat. BrainRes 232: 57–75

    Google Scholar 

  23. Nag S (1984) Cerebral endothelial surface change in hypertension. Acta Neuropath (Berl) 63: 276–281

    Google Scholar 

  24. Nag S (1986) Cerebral endothelial plasma membrane alterations in acute hypertension. Acta Neuropathol (Berl) 70: 38–43

    Google Scholar 

  25. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates, 2nd Ed. Academic Press, Sydney

    Google Scholar 

  26. Petito CK, Shaefer JA, Plum F (1977) Ultrastructural characteristics of brain and blood-brain barrier in experimental seizures. Brain Res 127: 251–267

    PubMed  Google Scholar 

  27. Preskorn SH, Hartman BK, Irwin GH, Hughes CW (1982) Role of central adrenergic system in mediating amitriptyline induced alterations in mammalian blood-brain barrier in vivo. J Pharmacol Exp Ther 223: 388–395

    PubMed  Google Scholar 

  28. Quagliarello VJ, Long WJ, Scheld WM (1986) Morphologic alterations of the blood-brain barrier with experimental meningitis in the rat. Temporal sequence and the role of encapsulation. J Clin Invest 77: 1084–1095

    PubMed  Google Scholar 

  29. Raichle ME, Eichling JO, Grubb RL, Hartman BK (1976) Central noradrenergic regulation of brain microcirculation. In: Pappius HM, Feindel WM (eds) Dynamics of brain edema. Springer, Berlin Heidelberg New York, pp 11–17

    Google Scholar 

  30. Raichle ME, Hartman BK, Eichling JO, Sharpe LG (1975) Central noradrenergic regulation of cerebral flow and vascular permeability. Proc Natl Acad Sci USA 72: 3726–3730

    PubMed  Google Scholar 

  31. Rapoport S, Thompson H (1975) Opening of the blood-brain barrier by a pulse of hidrostatic pressure. Biophys J 15: 326 a

    Google Scholar 

  32. Rennels ML, Nelson E (1975) Capillary innervation in mammalian central nervous system: an electron microscopic demonstration. Am J Anat 144: 233–241

    PubMed  Google Scholar 

  33. Sarmento A, Albino-Teixeira A, Azevedo I (1988) Increase in blood-brain barrier permeability due to amitriptyline is accompanied by augmented pinocytosis in cerebral capillaries. Br J Pharmacol 96: 838 (Abstract)

    Google Scholar 

  34. Sarmento A, Albino-Teixeira A, Azevedo I (1990) Amitriptyline induced morphologic alterations of the rat blood-brain barrier. Eur J Pharmacol 176: 69–74

    PubMed  Google Scholar 

  35. Sarmento A, Borges N, Azevedo I (1991) Adrenergic influences on the control of blood-brain barrier permeability. Naunyn-Schmiedebergs Arch Pharmacol 343: 633–637

    PubMed  Google Scholar 

  36. Skinho JE, Paulson OB (1969) Carbon dioxide and cerebral circulatory control. Arch Neurol 20: 249–252

    PubMed  Google Scholar 

  37. Swanson LW, Connelly MA, Hartman BK (1977) Ultrastructural evidence for central monoaminergic innervation of blood vessels in the paraventricular nucleus of the hypothalamus. Brain Res 136: 166–173

    PubMed  Google Scholar 

  38. Thierry AM, Javoy F, Glowinski F, Kety SS (1968) Effects of the stress on the metabolism of norepinephrine, dopamine and serotonin in the central nervous system of the rat. Modification of norepinephrine turnover. J Pharmacol Exp Ther 163: 163–171

    PubMed  Google Scholar 

  39. Tunkel AR, Sheld WM (1989) Alterations of blood-brain barrier in bacterial meningitis: in vivo and in vitro models. Ped Inf Dis J 8: 911–913

    Google Scholar 

  40. Tunkel AR, Wispelwey B, Sheld WM (1990) Pathogenesis and pathophysiology of meningitis. Inf Dis Clin North Am 4: 555–581

    Google Scholar 

  41. Ungerstedt U (1971) Mapping of the central dopamine, nor-adrenaline and 5-hydroxytryptamine pathways. Acta Physiol Scand [Suppl] 367: 1–30

    Google Scholar 

  42. Westergaard EV, Deurs B, Bronsted HE (1977) Increased vesicular transfer of horseradish peroxidase across cerebral endothelium evoked by active hypertension. Acta Neuropathol (Berl) 37: 141–152

    Google Scholar 

  43. Xu BN, Yabuki A, Mishima H, Miyazaki M, Maeda M, Ishii S (1993) Pathophysiology of brain swelling after acute experimental brain compression and decompression. Neurosurgery 32: 289–296

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Faculty of Medicine, Institute of Pharmacology and Therapeutics, Porto, Portugal

    A. Sarmento, N. Borges & D. Lima

  2. Faculty of Medicine, Institute of Histology and Embryology, Porto, Portugal

    D. Lima

Authors
  1. A. Sarmento
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. Borges
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. Lima
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Supported by Instituto Nacional de Investigação Científica (INIC FmP1).

Nuno Borges is a PhD student with a grant from Junta Nacional de Investigação Científica e Tecnológica (JNICT).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sarmento, A., Borges, N. & Lima, D. Influence of electrical stimulation of locus coeruleus on the rat blood-brain barrier permeability to sodium fluorescein. Acta neurochir 127, 215–219 (1994). https://doi.org/10.1007/BF01808769

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01808769

Keywords

Search

Navigation