medigraphic.com
ISSN 0185-3325 (Print)
Órgano Oficial del Instituto Nacional de Psiquiatría Ramón de la Fuente Muñiz

2012, Number 5

<< Back

Salud Mental 2012; 35 (5)

Regulación de la liberación de serotonina en distintos compartimientos neuronales

Trueta C, Cercós MG

Language: Spanish
References: 95
Page: 435-443
PDF size: 169.66 Kb.


ABSTRACT

Serotonin is fundamental for the modulation of social behavior, emotions and a wide variety of physiological functions. The functions of serotonergic systems have been highly conserved along the evolutionary scale and in general small numbers of neurons innervate virtually all the nervous system, and exert multiple effects depending on the site of release. Synaptic pools produce fast and local effects, while extrasynaptic pools in the soma, dendrites, axons and the periphery of synapses produce diffuse effects, characteristic of mood modulation. Serotonin release from synaptic terminals is produced by exocytosis of small clear vesicles and is activated by single or low-frequency impulses, while increases in the stimulation frequency produce synaptic facilitation and depression. In contrast, release from the soma is produced by exocytosis of dense-cored vesicles and requires stimulation at high frequencies, the activation of L-type calcium channels and calcium-induced calcium release from intracellular stores. Serotonin released from the presynaptic terminals immediately activates autoreceptors in the same terminals, locally decreasing the subsequent excitability, firing frequency and release. Differential regulation of serotonin release in different cell compartments allows the same neuron to produce different types of effects depending on the firing rate.


REFERENCES

  1. Raleigh MJ, McGuire MT, Brammer GL, Pollack DB et al. Serotonergic mechanisms promote dominance acquisition in adult male vervet monkeys. Brain Res 1991;559:181–190.

  2. Breisch ST, Zemlan FP, Hoebel BG. Hyperphagia and obesity following serotonin depletion by intraventricular p-chlorophenylalanine. Science 1976;192:382–385.

  3. Saller CF, Stricker EM. Hyperphagia and increased growth in rats after intraventricular injection of 5,7-dihydroxytryptamine. Science 1976;192:385–387.

  4. Jacobs BL, Azmitia EC. Structure and function of the brain serotonin system. Physiological Reviews 1992;72:165–229.

  5. Zangrossi H Jr, Viana MB, Zanoveli J, Bueno C et al. Serotonergic regulation of inhibitory avoidance and one-way escape in the rat elevated T-maze. Neurosci Biobehav Rev 2001;25:637–645.

  6. Prosser RA, Miller JD, Heller HC. A serotonin agonist phase-shifts the circadian clock in the suprachiasmatic nuclei in vitro. Brain Res 1990;534:336–339.

  7. Hull EM, Lorrain DS, Du J, Matuszewich L et al. Hormone-neurotransmitter interactions in the control of sexual behavior. Behav Brain Res 1999;105:105–116.

  8. Weiger WA. Serotonergic modulation of behaviour: a phylogenetic overview. Biol Rev Camb Philos Soc 1997;72:61–95.

  9. McCall RB, Aghajanian GK. Serotonergic facilitation of facial motoneuron excitation. Brain Research 1979;169:11–27.

  10. Jacobs BL, Fornal CA. 5-HT and motor control: a hypothesis. Trends Neurosci 1993;16:346–352.

  11. White SR, Fung SJ, Jackson DA, Imel KM. Serotonin, norepinephrine and associated neuropeptides: effects on somatic motoneuron excitability. Prog Brain Res 1996;107:183–199.

  12. Arango V, Underwood MD, Mann JJ. Serotonin brain circuits involved in major depression and suicide. Prog Brain Res 2002;136:443–453.

  13. Jobe PC, Dailey JW, Wernicke JF. A noradrenergic and serotonergic hypothesis of the linkage between epilepsy and affective disorders. Crit Rev Neurobiol 1999;13:317–356.

  14. Brieden T, Ujeyl M, Naber D. Psychopharmacological treatment of aggression in schizophrenic patients. Pharmacopsychiatry 2002;35:83–89.

  15. Jenike MA, Rauch SL, Cummings JL, Savage CR et al. Recent developments in neurobiology of obsessive-compulsive disorder. J Clin Psychiatry 1996;57:492–503.

  16. Livingstone MS, Harris-Warrick RM, Kravitz EA. Serotonin and octopamine produce opposite postures in lobsters. Science 1980;208:76–79.

  17. Harris-Warrick RM, Kravitz EA. Cellular mechanisms for modulation of posture by octopamine and serotonin in the lobster. J Neurosci 1984;4:1976–1993.

  18. Kravitz EA. Serotonin and aggression: insights gained from a lobster model system and speculations on the role of amine neurons in a complex behavior. J Comp Physiol A 2000;186:221–238.

  19. Higley JD, Linnoila M. Low central nervous system serotonergic activity is traitlike and correlates with impulsive behavior. A nonhuman primate model investigating genetic and environmental influences on neurotransmission. Ann N Y Acad Sci 1997;836:39–56.

  20. Ferris CF. Adolescent stress and neural plasticity in hamsters: a vasopressin- serotonin model of inappropriate aggressive behaviour. Exp Physiol 2000;85(número especial):85S–90S.

  21. Lesch KP, Merschdorf U. Impulsivity, aggression, and serotonin: a molecular psychobiological perspective. Behav Sci Law 2000;18:581–604.

  22. Dahlström A, Fuxe K. Localization of monoamines in the lower brain stem. Experientia 1964;20:398–399.

  23. Audet MA, Descarries L, Doucet G. Quantified regional and laminar distribution of the serotonin innervation in the anterior half of adult rat cerebral cortex. J Chem Neuroanat 1989;2:29–44.

  24. Oleskevich S, Descarries L. Quantified distribution of the serotonin innervation in adult rat hippocampus. Neuroscience 1990;34:19–33.

  25. Descarries L, Mechawar N. Ultrastructural evidence for diffuse transmission by monoamine and acetylcholine neurons of the central nervous system. Prog Brain Res 2000;125:27–47.

  26. Kosofsky BE, Molliver ME. The serotoninergic innervation of cerebral cortex: different classes of axon terminals arise from dorsal and median raphe nuclei. Synapse 1987;1:153–168.

  27. Van Bockstaele EJ, Pickel VM. Ultrastructure of serotonin-immunoreactive terminals in the core and shell of the rat nucleus accumbens: cellular substrates for interactions with catecholamine afferents. J Comp Neurol 1993;334:603–617.

  28. Ridet JL, Rajaofetra N, Teilhac JR, Geffard M et al. Evidence for nonsynaptic serotonergic and noradrenergic innervation of the rat dorsal horn and possible involvement of neuron-glia interactions. Neuroscience 1993;52:143–157.

  29. Chazal G, Ralston HJ 3rd. Serotonin-containing structures in the nucleus raphe dorsalis of the cat: an ultrastructural analysis of dendrites, presynaptic dendrites, and axon terminals. J Comp Neurol 1987;259:317–329.

  30. Trueta C, Méndez B, De-Miguel FF. Somatic exocytosis of serotonin mediated by L-type calcium channels in cultured leech neurones. J Physiol (Lond) 2003;547:405–416.

  31. Kaushalya SK, Desai R, Arumugam S, Ghosh H et al. Three-photon microscopy shows that somatic release can be a quantitatively significant component of serotonergic neurotransmission in the mammalian brain. J Neurosci Res 2008;86:3469–3480.

  32. Trueta C, De-Miguel FF. Extrasynaptic exocytosis and its functional implications in the nervous system. Frontiers in Membrane Physiology 2012 (en prensa).

  33. Agnati LF, Fuxe K, Zoli M, Ozini I et al. A correlation analysis of the regional distribution of central enkephalin and β-endorphin immunoreactive terminals and of opiate receptors in adult and old male rats. Evidence for the existence of two main types of communication in the central nervous system: the volume transmission and the wiring transmission. Acta Physiologica Scandinavica 1986;128:201–207.

  34. Agnati LF, Fuxe K, Zoli M, Pich EM et al. Aspects on the information handling by the central nervous system: focus on cotransmission in the aged rat brain. Prog Brain Res 1986;68:291–301.

  35. Fuxe K, Borroto-Escuela DO, Romero-Fernandez W, Ciruela F et al. On the role of volume transmission and receptor-receptor interactions in social behaviour: Focus on central catecholamine and oxytocin neurons. Brain Research Published Online First: 1 February 2012. doi:10.1016/j.brainres.2012.01.062

  36. Zimmermann H. Synaptic Transmission. Cellular and molecular basis. Stuttgart-New York: Georg Thieme Verlag, Oxford University Press; 1993.

  37. Baylor DA, Nicholls JG. Patterns of regeneration between individual nerve cells in the central nervous system of the leech. Nature 1971;232:268–270.

  38. Jansen JK, Nicholls JG. Regeneration and changes in synaptic connections between individual nerve cells in the central nervous system of the leech. Proc Natl Acad Sci USA 1972;69:636–639.

  39. Fuchs PA, Nicholls JG, Ready DF. Membrane properties and selective connexions of identified leech neurones in culture. J Physiol (Lond) 1981;316:203–223.

  40. Ready DF, Nicholls J. Identified neurones isolated from leech CNS make selective connections in culture. Nature 1979;281:67–69.

  41. Fernández-de-Miguel F, Drapeau P. Synapse formation and function: insights from identified leech neurons in culture. J Neurobiol 1995;27:367–379.

  42. Henderson LP. The role of 5-hydroxytryptamine as a transmitter between identified leech neurones in culture. J Physiol (Lond) 1983;339:309–324.

  43. Fuchs PA, Henderson LP, Nicholls JG. Chemical transmission between individual Retzius and sensory neurones of the leech in culture. J Physiol (Lond) 1982;323:195–210.

  44. Henderson LP, Kuffler DP, Nicholls J, Zhang R. Structural and functional analysis of synaptic transmission between identified leech neurones in culture. J Physiol (Lond) 1983;340:347–358.

  45. Kuffler DP, Nicholls J, Drapeau P. Transmitter localization and vesicle turnover at a serotoninergic synapse between identified leech neurons in culture. J Comp Neurol 1987;256:516–526.

  46. Bruns D, Jahn R. Real-time measurement of transmitter release from single synaptic vesicles. Nature 1995;377:62–65.

  47. Bruns D, Riedel D, Klingauf J, Jahn R. Quantal release of serotonin. Neuron 2000;28:205–220.

  48. Golding DW, Bayraktaroglu E. Exocytosis of secretory granules - A probable mechanism for the release of neuromodulators in invertebrate neuropiles. Experientia 1984;40:1277-1285.

  49. Zhu PC, Thureson-Klein A, Klein RL. Exocytosis from large dense cored vesicles outside the active synaptic zones of terminals within the trigeminal subnucleus caudalis: a possible mechanism for neuropeptide release. Neuroscience 1986;19:43–54.

  50. Lysakowski A, Figueras H, Price SD, Peng YY. Dense-cored vesicles, smooth endoplasmic reticulum, and mitochondria are closely associated with non-specialized parts of plasma membrane of nerve terminals: implications for exocytosis and calcium buffering by intraterminal organelles. J Comp Neurol 1999;403:378–390.

  51. Dietzel ID, Drapeau P, Nicholls JG. Voltage dependence of 5-hydroxytryptamine release at a synapse between identified leech neurones in culture. J Physiol (Lond) 1986;372:191–205.

  52. Stewart RR, Adams WB, Nicholls JG. Presynaptic calcium currents and facilitation of serotonin release at synapses between cultured leech neurones. J Exp Biol 1989;144:1–12.

  53. Trueta C, De-Miguel FF, Kuffler DP. Cycling of dense core vesicles involved in somatic exocytosis of serotonin by leech neurons. Frontiers Membrane Physiology 2012 (en prensa).

  54. Cochilla AJ, Angleson JK, Betz WJ. Monitoring secretory membrane with FM1-43 fluorescence. Annu Rev Neurosci 1999;22:1–10.

  55. Reuter H. Diversity and function of presynaptic calcium channels in the brain. Curr Opin Neurobiol 1996;6:331–337.

  56. Trueta C, Sánchez-Armass S, Morales MA, De-Miguel FF. Calciuminduced calcium release contributes to somatic secretion of serotonin in leech Retzius neurons. J Neurobiol 2004;61:309–316.

  57. Lin SL, Setya S, Johnson-Farley NN, Cowen DS. Differential coupling of 5-HT(1) receptors to G proteins of the G(i) family. Br J Pharmacol 2002;136:1072–1078.

  58. Aghajanian GK, Lakoski JM. Hyperpolarization of serotonergic neurons by serotonin and LSD: studies in brain slices showing increased K+ conductance. Brain Res 1984;305:181–185.

  59. Lessmann V, Dietzel ID. Development of serotonin-induced ion currents in identified embryonic Retzius cells from the medicinal leech (Hirudo medicinalis). J Neurosci 1991;11:800–809.

  60. Gerschenfeld HM. Serotonin: two different inhibitory actions on snail neurons. Science 1971;171:1252–1254.

  61. Blier P, Piñeyro G, el Mansari M, Bergeron R et al. Role of somatodendritic 5-HT autoreceptors in modulating 5-HT neurotransmission. Ann N Y Acad Sci 1998;861:204–216.

  62. Verge D, Daval G, Patey A, Gozlan H et al. Presynaptic 5-HT autoreceptors on serotonergic cell bodies and/or dendrites but not terminals are of the 5-HT1A subtype. Eur J Pharmacol 1985;113:463–464.

  63. Göthert M. Presynaptic serotonin receptors in the central nervous system. Ann N Y Acad Sci 1990;604:102–112.

  64. Roberts C, Price GW, Middlemiss DN. Ligands for the investigation of 5-HT autoreceptor function. Brain Res Bull 2001;56:463–469.

  65. Sari Y. Serotonin1B receptors: from protein to physiological function and behavior. Neurosci Biobehav Rev 2004;28:565–582.

  66. Stamford JA, Davidson C, McLaughlin DP, Hopwood SE. Control of dorsal raphé 5-HT function by multiple 5-HT(1) autoreceptors: parallel purposes or pointless plurality? Trends Neurosci 2000;23:459–465.

  67. Gallager DW, Aghajanian GK. Inhibition of firing of raphe neurones by tryptophan and 5-hydroxytryptophan: blockade by inhibiting serotonin synthesis with Ro-4-4602. Neuropharmacology 1976;15:149–156.

  68. Trulson ME, Jacobs BL. Dose-response relationships between systemically administered L-tryptophan or L-5-hydroxytryptophan and raphe unit activity in the rat. Neuropharmacology 1976;15:339–344.

  69. de Montigny C, Aghajanian GK. Preferential action of 5-methoxytryptamine and 5-methoxydimethyltryptamine on presynaptic serotonin receptors: A comparative iontophoretic study with LSD and serotonin. Neuropharmacology 1977;16:811–818.

  70. Rogawski MA, Aghajanian GK. Serotonin autoreceptors on dorsal raphe neurons: structure-activity relationships of tryptamine analogs. J Neurosci 1981;1:1148–1154.

  71. Chaput Y, Blier P, de Montigny C. In vivo electrophysiological evidence for the regulatory role of autoreceptors on serotonergic terminals. J Neurosci 1986;6:2796–2801.

  72. VanderMaelen CP, Matheson GK, Wilderman RC, Patterson LA. Inhibition of serotonergic dorsal raphe neurons by systemic and iontophoretic administration of buspirone, a non-benzodiazepine anxiolytic drug. Eur J Pharmacol 1986;129:123–130.

  73. Trulson ME, Crisp T. Do serotonin-containing dorsal raphe neurons possess autoreceptors? Exp Brain Res 1986;62:579–586.

  74. Trulson ME, Frederickson CJ. A comparison of the electrophysiological and pharmacological properties of serotonin-containing neurons in the nucleus raphe dorsalis, raphe medianus and raphe pallidus recorded from mouse brain slices in vitro: role of autoreceptors. Brain Res Bull 1987;18:179–190.

  75. Sprouse JS, Aghajanian GK. Responses of hippocampal pyramidal cells to putative serotonin 5-HT1A and 5-HT1B agonists: a comparative study with dorsal raphe neurons. Neuropharmacology 1988;27:707–715.

  76. Sinton CM, Fallon SL. Electrophysiological evidence for a functional differentiation between subtypes of the 5-HT1 receptor. Eur J Pharmacol 1988;157:173–181.

  77. O’Connor JJ, Kruk ZL. Frequency dependence of 5-HT autoreceptor function in rat dorsal raphe and suprachiasmatic nuclei studied using fast cyclic voltammetry. Brain Research 1991;568:123–130.

  78. Fornal CA, Litto WJ, Metzler CW, Marrosu F et al. Single-unit responses of serotonergic dorsal raphe neurons to 5-HT1A agonist and antagonist drug administration in behaving cats. J Pharmacol Exp Ther 1994;270:1345–1358.

  79. Gobert A, Lejeune F, Rivet JM, Audinot V et al. Modulation of the activity of central serotoninergic neurons by novel serotonin1A receptor agonists and antagonists: a comparison to adrenergic and dopaminergic neurons in rats. J Pharmacol Exp Ther 1995;273:1032–1046.

  80. Baumann PA, Waldmeier PC. Negative feedback control of serotonin release in vivo: comparison of 5-hydroxyindolacetic acid levels measured by voltammetry in conscious rats and by biochemical techniques. Neuroscience 1984;11:195–204.

  81. Stauderman KA, Jones DJ. Presynaptic serotonin receptors regulate 3Hserotonin release from rat spinal cord synaptosomes. Eur J Pharmacol 1986;120:107–109.

  82. Bonanno G, Maura G, Raiteri M. Pharmacological characterization of release-regulating serotonin autoreceptors in rat cerebellum. Eur J Pharmacol 1986;126:317–321.

  83. Hjorth S, Magnusson T. The 5-HT 1A receptor agonist, 8-OH-DPAT, preferentially activates cell body 5-HT autoreceptors in rat brain in vivo. Naunyn Schmiedebergs Arch Pharmacol 1988;338:463–471.

  84. Sharp T, Bramwell SR, Clark D, Grahame-Smith DG. In vivo measurement of extracellular 5-hydroxytryptamine in hippocampus of the anaesthetized rat using microdialysis: changes in relation to 5-hydroxytryptaminergic neuronal activity. J Neurochem 1989;53:234–240.

  85. Wichmann T, Limberger N, Starke K. Release and modulation of release of serotonin in rabbit superior colliculus. Neuroscience 1989;32:141–151.

  86. Invernizzi R, Bramante M, Samanin R. Chronic treatment with citalopram facilitates the effect of a challenge dose on cortical serotonin output: role of presynaptic 5-HT1A receptors. Eur J Pharmacol 1994;260:243–246.

  87. Bonvento G, Scatton B, Claustre Y, Rouquier L. Effect of local injection of 8-OH-DPAT into the dorsal or median raphe nuclei on extracellular levels of serotonin in serotonergic projection areas in the rat brain. Neurosci Lett 1992;137:101–104.

  88. Galzin AM, Poirier MF, Lista A, Chodkiewicz JP, Blier P, Ramdine R, et al. Characterization of the 5-hydroxytryptamine receptor modulating the release of 5-3Hhydroxytryptamine in slices of the human neocortex. J Neurochem 1992;59:1293–1301.

  89. Starkey SJ, Skingle M. 5-HT1D as well as 5-HT1A autoreceptors modulate 5-HT release in the guinea-pig dorsal raphé nucleus. Neuropharmacology 1994;33:393–402.

  90. Davidson C, Stamford JA. Evidence that 5-hydroxytryptamine release in rat dorsal raphé nucleus is controlled by 5-HT1A, 5-HT1B and 5- HT1D autoreceptors. Br J Pharmacol 1995;114:1107–1109.

  91. Piñeyro G, Castanon N, Hen R, Blier P. Regulation of 3H5-HT release in raphe, frontal cortex and hippocampus of 5-HT1B knock-out mice. Neuroreport 1995;7:353–359.

  92. Rollema H, Lu Y, Schmidt AW, Zorn SH. Clozapine increases dopamine release in prefrontal cortex by 5-HT1A receptor activation. Eur J Pharmacol 1997;338:R3–5.

  93. Rutz S, Riegert C, Rothmaier AK, Jackisch R. Presynaptic modulation of 5-HT release in the rat septal region. Neuroscience 2007;146:643–658.

  94. Birthelmer A, Ehret A, Riegert C, Rothmaier AK et al. Modulation of electrically evoked serotonin release in cultured rat raphe neurons. J Neurochem 2007;100:1613–1625.

  95. Cercós MG, De-Miguel FF, Trueta C. Real-time measurements of synaptic autoinhibition produced by serotonin release in cultured leech neurons. J Neurophysiol 2009;102:1075–1085.




2020     |     www.medigraphic.com