nach oben

Journal of Neural Transmission

Erschienen in:

01.02.2015 | Translational Neurosciences - Original Article

Endogenous serotonin facilitates hippocampal long-term potentiation at CA3/CA1 synapses

verfasst von: Boris Mlinar, Gabriella Stocca, Renato Corradetti

Erschienen in: Journal of Neural Transmission | Ausgabe 2/2015

Einloggen, um Zugang zu erhalten

Abstract

Encoding of episodic memory requires long-term potentiation (LTP) of neurotransmission at excitatory synapses of the hippocampal circuitry. Previous data obtained with the application of exogenous 5-hydroxytryptamine (5-HT) in hippocampal slices indicate that 5-HT blocks LTP, which contrasts with the facilitatory effect of selective serotonin reuptake inhibitors (SSRIs) on learning and memory observed in vivo. Here, we investigated the effects of endogenous 5-HT, released from terminals by the monoamine releaser 3,4-methylenedioxymethamphetamine (MDMA), on LTP of field EPSPs induced by theta-burst stimulation and recorded at CA3/CA1 synapses of rat hippocampal slices. LTP was greater in the presence of MDMA (10 µM; 45.76 ± 15.75 %; n = 28) than in controls (31.26 ± 11.03; n = 21; p < 0.01). This facilitatory effect on LTP persisted when the entry of MDMA in noradrenergic terminals was prevented by the selective noradrenaline reuptake inhibitor nisoxetine (44.90 ± 14.07 %; n = 27 vs. 34.49 ± 12.94 %; n = 20 in controls; p < 0.05). In both conditions, the facilitation of LTP was abolished by the SSRI citalopram that prevented the entry of MDMA in 5-HT terminals and the subsequent 5-HT release. These data show that, unlike exogenous 5-HT application, release of endogenous 5-HT does not impair cellular mechanisms responsible for induction of LTP, indicating that 5-HT is not detrimental to learning and memory. Moreover, facilitation of LTP by endogenous 5-HT may underlie the in vivo positive effects of augmented 5-HT tone on cognitive performance.

Abad S, Fole A, Del Olmo N, Pubill D, Pallàs M, Junyent F, Camarasa J, Camins A, Escubedo E (2014) MDMA enhances hippocampal-dependent learning and memory under restrictive conditions, and modifies hippocampal spine density. Psychopharmacology (Berl). Psychopharmacology 231(5):863–874PubMedCrossRef

Anderson IM, Juhasz G, Thomas E, Downey D, McKie S, Deakin JF, Elliott R (2011) The effect of acute citalopram on face emotion processing in remitted depression: a pharmacoMRI study. Eur Neuropsychopharmacol 21(1):140–148PubMedCrossRef

Andrade R, Beck SG (2010) Cellular effects of serotonin in the CNS. In: Muller CP, Jacobs B (eds) Handbook of the behavioral neurobiology of serotonin. Academic Press, London, pp 219–231CrossRef

Barnes NM, Sharp T (1999) A review of central 5-HT receptors and their function. Neuropharmacology 38(8):1083–1152PubMedCrossRef

Bliss TVP, Goddard GV, Riives M (1983) Reduction of long-term potentiation in the dentate gyrus of the rat following selective depletion of monoamines. J Physiol (London) 334:475–491CrossRef

Bliss TVP, Collingridge GL, Morris R (2007) Synaptic plasticity in the hippocampus. In: Andersen P, Morris R, Amaral D, Bliss T, O’Keefe J (eds) The hippocampus book. Oxford University Press Inc, New York, pp 343–474

Corradetti R, Ballerini L, Pugliese AM, Pepeu G (1992) Serotonin blocks the long-term potentiation induced by primed burst stimulation in the CA1 region of rat hippocampal slices. Neuroscience 46:511–518PubMedCrossRef

Del-Ben CM, Ferreira CA, Alves-Neto WC, Graeff FG (2008) Serotonergic modulation of face-emotion recognition. Braz J Med Biol Res 41:263–269PubMedCrossRef

Elliott R, Zahn R, Deakin JF, Anderson IM (2011) Affective cognition and its disruption in mood disorders. Neuropsychopharmacology 36(1):153–182PubMedCentralPubMedCrossRef

Fitzgerald JL, Reid JJ (1993) Interactions of methylenedioxymethamphetamine with monoamine transmitter release mechanisms in rat brain slices. Naunyn Schmiedebergs Arch Pharmacol 347:313–323PubMedCrossRef

Garrett AS, Maddock RJ (2006) Separating subjective emotion from the perception of emotion-inducing stimuli: an fMRI study. Neuroimage 33:263–274PubMedCrossRef

Harmer CJ, Bhagwagar Z, Cowen PJ, Goodwin GM (2002) Acute administration of citalopram facilitates memory consolidation in healthy volunteers. Psychopharmacology 163:106–110PubMedCrossRef

Harmer CJ, Bhagwagar Z, Perrett DI, Völlm BA, Cowen PJ, Goodwin GM (2003) Acute SSRI administration affects the processing of social cues in healthy volunteers. Neuropsychopharmacology 28(1):148–152PubMedCrossRef

Hayward G, Goodwin GM, Cowen PJ, Harmer CJ (2005) Low-dose tryptophan depletion in recovered depressed patients induces changes in cognitive processing without depressive symptoms. Biol Psychiatry 57(5):517–524PubMedCrossRef

Hensler JG (2006) Serotonergic modulation of the limbic system. Neurosci Biobehav Rev 30(2):203–214PubMedCrossRef

Hyttel J, Larsen JJ (1985) Neurochemical profile of Lu 19-005, a potent inhibitor of uptake of dopamine, noradrenaline, and serotonin. J Neurochem 44:1615–1622PubMedCrossRef

Izquierdo I, Medina JH (1995) Correlation between the pharmacology of long-term potentiation and the pharmacology of memory. Neurobiol Learn Mem 63(1):19–32PubMedCrossRef

Jahnsen H (1980) The action of 5-hydroxytryptamine on neuronal membranes and synaptic transmission in area CA1 of the hippocampus in vitro. Brain Res 197:83–94PubMedCrossRef

Jensen O, Lisman JE (2005) Hippocampal sequence-encoding driven by a cortical multi-item working memory buffer. Trends Neurosci 28(2):67–72PubMedCrossRef

Johnston D, Wu SMS (1995) Extracellular field recordings. In: Johnston D, Wu SMS (eds) Foundations of cellular neurophysiology. MIT Press, Cambridge, pp 423–439

Klancnik JM, Phillips AG (1991) Modulation of synaptic plasticity in the dentate gyrus of the rat by electrical stimulation of the median raphe nucleus. Brain Res 557(1–2):236–240PubMedCrossRef

Kuypers KP, Ramaekers JG (2007) Acute dose of MDMA (75 mg) impairs spatial memory for location but leaves contextual processing of visuospatial information unaffected. Psychopharmacology 189(4):557–563PubMedCrossRef

Larson J, Lynch G (1986) Induction of synaptic potentiation in hippocampus by patterned stimulation involves two events. Science 232:985–988PubMedCrossRef

Lesch KP, Waider J (2012) Serotonin in the modulation of neural plasticity and networks: implications for neurodevelopmental disorders. Neuron 76(1):175–191PubMedCrossRef

McKie S, Del-Ben C, Elliott R, Williams S, del Vai N, Anderson I, Deakin JF (2005) Neuronal effects of acute citalopram detected by pharmacoMRI. Psychopharmacology 180(4):680–686PubMedCrossRef

Mlinar B, Corradetti R (2003) Endogenous 5-HT, released by MDMA through serotonin transporter- and secretory vesicle-dependent mechanisms, reduces hippocampal excitatory synaptic transmission by preferential activation of 5-HT1B receptors located on CA1 pyramidal neurons. Eur J Neurosci 18:1559–1571PubMedCrossRef

Mlinar B, Mascalchi S, Morini R, Giachi F, Corradetti R (2008) MDMA induces EPSP-Spike potentiation in rat ventral hippocampus in vitro via serotonin and noradrenaline release and coactivation of 5-HT4 and beta1 receptors. Neuropsychopharmacology 33:1464–1475PubMedCrossRef

Morini R, Mlinar B, Baccini G, Corradetti R (2011) Enhanced hippocampal long-term potentiation following repeated MDMA treatment in Dark-Agouti rats. Eur Neuropsychopharmacol 21:80–91PubMedCrossRef

Moyano S, Frechilla D, Del Río J (2004) NMDA receptor subunit and CaMKII changes in rat hippocampus induced by acute MDMA treatment: a mechanism for learning impairment. Psychopharmacology 173(3–4):337–345PubMedCrossRef

Otto T, Eichenbaum H, Wiener SI, Wible CG (1991) Learning-related patterns of CA1 spike trains parallel stimulation parameters optimal for inducing hippocampal long-term potentiation. Hippocampus 1:181–192PubMedCrossRef

Pugliese AM, Ballerini L, Passani MB, Corradetti R (1994) EPSP-Spike potentiation during primed burst-induced long-term potentiation in the CA1 region of rat hippocampal slices. Neuroscience 62:1021–1032PubMedCrossRef

Pugliese AM, Passani MB, Corradetti R (1998) Effect of the selective 5-HT1A receptor antagonist WAY 100635 on the inhibition of e.p.s.ps produced by 5-HT in the CA1 region of rat hippocampal slices. Br J Pharmacol 124(1):93–100PubMedCrossRef

Richter-Levin G, Segal M (1991) The effects of serotonin depletion and raphe grafts on hippocampal electrophysiology and behavior. J Neurosci 11(6):1585–1596PubMed

Rodsiri R, Spicer C, Green AR, Marsden CA, Fone KC (2011) Acute concomitant effects of MDMA binge dosing on extracellular 5-HT, locomotion and body temperature and the long-term effect on novel object discrimination in rats. Psychopharmacology 213(2–3):365–376PubMedCrossRef

Ropert N (1988) Inhibitory action of serotonin in CA1 hippocampal neurons in vitro. Neuroscience 26:69–81PubMedCrossRef

Rozas C, Loyola S, Ugarte G, Zeise ML, Reyes-Parada M, Pancetti F, Rojas P, Morales B (2012) Acutely applied MDMA enhances long-term potentiation in rat hippocampus involving D1/D5 and 5-HT2 receptors through a polysynaptic mechanism. Eur Neuropsychopharmacol 22(8):584–595PubMedCrossRef

Rudnick G, Wall SC (1992) The molecular mechanism of ‘ecstasy’ [3,4-methylenedioxy-methamphetamine (MDMA)]: serotonin transporters are targets for MDMA-induced serotonin release. Proc Natl Acad Sci USA 89:1817–1821PubMedCentralPubMedCrossRef

Schaefer HS, Putnam KM, Benca RM, Davidson RJ (2006) Event-related functional magnetic resonance imaging measures of neural activity to positive social stimuli in pre- and post-treatment depression. Biol Psychiatry 60:974–986PubMedCrossRef

Segal M (1980) The action of serotonin in the hippocampal slice preparation. J Physiol (London) 303:423–439CrossRef

Sitte HH, Scholze P, Schloss P, Pifl C, Singer EA (2000) Characterization of carrier-mediated efflux in human embryonic kidney 293 cells stably expressing the rat serotonin transporter: a superfusion study. J Neurochem 74:1317–1324PubMedCrossRef

Staubli U, Otaky N (1994) Serotonin controls the magnitude of LTP induced by theta bursts via an action on NMDA- receptor-mediated responses. Brain Res 643:10–16PubMedCrossRef

Stough C, King R, Papafotiou K, Swann P, Ogden E, Wesnes K, Downey LA (2012) The acute effects of 3,4-methylenedioxymethamphetamine and d-methamphetamine on human cognitive functioning. Psychopharmacology 220(4):799–807PubMedCrossRef

Tse WS, Bond AJ (2002) Serotonergic intervention affects both social dominance and affiliative behaviour. Psychopharmacology 161(3):324–330PubMedCrossRef

van der Veen FM, Evers EA, van Deursen JA, Deutz NE, Backesm WH, Schmitt JA (2006) Acute tryptophan depletion reduces activation in the right hippocampus during encoding in an episodic memory task. Neuroimage 31(3):1188–1196PubMedCrossRef

Villani F, Johnston D (1993) Serotonin inhibits induction of long-term potentiation at commissural synapses in hippocampus. Brain Res 606:304–308PubMedCrossRef

Wang SH, Morris RG (2010) Hippocampal-neocortical interactions in memory formation, consolidation, and reconsolidation. Annu Rev Psychol 61(49–79):C1–C4

Whitlock JR, Heynen AJ, Shuler MG, Bear MF (2006) Learning induces long-term potentiation in the hippocampus. Science 313:1093–1097PubMedCrossRef

Winterer J, Stempel AV, Dugladze T, Földy C, Maziashvili N, Zivkovic AR, Priller J, Soltesz I, Gloveli T, Schmitz D (2011) Cell-type-specific modulation of feedback inhibition by serotonin in the hippocampus. J Neurosci 31(23):8464–8475PubMedCrossRef

Young SN, Leyton M (2002) The role of serotonin in human mood and social interaction Insight from altered tryptophan levels. Pharmacol Biochem Behav 71(4):857–865PubMedCrossRef

Titel: Endogenous serotonin facilitates hippocampal long-term potentiation at CA3/CA1 synapses
verfasst von: Boris Mlinar
Gabriella Stocca
Renato Corradetti
Publikationsdatum: 01.02.2015
Verlag: Springer Vienna
Erschienen in: Journal of Neural Transmission / Ausgabe 2/2015
Print ISSN: 0300-9564
Elektronische ISSN: 1435-1463
DOI: https://doi.org/10.1007/s00702-014-1246-7

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Neu im Fachgebiet Neurologie

Hirnblutung unter DOAK und VKA ähnlich bedrohlich

17.05.2024 Direkte orale Antikoagulanzien Nachrichten

Kommt es zu einer nichttraumatischen Hirnblutung, spielt es keine große Rolle, ob die Betroffenen zuvor direkt wirksame orale Antikoagulanzien oder Marcumar bekommen haben: Die Prognose ist ähnlich schlecht.

Thrombektomie auch bei großen Infarkten von Vorteil

16.05.2024 Ischämischer Schlaganfall Nachrichten

Auch ein sehr ausgedehnter ischämischer Schlaganfall scheint an sich kein Grund zu sein, von einer mechanischen Thrombektomie abzusehen. Dafür spricht die LASTE-Studie, an der Patienten und Patientinnen mit einem ASPECTS von maximal 5 beteiligt waren.

Schwindelursache: Massagepistole lässt Otholiten tanzen

14.05.2024 Benigner Lagerungsschwindel Nachrichten

Wenn jüngere Menschen über ständig rezidivierenden Lagerungsschwindel klagen, könnte eine Massagepistole der Auslöser sein. In JAMA Otolaryngology warnt ein Team vor der Anwendung hochpotenter Geräte im Bereich des Nackens.

Schützt Olivenöl vor dem Tod durch Demenz?

10.05.2024 Morbus Alzheimer Nachrichten

Konsumieren Menschen täglich 7 Gramm Olivenöl, ist ihr Risiko, an einer Demenz zu sterben, um mehr als ein Viertel reduziert – und dies weitgehend unabhängig von ihrer sonstigen Ernährung. Dafür sprechen Auswertungen zweier großer US-Studien.

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Die Highlights vom Kongress des American College of Cardiology 2024

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 2/2015

Safety aspects of incobotulinumtoxinA high-dose therapy

Serotonergic transmission after spinal cord injury

Cerebrospinal fluid inflammatory markers in patients with multiple sclerosis: a pilot study

The physiology of the pedunculopontine nucleus: implications for deep brain stimulation

Acknowledgement to reviewers 2014