Skip to main content
Log in

Voltammetric detection of the release of 5-hydroxyindole compounds throughout the sleep-waking cycle of the rat

  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Summary

In the present work, differential pulse voltammetry (DPV) measurements of the extracellular fraction of 5-hydroxyindole compounds were performed in rats under long-term chronic conditions. In the nucleus Raphe Dorsalis (n.RD), the voltammetric signal measured at +300 mv (peak 3) disappeared completely 70 to 90 min after injection of Clorgyline (10 mg/kg), a monoamine oxidase inhibitor type A (MAOI-A); the signal measured in such conditions is thus dependent upon extracellular 5-hydroxyindoleacetic acid (5-HIAA peak 3). Deprenyl, an MAOI type B, at the same dose, induced only a slight increase in peak 3 height; according to the fact that MAO-B is selectively located in the 5-HT neurons and since their inhibition does not decrease 5-HIAA peak 3 nor the endogenous 5-HIAA content as measured with High Performance Liquid Chromatography (HPLC), 5-HIAA measured with DPV in the extracellular fluid of untreated animals might come from 5HT released and metabolized by MAO-A outside the 5-HT neurons. In animals implanted for measurements of both voltammetric and polygraphic parameters, the 5-HIAA peak 3 measured mainly in the anterior and ventral part of the n.RD exhibited large increases in its height during slow-wave sleep (SWS: +39%) and paradoxical sleep (PS=+71%) as compared to the waking state (W=100%); these variations could reflect the dendritic release of 5-HT. In the Caudate nucleus (n.Cd) the same voltammetric signal presented reverse fluctuations, i.e. an increase during W and a decrease during SWS and PS. Intracerebroventricular administration of Corticotropin-Like Intermediate lobe Peptide (CLIP, 10 ng/2 μl) induced an increase in PS duration (+51%) preceded and accompanied by an increase in the n.RD 5-HIAA peak 3 height (+50%).

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

  • Arai R, Kimura H, Macola T (1986) Topographic atlas of monoamine oxidase — containing neurons in the rat brain studied by an improved histochemical method. Neuroscience 19:905–925

    Google Scholar 

  • Borbely AA, Tobler I (1989) Endogenous sleep-promoting substances and sleep regulation. Physiol Reviews 69:605–670

    Google Scholar 

  • Cespuglio R, Gomez ME, Walker E, Jouvet M (1979) Effets du refroidissement et de la stimulation des noyaux du système du raphe sur les états de vigilance chez le chat. Electroenceph Clin Neurophysiol 47:289–308

    Google Scholar 

  • Cespuglio R, Faradji H, Gomez ME, Jouvet M (1981a) Single unit recordings in the nuclei raphe dorsalis and magnus during the sleep waking cycle of semi-chronic pretreated cats. Neurosci Lett 24:133–138

    Google Scholar 

  • Cespuglio R, Faradji H, Ponchon JL, Buda M, Riou F, Gonon F, Pujol JF, Jouvet M (1981b) Differential pulse voltammetry in brain tissue. I. Detection of 5-hydroxyindols in the rat striatum. Brain Res 223:287–298

    Google Scholar 

  • Cespuglio R, Faradji H, Hahn Z, Jouvet M (1984) Voltammetric detection of brain 5-hydroxyindolamines by means of electrochemically treated carbon fiber electrodes: chronic recording for up to one month with movable cerebral electrodes in the sleeping or waking rat. In: Marsden CA (ed) Measurement of neurotransmitter release in vivo. IBRO handbook series, Vol 6. Wiley and Sons Ltd, Chichester, pp 173–191

    Google Scholar 

  • Cespuglio R, Sarda N, Gharib H, Faradji H, Jouvet M (1986) Differential pulse voltammetry in vivo with working carbon fiber electrodes: 5-hydroxy-indole compounds or uric acid detection? Exp Brain Res 64:598–595

    Google Scholar 

  • Cespuglio R, Chastrette N, Jouvet M (1988) Opposite variations of 5-hydroxyindoleacetic (5-HIAA) extracellular concentrations, measured with voltammetry either in the axonal nerve endings or in the cell bodies of the nucleus raphe dorsalis, throughout the sleep-waking cycle. CR Acad Sci (Paris) 307:817–823

    Google Scholar 

  • Cespuglio R, Chastrette N, Prevautel H, Jouvet M (1989) Serotonin and hypnogenic factors: functional relationship for sleep induction. In: Inoué S and Krueger JP (eds) Endogenous sleep factors. Bouma text. Wassenar, Tokyo, (in press)

  • Chastrette N, Cespuglio R (1985) Influence of proopiomelanocortin derived peptides on the sleep-waking cycle of the rat. Neurosci Lett 62:365–370

    Google Scholar 

  • Chastrette N, Cespuglio R, Lin YL, Jouvet M (1989) Proopiomelanocortin (POMC) derived peptides and sleep in the rat. II. Aminergic regulatory processes. Neuropeptides (in press)

  • Chazal G, Ralston HJ (1987) Serotonin-containing structures in the nucleus raphe dorsalis of the cat: an ultrastructural analysis of dendrites, presynaptic dendrites and axon terminals. J Comp Neurol 259:317–329

    Google Scholar 

  • Denoyer M, Sallanon M, Kitahama K, Aubert C, Jouvet M (1988) Reversibility of parachlorophenylalanine insomnia by intrahypothalamic microinjection of L 5-hydroxytryptophan. Neurosc 28:83–94

    Google Scholar 

  • De Simoni MG, Sokola A, Fodritto F, Dal Toso B, Algeri S (1987) Functional meaning of tryptophan-induced increase of 5-HT metabolism as clarified by in vivo voltammetry. Brain Res 411:89–94

    Google Scholar 

  • Dzoljic MR (1989) Sleep and selective monoamine oxidase B (MAO-B) inhibitors: possible clinical consequences. In: Koella WP (ed) Sleep 88. Gustav Fischer Verlag, Stuttgart New York, pp 219–221

    Google Scholar 

  • Fornal AC, Jacobs BL (1988) Physiological and behavioral correlates of serotoninergic single-unit activity. In: Osborne NN, Hamon M (eds) Neuronal serotonin. Wiley and Sons Ltd, Chichester, pp 305–345

    Google Scholar 

  • Fowler CJ, Tipton KF (1982) Deamination of 5-hydroxytryptamine by both forms of monoamine oxidase in the rat brain. J Neurochem 38:733–736

    Google Scholar 

  • Froment JL, Petitjean F, Bertrand N, Cointy C, Jouvet M (1974) Effets de l'injection intracérébrale de 5–6-Hydroxytryptamine sur les monoamines cérébrales et les états de sommeil du chat. Brain Res 67:405–417

    Google Scholar 

  • Fueri C, Faudon M, Hery M, Hery F (1984) Release of serotonin from perikarya in cat nodose ganglia. Brain Res 304:173–177

    Google Scholar 

  • Geffard M, Dulluc J, Rock AM (1985) Antisera against the indolkylamines: tryptophan, 5-hydroxytryptophan, 5-hydroxytryptamine, and 5-methoxytryptamine tested by an enzyme-linked immunosorbent assay method. J Neurochem 44:1221–1228

    Google Scholar 

  • Gharib A, Reynaud D, Sarda N, Vivien-Roels B, Pevet P, Pacheco H (1989) Adenosine analogs elevate N-acetylserotonin and melatonin in rat pineal gland. Neurosci Lett 106:345–349

    Google Scholar 

  • Gonon F, Buda M, Cespuglio R, Jouvet M, Pujol JF (1981) Voltammetry in the striatum of chronic freely-moving rats: detection of catechols and ascorbic acid. Brain Res 223:69–80

    Google Scholar 

  • Jouvet M, Renault J (1966) Insomnie persistante aprés lésions des noyaux du raphe chez le chat. CR Soc Biol (Paris) 160:1461–1465

    Google Scholar 

  • Jouvet M (1969) Biogenic amines and the states of sleep. Science 163:32–41

    Google Scholar 

  • Jouvet M (1984) Neuromediateurs et facteurs hypnogènes. Rev Neurol 140:389–400

    Google Scholar 

  • Jouvet M (1988) The regulation of paradoxical sleep by the hypothalamo-hypophysis. Arch Ital Biol 126:259–274

    Google Scholar 

  • Johnston JP (1968) Some observations on a new inhibitor of monoamine oxidase in brain tissue. Biochem Pharmacol 17:1285–1297

    Google Scholar 

  • Kalen P, Strecker RE, Rosengren E, Björklund A (1989) Regulation of striatal serotonin release by the lateral habenula-dorsal raphe pathway in the rat as demonstrated by in vivo microdialysis: role of excitatory amino acids and GABA. Brain Res 492:187–202

    Google Scholar 

  • Kato T, Dong B, Ishii K, Kinemuchi H (1986) Brain dialysis: in vivo metabolism of dopamine and serotonin by monoamine oxidase A but not B in the striatum of unrestained rats. J Neurochem 46:1277–1282

    Google Scholar 

  • Kitahama K, Kimura H, Maeda T, Jouvet M (1987) Distribution of two types of monoamine oxidase-containing neurons in the cat medulla oblongata demonstrated by an improved histo-chemical method. Neurosci 20:991–999

    Google Scholar 

  • Knoll J, Magyar K (1972) Some puzzling pharmacological effects of monoamine oxidase inhibitors. Adv Biochem Psychopharmacol 5:393–408

    Google Scholar 

  • Leger L, Lema F, Chastrette N, Charnay Y, Cespuglio R, Mazie JC, Jouvet M (1990) A monoclonal antibody directed againstCLIP (ACTH 18-39): anatomical distribution of immunoreactivity in the rat brain and hypophysis with quantification of the hypothalamic cell group. J Chem Neuroanat (in press)

  • Masson-Pevet M, Pevet P (1989) Cytochemical localization of type A and B monoamine oxidase in the rat pineal gland. Cell Tissue Res 255:299–305

    Google Scholar 

  • McGinty DJ, Harper RM (1976) Dorsal raphe neurons: depression of firing during sleep in cats. Brain Res 101:569–575

    Google Scholar 

  • Paxinos G, Watson C (1983) The rat brain in stereotaxic coordinates. Academic Press Publishers, New York Paris London, p 85

    Google Scholar 

  • Petitjean F, Buda C, Janin M, Sallanon M, Jouvet M (1980) L'insomnie provoquée par la p.chlorophenylalanine chez le chat: sa réversibilité par l'injection intraventriculaire d'indolamines. C R Acad Sci 291:1063–1066

    Google Scholar 

  • Puizillout JJ, Gaudin-Chazal G, Daszuta A, Seyfritz N, Ternaux JP (1979) Release of endogenous serotonin from “encephale isolé” cats. II. Correlations with raphe neuronal activity and sleep and wakefulness. J Physiol (Paris) 75:531–538

    Google Scholar 

  • Sallanon M, Sakai K, Buda C, Puymartin M, Jouvet M (1986) Augmentation du sommeil paradoxal induite par l'injection d'acide iboténique dans l'hypothalamus ventro latéral postérieur chez le chat. C R Acad Sci (Paris) 303:175–179

    Google Scholar 

  • Touret M, Kitahama K, Geffard M, Jouvet M (1987) 5-hydroxytryptophan (5-HTP) immunoreactive neurons in the rat brain tissue. Neurosci Lett 80:263–267

    Google Scholar 

  • Weissmann D, Belin MF, Aguera M, Meunier C, Maitre M, Cash CD, Ehret M, Mandel P, Pujol JF (1987) Immunohistochemistry of tryptophan hydroxylase in the rat brain. Neuroscience 23:291–304

    Google Scholar 

  • Westlund KN, Denney RM, Kochersperger LM, Rose RM, Abell CW (1985) Distinct monoamine oxidase A and B populations in primate brain. Science 230:181–183

    Google Scholar 

  • Westlund KN, Denney RM, Rose RM, Abell CW (1988) Localization of distinct monoamine oxidase A and monoamine oxidase B cell populations in human brainstem. Neuroscience 25:439–456

    Google Scholar 

  • Wolf WA, Youdim MB, Kuhn DM (1985) Does brain 5-HIAA indicate serotonin release or monoamine oxidase activity? Eur J Pharmacol 109:381–387

    Google Scholar 

  • Zoilla G, Foldi P, Hild G, Szekely AM, Knoll J (1986) The effect of repeated doses of (-) deprenyl on the dynamics of monoaminergic transmission: comparison with clorgyline. Pol J Pharmacol Pharm 38:57–67

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cespuglio, R., Sarda, N., Gharib, A. et al. Voltammetric detection of the release of 5-hydroxyindole compounds throughout the sleep-waking cycle of the rat. Exp Brain Res 80, 121–128 (1990). https://doi.org/10.1007/BF00228853

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00228853

Key words

Navigation