Role of serotonin in memory impairment.

Buhot, Marie-Christine; Martin, Stéphanie; Segu, Louis

doi:10.3109/07853890008998828

Cited by 420Neurotransmitter Receptor Influence on BehaviorMemory and Neural MechanismsNeuroscience and Neuropharmacology Research

Role of serotonin in memory impairment.

Buhot, Marie-Christine, Martin, Stéphanie, Segu, Louis·2000·Annals of Medicine

DOI 10.3109/07853890008998828

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Abstract

As a result of its presence in various structures of the central nervous system serotonin (5-HT) plays a role in a great variety of behaviours such as food intake, activity rythms, sexual behaviour and emotional states. Despite this lack of functional specialization, the serotonergic system plays a significant role in learning and memory, in particular by interacting with the cholinergic, glutamatergic, dopaminergic or GABAergic systems. Its action is mediated via specific receptors located in crucial brain structures involved in these functions, primarily the septo-hippocampal complex and the nucleus basalis magnocellularis (NBM)-frontal cortex. Converging evidence suggests that the administration of 5-HT2A/2C or 5-HT4 receptor agonists or 5-HT1A or 5-HT3 and 5-HT1B receptor antagonists prevents memory impairment and facilitates learning in situations involving a high cognitive demand. In contrast, antagonists for 5-HT2A/2C and 5-HT4, or agonists for 5-HT1A or 5-HT3 and 5-HT1B generally have opposite effects. A better understanding of the role played by these and other serotonin receptor subtypes in learning and memory is likely to result from the recent availability of highly specific ligands, such as 5-HT1A, 5-HT1B, 5-HT2A receptor antagonists, and new molecular tools, such as gene knock-out mice, especially inducible mice in which a specific genetic alteration can be restricted both temporally and anatomically.

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Age‐related Cognitive Deficits in Rats Are Associated with a Combined Loss of Cholinergic and Serotonergic Functionsa
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WAY 100635, a 5-HT1A receptor antagonist, prevents the impairment of spatial learning caused by blockade of hippocampal NMDA receptors
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Effects of 5-HT3 Receptor Antagonism on Hippocampal Cellular Activity in the Freely Moving Rat
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Forebrain serotonin depletion facilitates the acquisition and performance of a conditional visual discrimination task in rats
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Strategies That Support Declining Cholinergic Neurotransmission in Alzheimer’s Disease Patients
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S 15535, a benzodioxopiperazine acting as presynaptic agonist and postsynaptic 5‐HT1A receptor antagonist, prevents the impairment of spatial learning caused by intrahippocampal scopolamine
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8-OH-DPAT-induced release of hippocampal noradrenaline in vivo: evidence for a role of both 5-HT1A and dopamine D1 receptors
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Combined treatment with a 5HT1A receptor agonist and a muscarinic acetylcholine receptor antagonist disrupts water maze navigation behavior
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Effect of destruction of the 5-hydroxytryptaminergic pathways on the acquisition of temporal discrimination and memory for duration in a delayed conditional discrimination task
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Differential Effects of Forebrain 5‐Hydroxytryptamine Depletions on Pavlovian Aversive Conditioning to Discrete and Contextual Stimuli in the Rat
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Systemic injection of p-chloroamphetamine eliminates the effect of the 5-HT3 compounds on learning
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Serotonin influences the behavioral recovery of rats following nucleus basalis lesions
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Effect of WAY-100135 on the hippocampal acetylcholine release potentiated by 8-OH-DPAT, a serotonin1A receptor agonist, in normal and p-chlorophenylalanine-treated rats as measured by in vivo microdialysis
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Blockade of 5-HT1A receptors compensates loss of hippocampal cholinergic neurotransmission involved in working memory of rats
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Different Effects of Tropisetron and Ondansetron in Learning and Memory Paradigms
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Serotonergic drug effects on a delayed conditional discrimination task in the rat; involvement of the 5-HT1A receptor in working memory
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Atypical antipsychotics block the excitatory effects of serotonin in septohippocampal neurons in the rat
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The Influence of Ondansetron and m-Chlorophenylpiperazine on Scopolamine-Induced Cognitive, Behavioral, and Physiological Responses in Young Healthy Controls
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Cortical localization in the tree shrew (Tupaia)
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Daily fluoxetine administration impairs avoidance learning in the rat without altering sensory thresholds
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Effects of the serotonin receptor agonists 8-OH-DPAT and TFMPP on learning as assessed using a novel water maze
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Serotonin 1B receptor regulation after dorsal subiculum deafferentation
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Some behavioural effects of risperidone in rats: comparison with haloperidol
Nowakowska, E., Chodera, A., Kus, K., & RYBAKOWSKI, J. K. (1999) · European Neuropsychopharmacology · doi:10.1016/s0924-977x(99)00021-8 · Cited by 28 · see citing works
Combined pCPA and muscarinic antagonist treatment produces a deficit in rat water maze acquisition
Harder, J. A., Kelly, M. E., Cheng, C. H. K., & Costall, B. (1996) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(96)00049-4 · Cited by 27 · see citing works
Cognitive implications for H3 and 5-HT3 receptor modulation of cortical cholinergic function: A parallel story
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Intrahippocampal grafts containing cholinergic and serotonergic fetal neurons ameliorate spatial reference but not working memory in rats with fimbria-fornix/cingular bundle lesions
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The decrease of serotonin release induced by a tryptophan-free amino acid diet does not affect spatial and passive avoidance learning
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Effect of Tryptophan Restriction on Short-Term Memory
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Buspirone impaired acquisition and retention in avoidance tasks: involvement of the hippocampus.
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Differential effects of 5-HT3 receptor antagonism on working memory failure due to deficiency of hippocampal cholinergic and glutamatergic transmission in rats
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Acquisition of Conditioned Inhibition in Rats is Impaired by Ablation of Serotoninergic Pathways
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The 5-HT3 receptor antagonist, RS-56812, enhances delayed matching performance in monkeys
Terry, A. V., Buccafusco, J. J., Prendergast, M., Jackson, W. J., Fontana, D. L., Wong, E. H. F., Whiting, R. L., & Eglen, R. M. (1996) · Neuroreport · doi:10.1097/00001756-199612200-00011 · Cited by 18 · see citing works
Responses to novelty stress in female F344 rats: Effects of age and d-fenfluramine treatment
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Impaired patterned responding in rats with electrolytic median raphe lesions
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Effect of the 5-HT1A agonist, 8-OH-DPAT on instrumental performance in rats
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Effects of ondansetron on short-term memory retrieval in mice.
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Memories are made of this: the genetic basis of memory
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The Effect of Several Putative Cognition Enhancers on a Water Maze Acquisition Deficit Produced by pCPA + Scopolamine Combination Treatment
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BDNF and 5-HT: a dynamic duo in age-related neuronal plasticity and neurodegenerative disorders
Mattson, M. P., Maudsley, S., & Martin, B. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.08.001 · Cited by 942 · see citing works
Influence of Tryptophan and Serotonin on Mood and Cognition with a Possible Role of the Gut-Brain Axis
Jenkins, T., Nguyen, J., Polglaze, K., & Bertrand, P. (2016) · Nutrients · doi:10.3390/nu8010056 · Cited by 904 · see citing works
Multi-target strategies for the improved treatment of depressive states: Conceptual foundations and neuronal substrates, drug discovery and therapeutic application
Millan, M. J. (2006) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2005.11.006 · Cited by 549 · see citing works
Acute psychological and physiological effects of psilocybin in healthy humans: a double-blind, placebo-controlled dose-effect study
Hasler, F., Grimberg, U., Benz, M. A., Huber, T., & Vollenweider, F. X. (2004) · Psychopharmacology · doi:10.1007/s00213-003-1640-6 · Cited by 451 · see citing works
5-HT Receptor Regulation of Neurotransmitter Release
Fink, K., & Göthert, M. (2007) · Pharmacological Reviews · doi:10.1124/pr.59.07103 · Cited by 389 · see citing works
The role of 5-HT1A receptors in learning and memory
Ögren, S. O., Eriksson, T. M., Elvander-Tottie, E., D’Addario, C., Ekstrom, J. C., Svenningsson, P., Meister, B., Kehr, J., & Stiedl, O. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.02.023 · Cited by 341 · see citing works
A Sleep-Promoting Role for the Drosophila Serotonin Receptor 1A
Yuan, Q., Joiner, W. J., & Sehgal, A. (2006) · Current Biology · doi:10.1016/j.cub.2006.04.032 · Cited by 301 · see citing works
Vortioxetine (Lu AA21004), a novel multimodal antidepressant, enhances memory in rats
Mørk, A., Montezinho, L. P., Miller, S., Trippodi-Murphy, C., Plath, N., Li, Y., Gulinello, M. E., & Sánchez, C. (2013) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2013.01.019 · Cited by 298 · see citing works
Beyond happiness: Building a science of discrete positive emotions.
Shiota, M. N., Campos, B., Oveis, C., Hertenstein, M. J., Simon-Thomas, E. R., & Keltner, D. J. (2017) · American Psychologist · doi:10.1037/a0040456 · Cited by 279 · see citing works
Dopamine and Memory: Modulation of the Persistence of Memory for Novel Hippocampal NMDA Receptor-Dependent Paired Associates
Bethus, I., Tse, D., & Morris, R. G. M. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.2721-09.2010 · Cited by 270 · see citing works
Traditional uses, phytochemistry and pharmacology of Ficus religiosa: A review
Singh, D., Singh, B., & Goel, R. K. (2011) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2011.01.046 · Cited by 269 · see citing works
The serotonergic system in ageing and Alzheimer's disease
Rodriguez, J. J., Noristani, H. N., & Verkhratsky, A. (2012) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2012.06.010 · Cited by 266 · see citing works
Serotonin Modulates Circadian Entrainment in Drosophila
Yuan, Q., Lin, F., Zheng, X., & Sehgal, A. (2005) · Neuron · doi:10.1016/j.neuron.2005.05.027 · Cited by 262 · see citing works
Serotonin and Human Cognitive Performance
Schmitt, J. A. J., Wingen, M., Ramaekers, J. G., Evers, E. A. T., & Riedel, W. J. (2006) · Current Pharmaceutical Design · doi:10.2174/138161206777698909 · Cited by 258 · see citing works
The 5-HT3receptor as a therapeutic target
Thompson, A. J., & Lummis, S. C. R. (2007) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.11.4.527 · Cited by 258 · see citing works
Cholinergic–serotonergic imbalance contributes to cognitive and behavioral symptoms in Alzheimer's disease
Garcia-Alloza, M., Gil-Bea, F. J., Diez-Ariza, M., Chen, C. P. L.-H., Francis, P. T., Lasheras, B., & Ramirez, M. J. (2005) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2004.06.007 · Cited by 244 · see citing works
Dopaminergic modulation of the persistence of one-trial hippocampus-dependent memoryPreprint
O’Carroll, C., Martin, S. J., Sandin, J., Frenguelli, B. G., & Morris, R. G. M. (2006) · Learning & Memory · doi:10.1101/lm.321006 · Cited by 237 · see citing works
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The medical benefit of 5-HT research
Jones, B. J., & Blackburn, T. P. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(01)00745-6 · Cited by 227 · see citing works
Sleep and memory: a molecular perspective
Graves, L. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01744-6 · Cited by 216 · see citing works
Conserved role for the serotonin transporter gene in rat and mouse neurobehavioral endophenotypes
Kalueff, A. V., Olivier, J. D. A., Nonkes, L. J. P., & Homberg, J. R. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.08.003 · Cited by 203 · see citing works
Ghrelin in Central Neurons
Ferrini, F., Salio, C., Lossi, L., & Merighi, A. (2009) · Current Neuropharmacology · doi:10.2174/157015909787602779 · Cited by 197 · see citing works
Neurotoxicity of methylenedioxyamphetamines (MDMA; ecstasy) in humans: how strong is the evidence for persistent brain damage?
Gouzoulis‐Mayfrank, E., & Daumann, J. (2006) · Addiction · doi:10.1111/j.1360-0443.2006.01314.x · Cited by 189 · see citing works
Bipolar Disorder and Inflammation
Rosenblat, J. D., & McIntyre, R. S. (2016) · Psychiatric Clinics of North America · doi:10.1016/j.psc.2015.09.006 · Cited by 186 · see citing works
Differentiating antidepressants of the future: Efficacy and safety
Rosenzweig-Lipson, S. J., Beyer, C. E., Hughes, Z. A., Khawaja, X. Z., Rajarao, S. J. R., Malberg, J. E., Rahman, Z. U., Ring, R. H., & Schechter, L. E. (2006) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2006.07.002 · Cited by 182 · see citing works
Inflammation as a neurobiological substrate of cognitive impairment in bipolar disorder: Evidence, pathophysiology and treatment implications
Rosenblat, J. D., Brietzke, E., Mansur, R. B., Maruschak, N. A., Lee, Y., & McIntyre, R. S. (2015) · Journal of Affective Disorders · doi:10.1016/j.jad.2015.08.058 · Cited by 172 · see citing works
Serotonin transporter polymorphism, memory and hippocampal volume in the elderly: association and interaction with cortisol
O'Hara, R., Schröder, C. M., Mahadevan, R., Schatzberg, A. F., Lindley, S., Fox, S., Weiner, M., Kraemer, H. C., Noda, A., Lin, X., et al. (2007) · Molecular Psychiatry · doi:10.1038/sj.mp.4001978 · Cited by 171 · see citing works
Neotic preferences in laboratory rodents: Issues, assessment and substrates
Hughes, R. N. (2007) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2006.11.004 · Cited by 160 · see citing works
Stimulation of Neurogenesis and Synaptogenesis by Bilobalide and Quercetin via Common Final Pathway in Hippocampal Neurons
Tchantchou, F., Lacor, P. N., Cao, Z., Lao, L., Hou, Y., Cui, C., Klein, W. L., & Luo, Y. (2009) · Journal of Alzheimer s Disease · doi:10.3233/jad-2009-1189 · Cited by 163 · see citing works
Aerobic Exercise as a Tool to Improve Hippocampal Plasticity and Function in Humans: Practical Implications for Mental Health Treatment
Kandola, A., Hendrikse, J., Lucassen, P. J., & Yücel, M. (2016) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2016.00373 · Cited by 155 · see citing works
Differential Involvement of 5-HT1B/1D and 5-HT6 Receptors in Cognitive and Non-cognitive Symptoms in Alzheimer's Disease
Garcı́a-Alloza, M., Hirst, W. D., Chen, C., Lasheras, B., Francis, P. T., & Ramírez, M. J. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300330 · Cited by 151 · see citing works
Neuroactive steroid effects on cognitive functions with a focus on the serotonin and GABA systems
Birzniece, V., Bäckström, T. C., Johansson, I., Lindblad, C., Lundgren, P., Löfgren, M., Olsson, T., Ragagnin, G., Taube, M., Türkmen, Ş., et al. (2005) · Brain Research Reviews · doi:10.1016/j.brainresrev.2005.11.001 · Cited by 150 · see citing works
Memory impairment suggests hippocampal dysfunction in abstinent ecstasy users
Gouzoulis‐Mayfrank, E., Thimm, B., Rezk, M., Hensen, G., & Daumann, J. (2003) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/s0278-5846(03)00114-3 · Cited by 148 · see citing works
The Selective 5-HT6 Receptor Antagonist Ro4368554 Restores Memory Performance in Cholinergic and Serotonergic Models of Memory Deficiency in the Rat
Lieben, C. K. J., Blokland, A., Şık, A., Sung, E., van Nieuwenhuizen, P., & Schreiber, R. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300777 · Cited by 148 · see citing works
DARK Classics in Chemical Neuroscience: Psilocybin
Geiger, H. A., Wurst, M. G., & Daniels, R. N. (2018) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.8b00186 · Cited by 142 · see citing works
Of Minds and Embryos: Left-Right Asymmetry and the Serotonergic Controls of Pre-Neural Morphogenesis
Levin, M. G., Buznikov, G. A., & Lauder, J. M. (2006) · Developmental Neuroscience · doi:10.1159/000091915 · Cited by 137 · see citing works
Enhanced contextual fear memory in central serotonin-deficient mice
Dai, J., Han, H., Tian, M., Cao, J., Xiu, J., Song, N., Huang, Y., Xu, T., Ding, Y., & Xu, L. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0801329105 · Cited by 133 · see citing works
The age-dependent effects of selective serotonin reuptake inhibitors in humans and rodents: a review
Olivier, J. D. A., Blom, T., Arentsen, T., & Homberg, J. R. (2011) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2010.09.013 · Cited by 131 · see citing works
Activation of 5-HT7 Serotonin Receptors Reverses Metabotropic Glutamate Receptor-Mediated Synaptic Plasticity in Wild-Type and Fmr1 Knockout Mice, a Model of Fragile X Syndrome
Costa, L., Spatuzza, M., D’Antoni, S., Bonaccorso, C. M., Trovato, C., Musumeci, S. A., Leopoldo, M., Lacivita, E., Catania, M. V., & Ciranna, L. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.06.008 · Cited by 129 · see citing works
Neurophysiological symptoms and aspartame: What is the connection?
Choudhary, A. K., & Lee, Y. Y. (2017) · Nutritional Neuroscience · doi:10.1080/1028415x.2017.1288340 · Cited by 127 · see citing works
Drug targets for cognitive enhancement in neuropsychiatric disorders.
Wallace, T. L., Ballard, T. M., Pouzet, B., Riedel, W. J., & Wettstein, J. G. (2011) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2011.03.022 · Cited by 127 · see citing works
The 5-HT7 receptor is involved in allocentric spatial memory information processing
Sarkisyan, G., & Hedlund, P. B. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.03.011 · Cited by 126 · see citing works
G-Protein-Coupled Receptors in CNS: A Potential Therapeutic Target for Intervention in Neurodegenerative Disorders and Associated Cognitive Deficits
Azam, S., Haque, M. E., Jakaria, M., Jo, S.-H., Kim, I., & Choi, D. (2020) · Cells · doi:10.3390/cells9020506 · Cited by 124 · see citing works
REM sleep deprivation affects extinction of cued but not contextual fear conditioning
Silvestri, A. J. (2005) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.11.011 · Cited by 124 · see citing works
Inhibitory Effect of Hippocampal 5-HT1A Receptors on Human Explicit Memory
Yasuno, F., Suhara, T., Nakayama, T., Ichimiya, T., Okubo, Y., Takano, A., Ando, T., Inoue, M., Maeda, J., & Suzuki, K. (2003) · American Journal of Psychiatry · doi:10.1176/appi.ajp.160.2.334 · Cited by 123 · see citing works
Cognitive dysfunction in neuropsychiatric disorders: Selected serotonin receptor subtypes as therapeutic targets
Terry, A. V., Buccafusco, J. J., & Wilson, C. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.12.006 · Cited by 122 · see citing works
5-HT3 Receptor Antagonism: A Potential Therapeutic Approach for the Treatment of Depression and other Disorders
Bhatt, S., Devadoss, T., Manjula, S. N., & Rajangam, J. (2021) · Current Neuropharmacology · doi:10.2174/1570159x18666201015155816 · Cited by 119 · see citing works
Cholinergic connectivity: it's implications for psychiatric disorders
Scarr, E., Gibbons, A. S., Neo, J. H., Udawela, M., & Dean, B. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00055 · Cited by 117 · see citing works
Ameliorative effect of Curcumin on seizure severity, depression like behavior, learning and memory deficit in post-pentylenetetrazole-kindled mice
Choudhary, K. M., Mishra, A., Poroikov, V., & Goel, R. K. (2013) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2013.02.012 · Cited by 119 · see citing works
Role of Serotonin in Alzheimerʼs Disease: A New Therapeutic Target?
Geldenhuys, W. J., & Van der Schyf, C. J. (2011) · CNS Drugs · doi:10.2165/11590190-000000000-00000 · Cited by 117 · see citing works
Major depression, cognitive dysfunction and Alzheimer's disease: Is there a link?
Sierksma, A. S. R., van den Hove, D. L. A., Steinbusch, H. W. M., & Prickaerts, J. (2010) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2009.10.021 · Cited by 139 · see citing works
The 5-HT1B receptor - a potential target for antidepressant treatment
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Authors: Buhot, M.-C., Martin, S., & Segu, L.
Affiliations: Centre National de la Recherche Scientifique (FR)
Corresponding author: Buhot, Marie-Christine
Venue: Annals of Medicine
Publisher: Informa UK Limited
Published: 2000-01
Volume: 32
Issue: 3
Pages: 210-221
ISSN: 0785-3890 (ISSN-L)
1365-2060
DOI: 10.3109/07853890008998828
OpenAlex: W1973475326
Cited by: 419
References: 123
Citations by year: 2026: 4 · 2025: 8 · 2024: 13 · 2023: 12 · 2022: 9 · 2021: 19 · 2020: 15 · 2019: 14 · 2018: 8 · 2017: 11 · 2016: 13 · 2015: 8 · 2014: 19 · 2013: 18 · 2012: 15
FWCI: 6.29
Type: journal article
Language: en
Open access: closed
Locations: Annals of Medicine (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: serotonin, serotonin receptors, memory impairment, learning, 5-HT2A/2C receptors, 5-HT4 receptor, 5-HT1A receptor, 5-HT3 receptor, 5-HT1B receptor, serotonergic system, nucleus basalis magnocellularis, cholinergic system, glutamatergic system, dopaminergic system, GABAergic system, inducible knockout mice
MeSH terms: Aging, Alzheimer Disease, Animals, Brain, Cognition, Humans, Limbic System, Memory Disorders, Receptors, Serotonin, Serotonin, Mice, Knockout, Mice

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