Nicotinic modulation of glutamatergic synaptic transmission in region CA3 of the hippocampus
Abstract
Cholinergic modulation of synaptic transmission in the hippocampus appears to be involved in learning, memory and attentional processes. In brain slice preparations of hippocampal region CA3, we have explored the effect of nicotine on the afferent connections of stratum lacunosum moleculare (SLM) vs. the intrinsic connections of stratum radiatum (SR). Nicotine application had a lamina‐selective effect, causing changes in synaptic transmission only in SLM. The nicotinic effect in SLM was characterized by a transient decrease in synaptic potential size followed by a longer period of enhancement of synaptic transmission. The effect was blocked by γ‐aminobutyric acid (GABA)ergic antagonists, indicating the role of GABAergic interneurons in the observed nicotinic effect. The biphasic nature of the nicotinic effect could be due to a difference in receptor subtypes, as supported by the effects of the nicotinic antagonists mecamylamine and methyllycaconitine. Nicotinic modulation of glutamatergic synaptic transmission could complement muscarinic suppression of intrinsic connections, amplifying incoming information and providing a physiological mechanism for the memory‐enhancing effect of nicotine.
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Nicotinic receptor activation enhances the influence of afferent synaptic input in the hippocampus, including glutamatergic input to interneurons.
“Similar to thalamic input to neocortex, nicotinic receptor activation enhances the influence of afferent synaptic input in the hippocampus (Radcliffe and Dani, 1998; Giocomo and Hasselmo, 2005) including glutamatergic input to interneurons (Alkondon and Albuquerque, 2002).”
From Modes and models of forebrain cholinergic neuromodulation of cognition (2011) · cites this paper as Giocomo and Hasselmo, 2005
Cites
Physiological Diversity of Nicotinic Acetylcholine Receptors Expressed by Vertebrate Neurons
McGehee, D. S., & Role, L. W. (1995) · Annual Review of Physiology · doi:10.1146/annurev.ph.57.030195.002513 · Cited by 1,022 · see citing works
Hippocampal synaptic transmission enhanced by low concentrations of nicotine
Gray, R. G. F., Rajan, A. S., Radcliffe, K. A., Yakehiro, M., & Dani, J. A. (1996) · Nature · doi:10.1038/383713a0 · Cited by 947 · see citing works
Neuromodulation: acetylcholine and memory consolidation
Hasselmo, M. E. (1999) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(99)01365-0 · Cited by 809 · see citing works
Self-citationNicotinic acetylcholine involvement in cognitive function in animals
Levin, E. D., & Simon, B. B. (1998) · Psychopharmacology · doi:10.1007/s002130050667 · Cited by 675 · see citing works
Klink, R., d'Exaerde, A. D. K., Zoli, M., & Changeux, J.-P. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-05-01452.2001 · Cited by 674 · see citing works
Differential regulation of neocortical synapses by neuromodulators and activity
Gil, Z., Connors, B. W., & Amitai, Y. (1997) · Neuron · doi:10.1016/s0896-6273(00)80380-3 · Cited by 553 · see citing works
Alkondon, M., & Albuquerque, E. X. (1993) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)38283-2 · Cited by 538 · see citing works
Hasselmo, M., & Schnell, E. (1994) · The Journal of Neuroscience · doi:10.1523/jneurosci.14-06-03898.1994 · Cited by 466 · see citing works
Self-citationHasselmo, M. E., Schnell, E., & Barkai, E. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-07-05249.1995 · Cited by 463 · see citing works
Self-citationAlbuquerque, E. X., Alkondon, M., Pereira, E. F. R., Castro, N. G., Schrattenholz, A. S., Barbosa, C. T. F., Bonfante-Cabarcas, R. A., Aracava, Y., Eisenberg, H. M., & Maelicke, A. (1997) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)36503-6 · Cited by 436 · see citing works
Timing and Location of Nicotinic Activity Enhances or Depresses Hippocampal Synaptic Plasticity
Ji, D., Lape, R., & Dani, J. A. (2001) · Neuron · doi:10.1016/s0896-6273(01)00332-4 · Cited by 419 · see citing works
Le Novere, N., Zoli, M., & Changeux, J. (1996) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1996.tb01206.x · Cited by 385 · see citing works
Hasselmo, M. E., & Bower, J. M. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.67.5.1222 · Cited by 358 · see citing works
Self-citationTransdermal nicotine effects on attention
Levin, E. D., Conners, C. K., Silva, D., Hinton, S. C., Meck, W. H., March, J. S., & Rose, J. E. (1998) · Psychopharmacology · doi:10.1007/s002130050750 · Cited by 331 · see citing works
Frazier, C. J., Buhler, A. V., Weiner, J. L., & Dunwiddie, T. V. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-20-08228.1998 · Cited by 329 · see citing works
Functional nicotinic ACh receptors on interneurones in the rat hippocampus
Jones, S., & Yakel, J. L. (1997) · The Journal of Physiology · doi:10.1111/j.1469-7793.1997.603bd.x · Cited by 271 · see citing works
Nicotinic Stimulation Produces Multiple Forms of Increased Glutamatergic Synaptic Transmission
Radcliffe, K. A., & Dani, J. A. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-18-07075.1998 · Cited by 271 · see citing works
Nicotinic System Involvement in Alzheimer??s and Parkinson??s Diseases
NEWHOUSE, P. A., Potter, A., & Levin, E. D. (1997) · Drugs & Aging · doi:10.2165/00002512-199711030-00005 · Cited by 266 · see citing works
Vidal, C., & Changeux, J. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90558-w · Cited by 240 · see citing works
Alkondon, M., & Albuquerque, E. X. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.86.6.3043 · Cited by 240 · see citing works
Nicotinic Receptor Activation Excites Distinct Subtypes of Interneurons in the Rat Hippocampus
McQuiston, A. R., & Madison, D. V. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-08-02887.1999 · Cited by 239 · see citing works
Ji, D., & Dani, J. A. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.5.2682 · Cited by 231 · see citing works
Everitt, B. J., Robbins, T. W., & Muir, J. L. (1995) · Psychopharmacology · doi:10.1007/bf02245253 · Cited by 214 · see citing works
Freedman, R., Wetmore, C., Strömberg, I., Leonard, S. S., & Olson, L. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-05-01965.1993 · Cited by 202 · see citing works
Acute and chronic nicotine exposure differentially facilitate the induction of LTP
Fujii, S., Ji, Z., Morita, N., & Sumikawa, K. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01982-4 · Cited by 200 · see citing works
Alkondon, M., & Albuquerque, E. X. (2004) · Progress in brain research · doi:10.1016/s0079-6123(03)45007-3 · Cited by 197 · see citing works
Gioanni, Y., Rougeot, C., Clarke, P. B. S., Lepousé, C., Thierry, A. M., & Vidal, C. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00403.x · Cited by 191 · see citing works
Aramakis, V. B., & Metherate, R. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-20-08485.1998 · Cited by 182 · see citing works
Hsieh, C. Y., Cruikshank, S. J., & Metherate, R. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02766-9 · Cited by 165 · see citing works
Guo, J., Tredway, T. L., & Chiappinelli, V. A. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-06-01963.1998 · Cited by 143 · see citing works
Nicotine enhances delayed matching-to-sample performance by primates
Elrod, K., Buccafusco, J. J., & Jackson, W. J. (1988) · Life Sciences · doi:10.1016/0024-3205(88)90318-9 · Cited by 142 · see citing works
Sharples, C. G. V., & Wonnacott, S. (2001) · Cited by 141 · see citing works
Alkondon, M., Rocha, E. S., Maelicke, A., & Albuquerque, E. X. (1996) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)20801-1 · Cited by 135 · see citing works
Alkondon, M., Pereira, E. F. R., Almeida, L. E. F., Randall, W. R., & Albuquerque, E. X. (2000) · Neuropharmacology · doi:10.1016/s0028-3908(00)00156-8 · Cited by 129 · see citing works
Hunt, S., & Schmidt, J. (1978) · Brain Research · doi:10.1016/0006-8993(78)90185-3 · Cited by 120 · see citing works
Nicotine enhances morris water maze performance of young and aged rats
Socci, D. J., Sanberg, P. R., & Arendash, G. W. (1995) · Neurobiology of Aging · doi:10.1016/0197-4580(95)00091-r · Cited by 115 · see citing works
Ed, L., Kaplan, S., & Boardman, A. (1997) · PubMed · Cited by 110 · see citing works
Selective effects of nicotine on attentional processes
Mancuso, G., Sherwood, N., Tirelli, E., Warburton, D. M., & M�len, M. (1999) · Psychopharmacology · doi:10.1007/s002130051107 · Cited by 106 · see citing works
Buccafusco, J. J., Jackson, W. J., Terry, A. V., Marsh, K. C., Decker, M. W., & Arnerić, S. P. (1995) · Psychopharmacology · doi:10.1007/bf02311172 · Cited by 100 · see citing works
Nicotine enhances the learning and memory of aged rats
Aren-, G. W., Sanberg, P. R., & Sengstock, G. J. (1995) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(95)00119-h · Cited by 90 · see citing works
Buhler, A. V., & Dunwiddie, T. V. (2002) · Journal of Neurophysiology · doi:10.1152/jn.00316.2001 · Cited by 74 · see citing works
(2000) · Handbook of experimental pharmacology · doi:10.1007/978-3-642-57079-7 · Cited by 72 · see citing works
Cholinergic receptors in aging and Alzheimer's disease
Whitehouse, P. J., & Au, K. S. (1986) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/0278-5846(86)90035-7 · Cited by 72 · see citing works
Rusted, J. M., & Warburton, D. M. (1992) · Psychopharmacology · doi:10.1007/bf02247420 · Cited by 68 · see citing works
Pozza, M. F., Manuel, N. A., Steinmann, M., et al. (1999) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0702498 · Cited by 44 · see citing works
Green, A., Walls, S. B., Wise, A., et al. (2000) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0703755 · Cited by 43 · see citing works
Prendergast, M., Terry, A. V., Jackson, W. J., Marsh, K. C., Decker, M. W., Arnerić, S. P., Buccafusco, J. J., & Terry, A. V. (1997) · Psychopharmacology · doi:10.1007/s002130050240 · Cited by 43 · see citing works
Regulation of glutamate synapses by nicotinic acetylcholine receptors in auditory cortex
Metherate, R., & Hsieh, C. Y. (2003) · Neurobiology of Learning and Memory · doi:10.1016/s1074-7427(03)00062-5 · Cited by 41 · see citing works
Warburton, D. M., Skinner, A., & Martin, C. D. (2001) · Psychopharmacology · doi:10.1007/s002130000565 · Cited by 30 · see citing works
Patterns of facilitation of memory by nicotine
Warburton, D. M., Rusted, J. M., & LLER, C. M. (1992) · Behavioural Pharmacology · doi:10.1097/00008877-199208000-00013 · Cited by 29 · see citing works
Modulation of synaptic transmission by nicotine and nicotinic antagonists in hippocampus
Chiodini, F., TASSONYI, E., Hulo, S., Bertrand, D., & Müller, D. (1999) · Brain Research Bulletin · doi:10.1016/s0361-9230(99)00043-x · Cited by 26 · see citing works
An investigation into the effects of nicotine gum on short-term memory
Phillips, S., & Fox, P. (1998) · Psychopharmacology · doi:10.1007/s002130050786 · Cited by 24 · see citing works
Lacey, G., & Curtis, D. R. (1994) · Experimental Brain Research · doi:10.1007/bf00243217 · Cited by 20 · see citing works
Grigoryan, G. A., Peters, S., Gray, J. A. B., et al. (1994) · Behavioural Pharmacology · doi:10.1097/00008877-199406000-00004 · Cited by 18 · see citing works
Psarropoulou, C., Boivin, M., & Laudadio, M. A. (2003) · Experimental Brain Research · doi:10.1007/s00221-003-1546-x · Cited by 9 · see citing works
Determinants of nicotine self-administration
Shoaib, M. C. (1996) · Drug Development Research · doi:10.1002/(sici)1098-2299(199607/08)38:3/4 · Cited by 7 · see citing works
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The role of acetylcholine in learning and memory
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Self-citationModes and models of forebrain cholinergic neuromodulation of cognition
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- Authors
- Giocomo, L. M., & Hasselmo, M. E.
- Affiliations
- Boston University (US)
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2005-09
- Volume
- 22
- Issue
- 6
- Pages
- 1349-1356
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- OpenAlex
- W2075127191
- Cited by
- 52
- References
- 56
- Citations by year
- 2025: 2 · 2024: 3 · 2023: 2 · 2022: 2 · 2021: 2 · 2019: 2 · 2018: 4 · 2017: 3 · 2016: 2 · 2014: 1 · 2013: 2 · 2012: 3
- FWCI
- 2.13
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation
- National Institutes of Health
- National Institute of Mental Health (MH61492, R01MH061492, MH600013)
- National Institute on Drug Abuse (DA 16454, R01DA016454)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- nicotine, nicotinic acetylcholine receptors, glutamatergic neurotransmission, hippocampal CA3, stratum lacunosum-moleculare, stratum radiatum, GABAergic interneurons, mecamylamine, methyllycaconitine, memory enhancement, cholinergic modulation, synaptic potentiation
- MeSH terms
- Aconitine, Animals, Dose-Response Relationship, Drug, Electric Stimulation, Glutamates, Hippocampus, Male, Mecamylamine, Synaptic Transmission, Neurons, Afferent, Nicotine, Receptors, Nicotinic, Rats, Sprague-Dawley, Nicotinic Agonists, Nicotinic Antagonists, GABA Antagonists, Excitatory Postsynaptic Potentials, Rats, In Vitro Techniques
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