The promnesic effect of G-protein-coupled 5-HT4 receptors activation is mediated by a potentiation of learning-induced spine growth in the mouse hippocampus

Neuropsychopharmacology

Volumn 33, Issue 10, 2008, Pages 2427-2434

  Restivo, Leonardo ^a,b   Roman, François ^c   Dumuis, Aline ^d   Bockaert, Joel ^d   Marchetti, Evelyne ^c   Ammassari Teule, Martine ^a,b,e  

^a CNR Consiglio Nazionale delle Ricerche   (Italy)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^c AIX MARSEILLE UNIVERSITÉ   (France)

^d INSERM   (France)

^e CNR   (Italy)

Author keywords

5 HT4 receptor; Dendritic spines; Learning induced structural plasticity; Mice; Olfactory discrimination

Indexed keywords

5 (8 AMINO 7 CHLORO 2,3 DIHYDRO 1,4 BENZODIOXIN 5 YL) 3 [1 (2 PHENYLETHYL) 4 PIPERIDINYL] 1,3,4 OXADIAZOL 2(3H) ONE; G PROTEIN COUPLED RECEPTOR; RS 39604; SEROTONIN 4 AGONIST; SEROTONIN 4 ANTAGONIST; SEROTONIN 4 RECEPTOR; SL 650155; SODIUM CHLORIDE; UNCLASSIFIED DRUG; [1 [4 AMINO 5 CHLORO 2 (3,5 DIMETHOXYPHENYL)METHYLOXY] 3 [1 (2 METHYLSULFONYLAMINO)ETHYL]PIPERIDIN 4 YL]PROPAN 1 ONE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITIC SPINE; DRUG EFFECT; DRUG POTENTIATION; DRUG RECEPTOR BINDING; HIPPOCAMPUS; LEARNING; MALE; MEMORY; MOUSE; NERVE CELL GROWTH; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; OLFACTORY DISCRIMINATION; PRIORITY JOURNAL; PROTEIN FUNCTION; SYNAPTIC EFFICACY;

EID: 49549091142     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.npp.1301644     Document Type: Article

References (35)

1. Barthet G, Framery B, Gaven F, Pellissier L, Reiter E, Claeysen S et al. (2007). 5-HT4 receptor activation of the ERK pathway depends on Src activation but not on G protein or beta-arrestin signaling. Mol Biol Cell 6: 1979-1991.
2. Bickmeyer U, Heine M, Manzke T, Richter DW (2002). Differential modulation of I(h) by 5-HT receptors in mouse CA1 hippocampal neurons. Eur J Neurosci 16: 209-218.
3. Bockaert J, Claeysen S, Compan V, Dumuis A (2004). 5-HT4 receptors. Curr Drug Targets CNS Neurol Disord 3: 39-51.
4. Dumuis A, Bouhelal R, Sebben M, Bockaert J (1988). A 5-HT receptor in the central nervous system, positively coupled with adenylate cyclase, is antagonized by ICS 205 930. Eur J Pharmacol 146: 187-188.
5. Eichenbaum H (2004). Hippocampus: cognitive processes and neural representations that underlie declarative memory. Neuron 44: 109-120.
6. Eichenbaum H, Fagan A, Mathews P, Cohen NJ (1988). Hippocampal system dysfunction and odor discrimination learning in rats: impairment or facilitation depending on representational demands. Behav Neurosci 102: 331-339.
7. Gibb R, Kolb B (1998). A method for vibratome sectioning of Golgi-Cox stained whole rat brain. J Neurosci Methods 79: 1-4.
8. Glaser EM, Van der Loos H (1981). Analysis of thick brain sections by obverse-reverse computer microscopy: application of a new, high clarity Golgi-Nissl stain. J Neurosci Methods 4: 117-125.
9. Huang YY, Kandel ER (2007). 5-Hydroxytryptamine induces a protein kinase A/mitogen-activated protein kinase-mediated and macromolecular synthesis-dependent late phase of long-term potentiation in the amygdala. J Neurosci 27: 3111-3119.
10. Kaibara T, Leung LS (1993). Basal vs apical dendritic long-term potentiation of commissural afferents to hippocampal CA1: a current-source density study. J Neurosci 13: 2391-2404.
11. Kemp A, Manahan-Vaughan D (2005). The 5-hydroxytryptamine4 receptor exhibits frequency-dependent properties in synaptic plasticity and behavioural metaplasticity in the hippocampal CA1 region in vivo. Cereb Cortex 15: 1037-1043.
12. Knafo S, Libersat F, Barkai E (2005). Dynamics of learning-induced spine redistribution along dendrites of pyramidal neurons in rats. Eur J Neurosci 21: 927-935.
13. Kulla A, Manahan-Vaughan D (2002). Modulation by serotonin 5-HT(4) receptors of long-term potentiation and depotentiation in the dentate gyrus of freely moving rats. Cereb Cortex 12: 150-162.
14. Kushner SA, Elgersma Y, Murphy GG, Jaarsma D, van Woerden GM, Hojjati MR et al. (2005). Modulation of presynaptic plasticity and learning by the H-ras/extracellular signal-regulated kinase/synapsin I signaling pathway. J Neurosci 25: 9721-9734.
15. Leuner B, Falduto J, Shors TJ (2003). Associative memory formation increases the observation of dendritic spines in the hippocampus. J Neurosci 23: 659-665.
16. Marchetti E, Chaillan FA, Dumuis A, Bockaert J, Soumireu-Mourat B, Roman FS (2004). Modulation of memory processes and cellular excitability in the dentate gyrus of freely moving rats by a 5-HT4 receptors partial agonist, and an antagonist. Neuropharmacology 47: 1021-1035.
17. Marchetti E, Dumuis A, Bockaert J, Soumireu-Mourat B, Roman FS (2000). Differential modulation of the 5-HT(4) receptor agonists and antagonist on rat learning and memory. Neuropharmacology 39: 2017-2027.
18. Micale V, Marco Leggio G, Mazzola C, Drago F (2007). Cognitive effects of SL65.0155, a serotonin 5-HT(4) receptor partial agonist, in animal models of amnesia. Brain Res 1121: 207-215.
19. Morris RG, Moser EI, Riedel G, Martin SJ, Sandin J, Day M et al. (2003). Elements of a neurobiological theory of the hippocampus: the role of activity-dependent synaptic plasticity in memory. Philos Trans R Soc Lond B Biol Sci 358: 773-786.
20. Moser MB, Trommald M, Egeland T, Andersen P (1997). Spatial training in a complex environment and isolation alter the spine distribution differently in rat CA1 pyramidal cells. J Comp Neurol 380: 373-381.
21. Moser PC, Bergis OE, Jegham S, Lochead A, Duconseille E, Terranova JP et al. (2002). SL65.0155, a novel 5-hydroxytryptamine(4) receptor partial agonist with potent cognition-enhancing properties. J Pharmacol Exp Ther 302: 731-741.
22. Muller D, Toni N, Buchs PA (2000). Spine changes associated with long-term potentiation. Hippocampus 10: 596-604.
23. Myers CE, Gluck MA (1996). Cortico-hippocampal representations in simultaneous odor discrimination: a computational interpretation of Eichenbaum, Mathews, and Cohen (1989). Behav Neurosci 110: 685-706.
24. Orsetti M, Dellarole A, Ferri S, Ghi P (2003). Acquisition, retention, and recall of memory after injection of RS67333, a 5-HT(4) receptor agonist, into the nucleus basalis magnocellularis of the rat. Learn Mem 10: 420-426.
25. Paxinos G, Franklin KBJ (2001). The Mouse Brain in Stereotaxic Coordinates, 2nd edn. Academic Press: San Diego.
26. Restivo L, Roman FS, Ammassari-Teule M, Marchetti E (2006). Simultaneous olfactory discrimination elicits a strain-specific increase in dendritic spines in the hippocampus of inbred mice. Hippocampus 16: 472-479.
27. Roman FS, Marchetti E, Bouquerel A, Soumireu-Mourat B (2002). The olfactory tubing maze: a new apparatus for studying learning and memory processes in mice. J Neurosci Methods 117: 173-181.
28. Skeberdis VA, Chevaleyre V, Lau CG, Goldberg JH, Pettit DL, Suadicani SO et al. (2006). Protein kinase A regulates calcium permeability of NMDA receptors. Nat Neurosci 9: 501-510.
29. Spencer JP, Brown JT, Richardson JC, Medhurst AD, Sehmi SS, Calver AR et al. (2004). Modulation of hippocampal excitability by 5-HT4 receptor agonists persists in a transgenic model of Alzheimer's disease. Neuroscience 129: 49-54.
30. Swanson LW, Wyss JM, Cowan WM (1978). An autoradiographic study of the organization of intrahippocampal association pathways in the rat. J Comp Neurol 181: 681-715.
31. Torres GE, Arfken CL, Andrade R (1996). 5-Hydroxytryptamine4 receptors reduce after hyperpolarization in hippocampus by inhibiting calcium-induced calcium release. Mol Pharmacol 50: 1316-1322.
32. Toth K, Freund TF (1992). Calbindin D28k-containing nonpyramidal cells in the rat hippocampus: their immunoreactivity for GABA and projection to the medial septum. Neuroscience 49: 793-805.
33. Tyler WJ, Pozzo-Miller L (2003). Miniature synaptic transmission and BDNF modulate dendritic spine growth and form in rat CA1 neurones. J Physiol 553: 497-509.
34. Tyler WJ, Pozzo-Miller LD (2001). BDNF enhances quantal neurotransmitter release and increases the number of docked vesicles at the active zones of hippocampal excitatory synapses. J Neurosci 21: 4249-4258.
35. White NM, McDonald RJ (2002). Multiple parallel memory systems in the brain of the rat. Neurobiol Learn Mem 77: 125-184.