The 5-HT4 receptor levels in hippocampus correlates inversely with memory test performance in humans

Human Brain Mapping

Volumn 34, Issue 11, 2013, Pages 3066-3074

  Haahr, Mette Ewers ^a,c   Fisher, Patrick ^a,c   Holst, Klaus ^a,b,c   Madsen, Karine ^a,c   Jensen, Christian Gaden ^a,c   Marner, Lisbeth ^a,c   Lehel, Szabols ^a,c   Baaré, William ^a,c   Knudsen, Gitte ^a,c   Hasselbalch, Steen ^a,c  

^a International Center for Research and Research Training in Endocrine Disruption of Male Reproduction and Child Health   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c HVIDOVRE HOSPITAL   (Denmark)

Author keywords

Cerebral 5 HT4 receptor; Hippocampus; Human experimentation; Memory; Positron Emission Tomography; Reys Auditory Verbal Learning Test

Indexed keywords

SB 207145 C 11; SEROTONIN 4 RECEPTOR; TRACER; UNCLASSIFIED DRUG;

ADULT; ARTICLE; BRAIN LEVEL; FEMALE; GRAY MATTER; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; MALE; MEMORY; MEMORY ACQUISITION; MEMORY CONSOLIDATION; MENTAL PERFORMANCE; MENTAL TEST; NORMAL HUMAN; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RECALL; RESPONSE TIME; REY OSTERRIETH COMPLEX FIGURE TEST; REYS AUDITORY VERBAL LEARNING TEST; SCORING SYSTEM; ALGORITHM; BRAIN MAPPING; CEREBRAL 5-HT4 RECEPTOR; EPISODIC MEMORY; HEMISPHERIC DOMINANCE; HISTOLOGY; IMAGE PROCESSING; LEARNING; METABOLISM; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE; SCINTISCANNING; STATISTICAL ANALYSIS; YOUNG ADULT;

CEREBRAL 5-HT4 RECEPTOR; HIPPOCAMPUS; HUMAN EXPERIMENTATION; MEMORY; POSITRON EMISSION TOMOGRAPHY; REYS AUDITORY VERBAL LEARNING TEST;

ADULT; ALGORITHMS; BRAIN MAPPING; DATA INTERPRETATION, STATISTICAL; FEMALE; FUNCTIONAL LATERALITY; HIPPOCAMPUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; LEARNING; MAGNETIC RESONANCE IMAGING; MALE; MEMORY, EPISODIC; MENTAL RECALL; NEUROPSYCHOLOGICAL TESTS; POSITRON-EMISSION TOMOGRAPHY; PSYCHOMOTOR PERFORMANCE; RECEPTORS, SEROTONIN, 5-HT4; VERBAL LEARNING; YOUNG ADULT;

EID: 84886305113     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.22123     Document Type: Article

References (70)

1. Amthauer R (2001): Intelligenz-Struktur-Test 2000. R. Hogrefe.
2. Andrade R, Chaput Y (1991): 5-Hydroxytryptamine4-like receptors mediate the slow excitatory response to serotonin in the rat hippocampus. J Pharmacol Exp Ther 257:930-937.
3. Bianchi C, Rodi D, Marino S, Beani L, Siniscalchi A (2002): Dual effects of 5-HT4 receptor activation on GABA release from guinea pig hippocampal slices. Neuroreport 13:2177-2180.
4. Bockaert J, Claeysen S, Becamel C, Dumuis A, Marin P (2006): Neuronal 5-HT metabotropic receptors: Fine-tuning of their structure, signaling, and roles in synaptic modulation. Cell Tissue Res 326:553-572.
5. Bockaert J, Claeysen S, Compan V, Dumuis A (2004): 5-HT4 receptors. Curr Drug Targets CNS Neurol Disord 3:39-51.
6. Buhot MC, Martin S, Segu L (2000): Role of serotonin in memory impairment. Ann Med 32:210-221.
7. Cifariello A, Pompili A, Gasbarri A (2008): 5-HT(7) receptors in the modulation of cognitive processes. Behav Brain Res 195:171-179.
8. Cipolotti L, Bird CM (2006): Amnesia and the hippocampus. Curr Opin Neurol 19:593-598.
9. Compan V, Charnay Y, Dusticier N, Daszuta A, Hen R, Bockaert J (2004): [Feeding disorders in 5-HT4 receptor knockout mice]. J Soc Biol 198:37-49.
10. Compan V, Jean A, Laurent L, Aribo O, Malapris C, Dantec C, Barrot M, Neve RL, Dusticier N, Nieoullon A, Hen R, Bockaert J (2010): Anorexia coexists with psychoactive and rewarding effects when meidated by serotonin 4 receptors in the nucleus accembens (abstract). Society for Neuroscience, Annual Meeting, San Diego, California Online:299.2/JJJ32.
11. Comtat C (2008): Image based resolution modeling for the HRRT OSEM reconstructions software. IEEE MIC Conf. Rec, Dresden.
12. Cools R, D'Esposito M (2011): Inverted-U-shaped dopamine actions on human working memory and cognitive control. Biol Psychiatry 69:e113-e125.
13. Desgranges B, Baron JC, Eustache F (1998): The functional neuroanatomy of episodic memory: The role of the frontal lobes, the hippocampal formation, and other areas. Neuroimage 8:198-213.
14. Dumont GJ, de Visser SJ, Cohen AF, van Gerven JM (2005): Biomarkers for the effects of selective serotonin reuptake inhibitors (SSRIs) in healthy subjects. Br J Clin Pharmacol 59:495-510.
15. Fagni L, Dumuis A, Sebben M, Bockaert J (1992): The 5-HT4 receptor subtype inhibits K+ current in colliculi neurones via activation of a cyclic AMP-dependent protein kinase. Br J Pharmacol 105:973-979.
16. Fanselow MS, Dong HW (2010): Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65:7-19.
17. Francis HM, Kraushaar NJ, Hunt LR, Cornish JL (2011): Serotonin 5-HT4 receptors in the nucleus accumbens are specifically involved in the appetite suppressant and not locomotor stimulant effects of MDMA ('ecstasy'). Psychopharmacology (Berl) 213:355-363.
18. Frautschy SA, Cole GM (2010): Why pleiotropic interventions are needed for Alzheimer's disease. Mol Neurobiol 41( 2-3):392-409.
19. Galeotti N, Ghelardini C, Bartolini A (1998): Role of 5-HT4 receptors in the mouse passive avoidance test. J Pharmacol Exp Ther 286:1115-1121.
20. Ge J, Barnes NM (1996): 5-HT4 receptor-mediated modulation of 5-HT release in the rat hippocampus in vivo. Br J Pharmacol 117:1475-1480.
21. Gee AD, Martarello L, Passchier M (2008): Synthesis and evaluation of [11C]SB207145 as the first in vivo serotonin 5-HT4 receptor radioligand for PET imaging in man. Curr Radiopharma 110-114.
22. Gillings N, Larsen P (2005): A highly flexible modular radiochemistry system [abstract]. J Label Comp Radiopharm 48 (Suppl):338.
23. Gunn RN, Lammertsma AA, Hume SP, Cunningham VJ (1997): Parametric imaging of ligand-receptor binding in PET using a simplified reference region model. Neuroimage 6:279-287.
24. Jean A, Conductier G, Manrique C, Bouras C, Berta P, Hen R, Charnay Y, Bockaert J, Compan V (2007): Anorexia induced by activation of serotonin 5-HT4 receptors is mediated by increases in CART in the nucleus accumbens. Proc Natl Acad Sci USA 104:16335-16340.
25. Jovicich J, Czanner S, Greve D, Haley E, van der Kouwe A, Gollub R, Kennedy D, Schmitt F, Brown G, Macfall J, Fischl B, Dale A (2006): Reliability in multi-site structural MRI studies: Effects of gradient non-linearity correction on phantom and human data. Neuroimage 30:436-443.
26. Kemp A, Manahan-Vaughan D (2004): Hippocampal long-term depression and long-term potentiation encode different aspects of novelty acquisition. Proc Natl Acad Sci USA 101:8192-8197.
27. King MV, Marsden CA, Fone KC (2008): A role for the 5-HT(1A), 5-HT4 and 5-HT6 receptors in learning and memory. Trends Pharmacol Sci 29:482-492.
28. 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.
29. Lamirault L, Simon H (2001): Enhancement of place and object recognition memory in young adult and old rats by RS 67333, a partial agonist of 5-HT4 receptors. Neuropharmacology 41:844-853.
30. Lammertsma AA, Hume SP (1996): Simplified reference tissue model for PET receptor studies. Neuroimage 4( Part 1):153-158.
31. Lelong V, Dauphin F, Boulouard M (2001): RS 67333 and D-cycloserine accelerate learning acquisition in the rat. Neuropharmacology 41:517-522.
32. Letty S, Child R, Dumuis A, Pantaloni A, Bockaert J, Rondouin G (1997): 5-HT4 receptors improve social olfactory memory in the rat. Neuropharmacology 36( 4-5):681-687.
33. Lezak M, Howieson DB, Loring DW, Hannay HJ, Fischer JS (2004): Neuropsychological Assessment. Oxford: Oxford University Press.
34. Licht CL, Knudsen GM, Sharp T (2010): Effects of the 5-HT(4) receptor agonist RS67333 and paroxetine on hippocampal extracellular 5-HT levels. Neurosci Lett 476:58-61.
35. Licht CL, Marcussen AB, Wegener G, Overstreet DH, Aznar S, Knudsen GM (2009): The brain 5-HT4 receptor binding is down-regulated in the Flinders Sensitive Line depression model and in response to paroxetine administration. J Neurochem 109:1363-1374.
36. Madsen K, Marner L, Haahr M, Gillings N, Knudsen GM (2010a): Age and sex effects on 5-HT4 receptors in the human brain-A [11C]SB207145 PET study. J Cerebral Blood Flow Metabolism.
37. Madsen K, Neumann WJ, Holst K, Marner L, Haahr MT, Lehel S, Knudsen GM, Hasselbalch SG (2011): Cerebral serotonin 4 receptors and amyloid-beta in early Alzheimer's disease. J Alzheimers Dis 26:457-466.
38. Madsen K, Erritzoe D, Mortensen EL, Gade A, Madsen J, Baare W, Knudsen GM, Hasselbalch SG (2011): Cognitive function is related to fronto-striatal serotonin transporter levels-A brain PET study in young healthy subjects. Psychopharmacology (Berl) 213( 2-3):573-581.
39. Maldjian JA, Laurienti PJ, Burdette JH (2004): Precentral gyrus discrepancy in electronic versions of the Talairach atlas. Neuroimage 21:450-455.
40. Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003): An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19:1233-1239.
41. Manuel-Apolinar L, Rocha L, Pascoe D, Castillo E, Castillo C, Meneses A (2005): Modifications of 5-HT4 receptor expression in rat brain during memory consolidation. Brain Res 1042:73-81.
42. 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.
43. 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.
44. Marchetti-Gauthier E, Roman FS, Dumuis A, Bockaert J, Soumireu-Mourat B (1997): BIMU1 increases associative memory in rats by activating 5-HT4 receptors. Neuropharmacology 36( 4-5):697-706.
45. Marner L, Gillings N, Comley RA, Baare WF, Rabiner EA, Wilson AA, Houle S, Hasselbalch SG, Svarer C, Gunn RN, Laruelle M, Knudsen GM (2009): Kinetic modeling of 11C-SB207145 binding to 5-HT4 receptors in the human brain in vivo. J Nucl Med 50:900-908.2009.
46. Marner L, Gillings N, Madsen K, Erritzoe D, Baare WF, Svarer C, Hasselbalch SG, Knudsen GM (2010): Brain imaging of serotonin 4 receptors in humans with [11C]SB207145-PET. Neuroimage 50:855-861.
47. Matsumoto M, Togashi H, Mori K, Ueno K, Ohashi S, Kojima T, Yoshioka M (2001): Evidence for involvement of central 5-HT(4) receptors in cholinergic function associated with cognitive processes: Behavioral, electrophysiological, and neurochemical studies. J Pharmacol Exp Ther 296:676-682.
48. Mendelsohn D, Riedel WJ, Sambeth A (2009): Effects of acute tryptophan depletion on memory, attention and executive functions: A systematic review. Neurosci Biobehav Rev 33:926-952.
49. Meneses A, Hong E (1997): Effects of 5-HT4 receptor agonists and antagonists in learning. Pharmacol Biochem Behav 56:347-351.
50. Mlinar B, Mascalchi S, Mannaioni G, Morini R, Corradetti R (2006): 5-HT4 receptor activation induces long-lasting EPSP-spike potentiation in CA1 pyramidal neurons. Eur J Neurosci 24:719-731.
51. Mohler EG, Shacham S, Noiman S, Lezoualc'h F, Robert S, Gastineau M, Rutkowski J, Marantz Y, Dumuis A, Bockaert J, Gold PE, Ragozzino ME (2007): VRX-03011, a novel 5-HT4 agonist, enhances memory and hippocampal acetylcholine efflux. Neuropharmacology 53:563-573.
52. Neubauer AC, Grabner RH, Fink A, Neuper C (2005): Intelligence and neural efficiency: Further evidence of the influence of task content and sex on the brain-IQ relationship. Brain Res Cogn Brain Res 25:217-225.
53. Nyberg L, Persson J, Habib R, Tulving E, McIntosh AR, Cabeza R, Houle S (2000): Large scale neurocognitive networks underlying episodic memory. J Cogn Neurosci 12:163-173.
54. Olesen O, Sibomana M, Keller S, Andersen F, Jensen J, Holm S, Svarer C, Hjgaard L (2009): Spatial resolution of the HRRT PET scanner using 3D-OSEM PSF reconstruction. IEEE MIC Record, Orlando.
55. Perez-Garcia G, Meneses A (2008): Memory formation, amnesia, improved memory and reversed amnesia: 5-HT role. Behav Brain Res 195:17-29.
56. Sambeth A, Blokland A, Harmer CJ, Kilkens TO, Nathan PJ, Porter RJ, Schmitt JA, Scholtissen B, Sobczak S, Young AH, Riedel WJ (2007): Sex differences in the effect of acute tryptophan depletion on declarative episodic memory: A pooled analysis of nine studies. Neurosci Biobehav Rev 31:516-529.
57. Schmitt JA, Wingen M, Ramaekers JG, Evers EA, Riedel WJ (2006): Serotonin and human cognitive performance. Curr Pharm Des 12:2473-2486.
58. Sled JG, Zijdenbos AP, Evans AC (1998): A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging 17:87-97.
59. Sureau FC, Reader AJ, Comtat C, Leroy C, Ribeiro MJ, Buvat I, Trebossen R (2008): Impact of image-space resolution modeling for studies with the high-resolution research tomograph. J Nucl Med 49:1000-1008.
60. Svarer C, Madsen K, Hasselbalch SG, Pinborg LH, Haugbol S, Frokjaer VG, Holm S, Paulson OB, Knudsen GM (2005): MR-based automatic delineation of volumes of interest in human brain PET images using probability maps. Neuroimage 24:969-979.
61. Terry AV, Jr., Buccafusco JJ, Jackson WJ, Prendergast MA, Fontana DJ, Wong EH, Bonhaus DW, Weller P, Eglen RM (1998): Enhanced delayed matching performance in younger and older macaques administered the 5-HT4 receptor agonist, RS 17017. Psychopharmacology (Berl) 135:407-415.
62. Tobin J (1958): Estimation of relationships for limited dependent variables. Econometrica 26:24-36.
63. Torres GE, Arfken CL, Andrade R (1996): 5-Hydroxytryptamine4 receptors reduce afterhyperpolarization in hippocampus by inhibiting calcium-induced calcium release. Mol Pharmacol 50:1316-1322.
64. Uttl B (2005): Measurement of individual differences: Lessons from memory assessment in research and clinical practice. Psychol Sci 16:460-467.
65. Vakil E, Greenstein Y, Blachstein H (2010): Normative data for composite scores for children and adults derived from the Rey Auditory Verbal Learning Test. Clin Neuropsychol 24:662-677.
66. Van der Elst W, van Boxtel MP, van Breukelen GJ, Jolles J (2005): Rey's verbal learning test: Normative data for 1855 healthy participants aged 24-81 years and the influence of age, sex, education, and mode of presentation. J Int Neuropsychol Soc 11:290-302.
67. Veall MT, Zimmermann KF (1994): Goodness of fit measures in the Tobit Model. Oxford Bull Econ Stat 56:485-499.
68. Vidal R, Valdizan EM, Mostany R, Pazos A, Castro E (2009): Long-term treatment with fluoxetine induces desensitization of 5-HT4 receptor-dependent signalling and functionality in rat brain. J Neurochem 110:1120-1127.
69. Vilaro MT, Cortes R, Mengod G (2005): Serotonin 5-HT4 receptors and their mRNAs in rat and guinea pig brain: Distribution and effects of neurotoxic lesions. J Comp Neurol 484:418-439.
70. Waeber C, Sebben M, Bockaert J, Dumuis A (1996): Regional distribution and ontogeny of 5-HT4 binding sites in rat brain. Behav Brain Res 73( 1-2):259-262.