Cholinergic modulation of excitatory synaptic transmission in the CA3 area of the hippocampus
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Cholinergic innervation of the hippocampus has been implicated in memory formation and retrieval. Here we study cholinergic modulation of excitatory transmission in the CA3 area of the rat hippocampus. We used a combination of optical measurements of presynaptic calcium and electrophysiological measurements of synaptic currents to study associational–commissural (A/C) and mossy fiber (MF) synapses in brain slices. Direct synaptic modulation mediated by ACh receptors is only evident at the A/C synapse, where synaptic inhibition primarily reflects presynaptic calcium channel inhibition mediated by muscarinic receptors. MF synapses can, however, be indirectly modulated by muscarinic receptor activation. Muscarine elevates the firing rate of inhibitory cells, which increases GABA release and inhibits MF synapses by activating presynaptic GABA B receptors. Muscarine also depolarizes dentate granule cells and elevates their rate of firing. This leads to synaptic enhancement when combined with the use-dependent facilitation of MF synapses. In addition we were unable to evoke an increase in presynaptic calcium levels in MF boutons with local application of nicotinic receptor agonists. This finding does not support a leading hypothesis for MF modulation in which activation of presynaptic nicotinic receptors enhances transmission directly by elevating presynaptic calcium levels. However, indirect synaptic modulation could arise from nicotinic excitation of inhibitory neurons. Thus, to understand cholinergic modulation within the CA3 region, it is necessary to take into account secondary actions on synapses arising from other chemical messengers released by other cell types and to consider effects on firing patterns of presynaptic cells, which in turn influence release via use-dependent synaptic plasticity.
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Several neuromodulators, such as acetylcholine, dopamine, and noradrenaline, have been reported to affect mossy fiber synaptic transmission.
“Several neuromodulators, such as acetylcholine [97], dopamine [98], and noradrenaline [54] have been reported to affect mossy fiber synaptic transmission.”
From Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons (2024) · cites this paper as [97]
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A new generation of Ca2+ indicators with greatly improved fluorescence properties.
Grynkiewicz, G., Poenie, M., & Tsien, R. Y. (1985) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)83641-4 · Cited by 21,722 · see citing works
Polazzi, E., Mengoni, I., Caprini, M., Peña‐Altamira, E., Kurtys, E., & Monti, B. (2012) · Neurosignals · doi:10.1159/000337115 · Cited by 9,023 · see citing works
The cholinergic hypothesis of geriatric memory dysfunction
Bartus, R. T., Dean, R. L., Beer, B., & Lippa, A. S. (1982) · Science · doi:10.1126/science.7046051 · Cited by 5,545 · see citing works
Alzheimer's Disease: A Disorder of Cortical Cholinergic Innervation
Coyle, J. T., Price, D. L., & DeLong, M. R. (1983) · Science · doi:10.1126/science.6338589 · Cited by 3,050 · see citing works
The three-dimensional organization of the hippocampal formation: A review of anatomical data
Amaral, D. G., & Witter, M. P. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90424-7 · Cited by 2,180 · see citing works
Séguéla, P., Wadiche, J. I., Dineley‐Miller, K., Dani, J., & Jw, P. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-02-00596.1993 · Cited by 1,471 · see citing works
Hulme, E. C., Birdsall, N. J. M., & Buckley, N. J. (1990) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pa.30.040190.003221 · Cited by 1,344 · see citing works
Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors
McGehee, D. S., Heath, M. J. S., Gelber, S., Devay, P., & Role, L. W. (1995) · Science · doi:10.1126/science.7569895 · Cited by 1,070 · 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
Spatial selectivity of unit activity in the hippocampal granular layer
Jung, M. W., & McNaughton, B. L. (1993) · Hippocampus · doi:10.1002/hipo.450030209 · Cited by 789 · see citing works
Comparison between the behavioural effects of septal and hippocampal lesions: A review
Gray, J. A., & McNaughton, N. (1983) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(83)90014-3 · Cited by 658 · see citing works
Presynaptic inhibition of elicited neurotransmitter release
Wu, L., & Saggau, P. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)01015-6 · Cited by 627 · see citing works
Amaral, D. G., & Dent, J. A. (1981) · The Journal of Comparative Neurology · doi:10.1002/cne.901950106 · Cited by 606 · see citing works
Huerta, P. T., & Lisman, J. E. (1993) · Nature · doi:10.1038/364723a0 · Cited by 564 · see citing works
Calcium control of transmitter release at a cerebellar synapse.
Mintz, I., Sabatini, B., & Regehr, W. (1995) · Neuron · doi:10.1016/0896-6273(95)90155-8 · Cited by 551 · see citing works
Self-citationHasselmo, M., & Schnell, E. (1994) · The Journal of Neuroscience · doi:10.1523/jneurosci.14-06-03898.1994 · Cited by 466 · see citing works
Hasselmo, M. E., Schnell, E., & Barkai, E. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-07-05249.1995 · Cited by 463 · see citing works
Choline is a Selective Agonist of α7 Nicotinic Acetylcholine Receptors in the Rat Brain Neurons
Alkondon, M., Pereira, E. F. R., Cartes, W. S., Maelicke, A., & Albuquerque, E. X. (1997) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1997.tb01702.x · Cited by 441 · see citing works
Distinct short-term plasticity at two excitatory synapses in the hippocampus
Salin, P. A., Scanziani, M., Malenka, R. C., & Nicoll, R. A. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.23.13304 · Cited by 438 · see citing works
Levey, A. I., Edmunds, S. M., Koliatsos, V. E., Wiley, R. G., & Heilman, C. J. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-05-04077.1995 · Cited by 423 · see citing works
Inhibitory control of local excitatory circuits in the guinea‐pig hippocampus.
Miles, R., & Wong, R. K. S. (1987) · The Journal of Physiology · doi:10.1113/jphysiol.1987.sp016634 · Cited by 379 · see citing works
Kamiya, H., Shinozaki, H., & Yamamoto, C. (1996) · The Journal of Physiology · doi:10.1113/jphysiol.1996.sp021395 · Cited by 327 · see citing works
Synaptic activation of kainate receptors on hippocampal interneurons
Frerking, M., Malenka, R. C., & Nicoll, R. A. (1998) · Nature Neuroscience · doi:10.1038/2194 · Cited by 312 · see citing works
Dittman, J. S., & Regehr, W. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-05-01623.1996 · Cited by 277 · see citing works
Self-citationThe role of presynaptic calcium in short-term enhancement at the hippocampal mossy fiber synapse
Regehr, W. G., Delaney, K., & Tank, D. W. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-02-00523.1994 · Cited by 269 · see citing works
Self-citationNicotinic 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
The central effects of scopolamine in man.
Safer, D. J., & Allen, R. P. (1971) · PubMed · Cited by 191 · see citing works
Vogt, K. E., & Nicoll, R. A. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.3.1118 · Cited by 174 · see citing works
Self-citationCalcium transients in cerebellar granule cell presynaptic terminals
Regehr, W. G., & Atluri, P. P. (1995) · Biophysical Journal · doi:10.1016/s0006-3495(95)80398-x · Cited by 165 · see citing works
Self-citationNicotinic Receptor Function in the Mammalian Central Nervous Systema
Albuquerque, E. X., Pereira, E. F. R., Castro, N. G., Alkondon, M., Reinhardt, S., Schröder, H., & Maelicke, A. (1995) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1995.tb17464.x · Cited by 156 · see citing works
Properties of tri- and tetracarboxylate Ca2+ indicators in frog skeletal muscle fibers
Zhao, M., Hollingworth, S., & Baylor, S. M. (1996) · Biophysical Journal · doi:10.1016/s0006-3495(96)79633-9 · Cited by 131 · see citing works
Regehr, W. G., & Tank, D. W. (1991) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(91)90121-f · Cited by 125 · see citing works
Self-citationMechanisms underlying kainate receptor-mediated disinhibition in the hippocampus
Frerking, M. E., Petersen, C. C. H., & Nicoll, R. A. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.22.12917 · Cited by 115 · see citing works
Squire, L. R. (1998) · Comptes Rendus de l Académie des Sciences - Series III - Sciences de la Vie · doi:10.1016/s0764-4469(97)89814-9 · Cited by 105 · see citing works
Manzoni, O. J. J., Castillo, P. E., & Nicoll, R. A. (1995) · Neuropharmacology · doi:10.1016/0028-3908(95)00060-j · Cited by 104 · see citing works
Alkondon, M., Braga, M. F. M., Pereira, E. F. R., Maelicke, A., & Albuquerque, E. X. (2000) · European Journal of Pharmacology · doi:10.1016/s0014-2999(00)00006-6 · Cited by 102 · see citing works
Muscarinic receptor subtypes involved in hippocampal circuits
Rouse, S. T., Marino, M. J., Potter, L. T., Conn, P. J., & Levey, A. I. (1999) · Life Sciences · doi:10.1016/s0024-3205(98)00594-3 · Cited by 101 · see citing works
A hippocampal interneuron associated with the mossy fiber system
Vida, I., & Frotscher, M. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.3.1275 · Cited by 94 · see citing works
Kamiya, H., & Ozawa, S. (1999) · Journal of Physiology · doi:10.1111/j.1469-7793.1999.0497p.x · Cited by 90 · see citing works
Christian, E. P., & Dudek, F. E. (1988) · Journal of Neurophysiology · doi:10.1152/jn.1988.59.1.90 · Cited by 87 · see citing works
The Molecular Biology of Neuronal Nicotinic Acetylcholine Receptors
Boyd, R. T. (1997) · Critical Reviews in Toxicology · doi:10.3109/10408449709089897 · Cited by 84 · see citing works
Qian, J., & Saggau, P. (1997) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0701400 · Cited by 76 · see citing works
Amnesia induced by Scopolamine and its Temporal Variations
Deutsch, J. A., & Rocklin, K. W. (1967) · Nature · doi:10.1038/216089b0 · Cited by 69 · see citing works
McQuiston, A. R., & Madison, D. V. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-14-05703.1999 · Cited by 67 · see citing works
Albuquerque, E. X., Pereira, E. F. R., Alkondon, M., Schrattenholz, A. S., & Maelicke, A. (1997) · Journal of Receptors and Signal Transduction · doi:10.3109/10799899709036607 · Cited by 66 · see citing works
Structure and function of glutamate and nicotinic acetylcholine receptors
Dani, J. A., & Mayer, M. L. (1995) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(95)80043-3 · Cited by 63 · see citing works
Muscarinic depression of synaptic transmission at the hippocampal mossy fiber synapse
Williams, S., & Johnston, D. (1990) · Journal of Neurophysiology · doi:10.1152/jn.1990.64.4.1089 · Cited by 61 · see citing works
Presynaptic calcium dynamics at the frog retinotectal synapse
Feller, M. B., Delaney, K. R., & Tank, D. W. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.76.1.381 · Cited by 54 · see citing works
Misgeld, U., Müller, W. S., & Polder, H.-R. (1989) · The Journal of Physiology · doi:10.1113/jphysiol.1989.sp017492 · Cited by 43 · see citing works
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Sorted by citations
The role of acetylcholine in learning and memory
Hasselmo, M. E. (2006) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2006.09.002 · Cited by 1,693 · see citing works
Südhof, T. C. (2012) · Neuron · doi:10.1016/j.neuron.2012.06.012 · Cited by 1,062 · see citing works
Modes and models of forebrain cholinergic neuromodulation of cognition
Hasselmo, M. E., & Sarter, M. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.104 · Cited by 733 · see citing works
Jurd, R., Arrasa, M., Lambert, S., Drexler, B., Siegwart, R., Crestani, F., Zaugg, M., Vogt, K. E., Ledermann, B., Antkowiak, B., et al. (2003) · The FASEB Journal · doi:10.1096/fj.02-0611fje · Cited by 558 · see citing works
Self-citationTrace fear conditioning involves hippocampal α <sub>5</sub> GABA <sub>A</sub> receptors
Crestani, F., Keist, R., Fritschy, J.-M., Benke, D., Vogt, K., Prut, L., Blüthmann, H., Möhler, H., & Rudolph, U. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.142288699 · Cited by 528 · see citing works
Self-citationHasselmo, M. E., & McGaughy, J. (2004) · Progress in Brain Research · doi:10.1016/s0079-6123(03)45015-2 · Cited by 525 · see citing works
Ultrastructural Distribution of the α7 Nicotinic Acetylcholine Receptor Subunit in Rat Hippocampus
Fabian‐Fine, R., Skehel, P., Errington, M. L., Davies, H. A., Sher, E., Stewart, M. G., & Fine, A. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-20-07993.2001 · Cited by 361 · see citing works
Modulation of Presynaptic Store Calcium Induces Release of Glutamate and Postsynaptic Firing
Sharma, G., & Vijayaraghavan, S. (2003) · Neuron · doi:10.1016/s0896-6273(03)00322-2 · Cited by 297 · see citing works
Monosynaptic inputs to new neurons in the dentate gyrus
Vivar, C., Potter, M. C., Choi, J., Lee, J.-Y., Stringer, T. P., Callaway, E. M., Gage, F. H., Suh, H., & van Praag, H. (2012) · Nature Communications · doi:10.1038/ncomms2101 · Cited by 289 · see citing works
Scharfman, H. E., Mercurio, T. C., Goodman, J. H., Wilson, M. A., & MacLusky, N. J. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-37-11641.2003 · Cited by 272 · see citing works
Fukudome, Y., Ohno‐Shosaku, T., Matsui, M., Omori, Y., Fukaya, M., Tsubokawa, H., Taketo, M. M., Watanabe, M., Manabe, T., & Kano, M. (2004) · European Journal of Neuroscience · doi:10.1111/j.0953-816x.2004.03384.x · Cited by 238 · see citing works
Presynaptic ionotropic receptors and control of transmitter release
Engelman, H. S., & MacDermott, A. B. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1297 · Cited by 230 · see citing works
Focusing Effect of Acetylcholine on Neuroplasticity in the Human Motor Cortex
Kuo, M., Grosch, J., Fregni, F., Paulus, W., & Nitsche, M. A. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4104-07.2007 · Cited by 212 · see citing works
Functional Specialization of Presynaptic Cav2.3 Ca2+ Channels
Dietrich, D., Kirschstein, T., Kukley, M., Pereverzev, A., von der Brelie, C., Schneider, T., & Beck, H. (2003) · Neuron · doi:10.1016/s0896-6273(03)00430-6 · Cited by 203 · see citing works
Specific basal forebrain-cortical cholinergic circuits coordinate cognitive operations
Záborszky, L., Gombkoto, P., Varsanyi, P., Gielow, M. R., Poe, G., Role, L. W., Ananth, M., Rajebhosale, P., Talmage, D. A., Hasselmo, M. E., et al. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.1676-18.2018 · Cited by 202 · see citing works
Shibley, H., & Smith, B. N. (2002) · Epilepsy Research · doi:10.1016/s0920-1211(02)00012-8 · Cited by 201 · see citing works
Nicotinic α7 receptors: Synaptic options and downstream signaling in neurons
Berg, D. K., & Conroy, W. G. (2002) · Journal of Neurobiology · doi:10.1002/neu.10116 · Cited by 198 · see citing works
Carbonic anhydrase gating of attention: memory therapy and enhancement
Sun, M., & Alkon, D. L. (2002) · Trends in Pharmacological Sciences · doi:10.1016/s0165-6147(02)01899-0 · Cited by 175 · see citing works
Giocomo, L. M., & Hasselmo, M. E. (2007) · Molecular Neurobiology · doi:10.1007/s12035-007-0032-z · Cited by 161 · see citing works
Carter, A. G., Vogt, K. E., Foster, K. A., & Regehr, W. G. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-01-00021.2002 · Cited by 151 · see citing works
Self-citationNonsynaptic Chemical Transmission Through Nicotinic Acetylcholine Receptors
Lendvai, B., & Vizi, E. S. (2008) · Physiological Reviews · doi:10.1152/physrev.00040.2006 · Cited by 137 · see citing works
Prinz, A. A., Thirumalai, V., & Marder, E. E. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-03-00943.2003 · Cited by 129 · see citing works
Khiroug, L. S., Giniatullin, R. A., Klein, R. C., Fayuk, D. A., & Yakel, J. L. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-27-09024.2003 · Cited by 124 · see citing works
Endogenous Ca 2+ Buffer Concentration and Ca 2+ Microdomains in Hippocampal Neurons
Müller, A., Kukley, M., Stausberg, P., Beck, H., Müller, W. S., & Dietrich, D. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.3799-04.2005 · Cited by 117 · see citing works
Wang, H., Song, L., Laird, F. M., Wong, P. C., & Lee, H. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.2440-08.2008 · Cited by 114 · see citing works
Regulation of GABA release by nicotinic acetylcholine receptors in the neonatal rat hippocampus
Maggi, L., Sher, E., & Cherubini, E. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.00089.x · Cited by 91 · see citing works
Thirugnanasambandam, N., Grundey, J., Adam, K., Drees, A., Skwirba, A. C., Lang, N., Paulus, W., & Nitsche, M. A. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.227 · Cited by 91 · see citing works
Sipilä, S. T., Huttu, K., Voipio, J., & Kaila, K. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04757.x · Cited by 84 · see citing works
Choi, Y., Lin, S. L., Lee, B., Kurup, P. K., Cho, H., Naegele, J. R., Lombroso, P. J., & Obrietan, K. H. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4913-06.2007 · Cited by 85 · see citing works
Carey, M. R., & Regehr, W. G. (2009) · Neuron · doi:10.1016/j.neuron.2009.02.022 · Cited by 80 · see citing works
Self-citationKukolja, J., Thiel, C., & Fink, G. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0203-09.2009 · Cited by 77 · see citing works
Frazier, C. J., Strowbridge, B. W., & Papke, R. L. (2003) · Journal of Neurophysiology · doi:10.1152/jn.01036.2002 · Cited by 80 · see citing works
Possible role of acetylcholine in regulating spatial novelty effects on theta rhythm and grid cells
Barry, C., Heys, J. G., & Hasselmo, M. E. (2012) · Frontiers in Neural Circuits · doi:10.3389/fncir.2012.00005 · Cited by 79 · see citing works
Sharma, G., Grybko, M. J., & Vijayaraghavan, S. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.5407-07.2008 · Cited by 75 · see citing works
Fayuk, D. A., & Yakel, J. L. (2004) · Molecular Pharmacology · doi:10.1124/mol.104.000042 · Cited by 71 · see citing works
Targeting the Hippocampal Mossy Fiber Synapse for the Treatment of Psychiatric Disorders
Kobayashi, K. (2009) · Molecular Neurobiology · doi:10.1007/s12035-008-8049-5 · Cited by 67 · see citing works
Cholinergic Modulation of Spindle Bursts in the Neonatal Rat Visual Cortex<i>In Vivo</i>
Hanganu, I. L., Staiger, J. F., Ben-Ari, Y., & Khazipov, R. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.5233-06.2007 · Cited by 67 · see citing works
A Non-α7 Nicotinic Acetylcholine Receptor Modulates Excitatory Input to Hippocampal CA1 Interneurons
Alkondon, M., & Albuquerque, E. X. (2002) · Journal of Neurophysiology · doi:10.1152/jn.00708.2001 · Cited by 67 · see citing works
Cheng, Q., & Yakel, J. L. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2973-13.2014 · Cited by 66 · see citing works
Function of local circuits in the hippocampal dentate gyrus-CA3 system
Senzai, Y. (2018) · Neuroscience Research · doi:10.1016/j.neures.2018.11.003 · Cited by 64 · see citing works
Xu, Z.-Q., Zhang, W.-J., Su, D.-F., Zhang, G.-Q., & Miao, C.-Y. (2021) · Annals of Translational Medicine · doi:10.21037/atm-21-273 · Cited by 60 · see citing works
Hippocampal gene expression profiling in spatial discrimination learning
Robles, Y., Vivas‐Mejía, P. E., Ortiz‐Zuazaga, H., Félix, J., Ramos, X., & de Ortı́z, S. P. (2003) · Neurobiology of Learning and Memory · doi:10.1016/s1074-7427(03)00025-x · Cited by 63 · see citing works
Shimizu, H., Fukaya, M., Yamasaki, M., Watanabe, M., Manabe, T., & Kamiya, H. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0802175105 · Cited by 62 · see citing works
Synaptic mechanisms underlying cholinergic control of thalamic reticular nucleus neurons
Beierlein, M. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2014.277376 · Cited by 61 · see citing works
Knauer, B., Jochems, A., Valero-Aracama, M. J., & Yoshida, M. (2013) · Hippocampus · doi:10.1002/hipo.22136 · Cited by 62 · see citing works
Effects of acetylcholine on neuronal properties in entorhinal cortex
Heys, J. G., Schultheiss, N. W., Shay, C. F., Tsuno, Y., & Hasselmo, M. E. (2012) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2012.00032 · Cited by 56 · see citing works
Aznavour, N., Mechawar, N., & Descarries, L. (2002) · Hippocampus · doi:10.1002/hipo.1108 · Cited by 60 · see citing works
Dynamic internal states shape memory retrievalPreprint
Tarder-Stoll, H., Jayakumar, M., Dimsdale-Zucker, H. R., Günseli, E., & Aly, M. (2019) · doi:10.1016/j.neuropsychologia.2019.107328 · Cited by 57 · see citing works
M‐type potassium channels modulate Schaffer collateral–CA1 glutamatergic synaptic transmission
Sun, J., & Kapur, J. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2012.235820 · Cited by 55 · see citing works
Regulation of synaptic plasticity in a schizophrenia model
Gisabella, B., Bolshakov, V. Y., & Benes, F. M. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506034102 · Cited by 55 · see citing works
Mossy fiber synaptic transmission: communication from the dentate gyrus to area CA3
Jaffe, D. B., & Gutiérrez, R. (2007) · Progress in brain research · doi:10.1016/s0079-6123(07)63006-4 · Cited by 54 · see citing works
A transgenic mouse model reveals fast nicotinic transmission in hippocampal pyramidal neurons
Grybko, M. J., Hahm, E.-T., Perrine, W., Parnes, J. A., Chick, W. S. H., Sharma, G., Finger, T. E., & Vijayaraghavan, S. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07671.x · Cited by 53 · see citing works
Neuromodulation of the Feedforward Dentate Gyrus-CA3 Microcircuit
Prince, L. Y., Bacon, T., Tigaret, C. M., & Mellor, J. R. (2016) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2016.00032 · Cited by 51 · see citing works
Kremin, T., GERBER, D., Giocomo, L. M., Huang, S., Tonegawa, S., & Hasselmo, M. E. (2005) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2005.09.005 · Cited by 52 · see citing works
Treviño, M., & Gutiérrez, R. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.092064 · Cited by 50 · see citing works
Phasic cholinergic signaling in the hippocampus: Functional homology with the neocortex?
Gulledge, A. T., & Kawaguchi, Y. (2007) · Hippocampus · doi:10.1002/hipo.20279 · Cited by 48 · see citing works
Ca2+ permeability of nicotinic acetylcholine receptors in rat hippocampal CA1 interneurones
Fayuk, D. A., & Yakel, J. L. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.089789 · Cited by 48 · see citing works
Persistent firing supported by an intrinsic cellular mechanism in hippocampal CA 3 pyramidal cells
Jochems, A., & Yoshida, M. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12236 · Cited by 45 · see citing works
Parra, H. R., Vivar, C., Maqueda, J., Morales, M. A., & Gutiérrez, R. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00985.2002 · Cited by 45 · see citing works
Kremin, T., & Hasselmo, M. E. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.07.007 · Cited by 43 · see citing works
An, L., Yang, Z. R., & Zhang, T. (2012) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2012.12.003 · Cited by 44 · see citing works
Molyneaux, B. J., & Hasselmo, M. E. (2002) · Journal of Neurophysiology · doi:10.1152/jn.00077.2001 · Cited by 43 · see citing works
Hippocampal storage and recall of neocortical “What”–“Where” representations
Rolls, E. T., Zhang, C., & Feng, J. (2024) · Hippocampus · doi:10.1002/hipo.23636 · Cited by 42 · see citing works
Haley, J. A., Hampton, D., & Marder, E. E. (2018) · eLife · doi:10.7554/elife.41877 · Cited by 42 · see citing works
Circuits for State-Dependent Modulation of Locomotion
Pernía‐Andrade, A. J., Wenger, N., Esposito, M. S., & Tovote, P. (2021) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2021.745689 · Cited by 38 · see citing works
Reyes‐Castro, L. A., Padilla‐Gómez, E., Parga‐Martínez, N. J., Castro‐Rodríguez, D. C., Quirarte, G. L., Díaz‐Cintra, S., Nathanielsz, P. W., & Zambrano, E. (2018) · Hippocampus · doi:10.1002/hipo.22798 · Cited by 36 · see citing works
Septal Modulation of Excitatory Transmission in Hippocampus
Colgin, L. L., Kramár, E. A., Gall, C. M., & LYNCH, G. S. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00262.2003 · Cited by 36 · see citing works
Altered hippocampal circuit function in C3H α7 null mutant heterozygous mice
Adams, C. E., Yonchek, J. C., Zheng, L., Collins, A. C., & Stevens, K. E. (2008) · Brain Research · doi:10.1016/j.brainres.2007.12.007 · Cited by 35 · see citing works
Hummos, A., Franklin, C. C., & Nair, S. S. (2014) · Hippocampus · doi:10.1002/hipo.22324 · Cited by 32 · see citing works
Carver, C. M., & Shapiro, M. S. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.1781-18.2018 · Cited by 31 · see citing works
Hanganu, I. L., & Luhmann, H. J. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00010.2004 · Cited by 32 · see citing works
Section I. The Cholinergic System
Smythies, J. (2005) · International review of neurobiology · doi:10.1016/s0074-7742(05)64001-9 · Cited by 32 · see citing works
Nicotine augmentation for refractory obsessive-compulsive disorder. A case report
Pasquini, M., Garavini, A., & Biondi, M. (2004) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2004.08.011 · Cited by 31 · see citing works
Chronic nicotine and smoking exposure decreases GABAB1 receptor expression in the rat hippocampus
Li, S. P., Park, M. S., Bahk, J. Y., & Kim, M. O. (2002) · Neuroscience Letters · doi:10.1016/s0304-3940(02)01065-0 · Cited by 30 · see citing works
Jochems, A., Reboreda, A., Hasselmo, M. E., & Yoshida, M. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.06.027 · Cited by 26 · see citing works
Gol, M., Ghorbanian, D., Soltanpour, N., Faraji, J., & Pourghasem, M. (2017) · Nutritional Neuroscience · doi:10.1080/1028415x.2017.1354959 · Cited by 27 · see citing works
Pre- and postsynaptic properties of somatic and dendritic inhibition in dentate gyrus
Harney, S. C., & Jones, M. V. (2002) · Neuropharmacology · doi:10.1016/s0028-3908(02)00169-7 · Cited by 26 · see citing works
Bancila, V., Cordeiro, M., Bloc, A., & Dunant, Y. (2009) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.06169.x · Cited by 25 · see citing works
An integrative model of the intrinsic hippocampal theta rhythm
Hummos, A., & Nair, S. S. (2017) · PLoS ONE · doi:10.1371/journal.pone.0182648 · Cited by 24 · see citing works
The race to learn: Spike timing and STDP can coordinate learning and recall in CA3
Nolan, C. R., Wyeth, G. F., Milford, M. J., & Wiles, J. (2010) · Hippocampus · doi:10.1002/hipo.20777 · Cited by 25 · see citing works
Zheng, F., Wess, J., & Alzheimer, C. (2012) · Journal of Neurophysiology · doi:10.1152/jn.00740.2011 · Cited by 24 · see citing works
Gholami, M., Saboory, E., Zare, S., Roshan‐Milani, S., & Moghaddam, A. H. (2012) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2012.07.004 · Cited by 25 · see citing works
Sola, E., Capsoni, S., Rosato‐Siri, M. D., Cattaneo, A., & Cherubini, E. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04996.x · Cited by 23 · see citing works
Sinha, N., Karche, N. P., Verma, M. K., Walunj, S. S., Nigade, P. B., Jana, G., Kurhade, S. P., Hajare, A. K., Tilekar, A. R., Jadhav, G. R., et al. (2020) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.9b01569 · Cited by 30 · see citing works
Chen, G., & Yan, J. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05432.x · Cited by 22 · see citing works
Mishra, K. A., & Sethi, K. K. (2024) · Archiv der Pharmazie · doi:10.1002/ardp.202400748 · Cited by 21 · see citing works
Choline‐mediated modulation of hippocampal sharp wave–ripple complexesin vitro
Fischer, V., Both, M., Draguhn, A., & Egorov, A. V. (2014) · Journal of Neurochemistry · doi:10.1111/jnc.12693 · Cited by 20 · see citing works
Potential roles of cholinergic modulation in the neural coding of location and movement speed
Dannenberg, H., Hinman, J. R., & Hasselmo, M. E. (2016) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2016.09.002 · Cited by 21 · see citing works
Kajikawa, K., Hulse, B., Siapas, A. G., & Lubenov, E. V. (2022) · eLife · doi:10.7554/elife.69596 · Cited by 15 · see citing works
Saravanan, V., Arabali, D., Jochems, A., Cui, A., Gootjes-Dreesbach, L., Cutsuridis, V., & Yoshida, M. (2015) · Hippocampus · doi:10.1002/hipo.22429 · Cited by 18 · see citing works
Regulation of epileptiform activity in hippocampus by nicotinic acetylcholine receptor activation
Roshan‐Milani, S., Ferrigan, L., Khoshnoud, M. J., Davies, C. H., & Cobb, S. (2003) · Epilepsy Research · doi:10.1016/j.eplepsyres.2003.08.005 · Cited by 18 · see citing works
Benes, F. M. (2012) · Handbook of experimental pharmacology · doi:10.1007/978-3-642-25758-2_13 · Cited by 17 · see citing works
Uematsu, N., Matsukawa, N., Kanamori, T., Arai, Y., Sagisaka, T., Toyoda, T., Yoshida, M., & Ojika, K. (2009) · Brain Research · doi:10.1016/j.brainres.2009.09.112 · Cited by 17 · see citing works
Kim, O., Okamoto, Y., Kaufmann, W. A., Brose, N., Shigemoto, R., & Jonas, P. (2024) · PLOS Biology · doi:10.1371/journal.pbio.3002879 · Cited by 15 · see citing works
“Several neuromodulators, such as acetylcholine [97], dopamine [98], and noradrenaline [54] have been reported to affect mossy fiber synaptic transmission.”
A rodent model of schizophrenia derived from postmortem studies
Berretta, S., Gisabella, B., & Benes, F. M. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.06.019 · Cited by 15 · see citing works
HCNP precursor protein transgenic mice display a depressive-like phenotype in old age
Matsukawa, N., Furuya, Y., Ogura, H., & Ojika, K. (2010) · Brain Research · doi:10.1016/j.brainres.2010.06.041 · Cited by 15 · see citing works
Presynaptic Inhibition of Excitatory Afferents to Hilar Mossy Cells
Nahir, B., Bhatia, C., & Frazier, C. J. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00069.2007 · Cited by 15 · see citing works
de Vin, F., Choi, S. M., Bolognesi, M. L., & Lefebvre, R. A. (2015) · Brain Research · doi:10.1016/j.brainres.2015.10.031 · Cited by 14 · see citing works
Hasselmo, M. E. (2024) · Hippocampus · doi:10.1002/hipo.23676 · Cited by 17 · see citing works
Chu, Y., Fioravante, D., Thanawala, M. S., Leitges, M., & Regehr, W. G. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.2158-12.2012 · Cited by 13 · see citing works
Self-citation
- Authors
- Vogt, K. E., & Regehr, W. G.
- Affiliations
- Harvard University (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2001-01-01
- Volume
- 21
- Issue
- 1
- Pages
- 75-83
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6762445
- OpenAlex
- W2125706064
- Cited by
- 149
- References
- 49
- Citations by year
- 2025: 4 · 2024: 5 · 2023: 5 · 2022: 2 · 2021: 5 · 2020: 3 · 2019: 2 · 2018: 6 · 2017: 4 · 2016: 2 · 2015: 4 · 2014: 6 · 2013: 5 · 2012: 10
- FWCI
- 4.56
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
- National Institutes of Health
- U.S. Public Health Service (P01-N538312)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- cholinergic modulation, excitatory synaptic transmission, hippocampal CA3, muscarinic receptors, nicotinic acetylcholine receptors, mossy fiber synapses, presynaptic calcium, GABAergic inhibition, GABAB receptors, dentate gyrus granule cells, synaptic plasticity, acetylcholine
- MeSH terms
- Animals, Calcium, Cholinergic Fibers, Fluorescent Dyes, Hippocampus, Muscarine, Synaptic Transmission, Nicotine, Synapses, Fura-2, Rats, Sprague-Dawley, Pyramidal Cells, Receptors, Metabotropic Glutamate, Patch-Clamp Techniques, Cholinergic Agonists, Glutamic Acid, Nicotinic Agonists, Mossy Fibers, Hippocampal, Excitatory Postsynaptic Potentials, Rats, GABA-B Receptor Agonists, GABA-A Receptor Antagonists, GABA-B Receptor Antagonists, In Vitro Techniques
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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