Cholinergic modulation of the hippocampus during encoding and retrieval
Abstract
The present experiments were aimed at determining whether acetylcholine (ACh) plays a role in encoding and retrieval of spatial information using a modified Hebb-Williams maze. In addition, the present experiments tested two computational models of hippocampal function during encoding and retrieval using a maze sensitive to hippocampal disruption. Thirty male, Long-Evans rats served as subjects. Chronic cannulae were implanted bilaterally into the CA3 (n=26) and CA1 (n=5) subregions of the hippocampus. Rats were tested using a modified Hebb-Williams maze. In the first experiment, rats were injected with either saline or scopolamine hydrobromide 10 min before testing for each day. The number of errors made per day per group was used as the measure of learning. Encoding was assessed by the average number of errors made on the first five trials of Day 1 compared to the last five trials of Day 1, whereas the average number of errors made on the first five trials of Day 2 compared to the last five trials of Day I was used to assess retrieval. No deficit was found for the saline group. The scopolamine group showed a deficit in encoding, but not retrieval. In the second experiment, rats were injected with either saline or physostigmine 10 min before testing each day. In contrast to the scopolamine groups, the physostigmine group showed a deficit in retrieval, but not encoding. To test whether the retrieval deficit was due to a disruption in storage or gaining access to the information two groups of rats received either saline on Day 1 and physostigmine on Day 2 or physostigmine on Day 1 and saline on Day 2. In addition, one group received physostigmine immediately after testing on Day 1. Data indicate that physostigmine causes a disruption of retrieval by means of a disruption in consolidation process. In conclusion, the cholinergic antagonist, scopolamine, disrupts encoding in both CA3 and CA1 subregions of the hippocampus. Furthermore, the cholinesterase inhibitor, physostigmine, boosts ACh action during a time when cholinergic levels need to decline for proper consolidation.
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Local infusions of scopolamine into the hippocampus impair encoding of spatial information.
“Local infusions of scopolamine into the hippocampus impair encoding of spatial information (Blokland et al., 1992; Rogers and Kesner, 2003).”
From Modes and models of forebrain cholinergic neuromodulation of cognition (2011) · cites this paper as Rogers and Kesner, 2003
Cites
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
Graded persistent activity in entorhinal cortex neurons
Egorov, A. V., Hamam, B. N., Fransén, E., Hasselmo, M. E., & Alonso, A. A. (2002) · Nature · doi:10.1038/nature01171 · Cited by 769 · see citing works
The Cholinergic Synapse and the Site of Memory
Deutsch, J. A. (1972) · Advances in behavioral biology · doi:10.1007/978-1-4684-3060-8_11 · Cited by 740 · see citing works
The Physiological Basis of Memory
Deutsch, J. A. (1969) · Annual Review of Psychology · doi:10.1146/annurev.ps.20.020169.000505 · Cited by 658 · see citing works
Neuromodulation and cortical function: modeling the physiological basis of behavior
Hasselmo, M. E. (1995) · Behavioural Brain Research · doi:10.1016/0166-4328(94)00113-t · Cited by 552 · 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
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
Hasselmo, M. E., & Bower, J. M. (1993) · Trends in Neurosciences · doi:10.1016/0166-2236(93)90159-j · Cited by 429 · see citing works
Hasselmo, M. E., & Wyble, B. (1997) · Behavioural Brain Research · doi:10.1016/s0166-4328(97)00048-x · Cited by 337 · see citing works
A closed-field intelligence test for rats.
Rabinovitch, M. S., & Rosvold, H. E. (1951) · Canadian Journal of Psychology/Revue Canadienne de Psychologie · doi:10.1037/h0083542 · Cited by 310 · see citing works
Functions of Neuronal Networks in the Hippocampus and Neocortex in Memory
Rolls, E. T. (1989) · Elsevier eBooks · doi:10.1016/b978-0-12-148955-7.50017-5 · Cited by 292 · see citing works
Lee, I., & Kesner, R. P. (2004) · Hippocampus · doi:10.1002/hipo.10167 · Cited by 253 · see citing works
Self-citationThe Physiological Basis of Memory
Hogarth, P. J. (1983) · Elsevier eBooks · doi:10.1016/b978-0-12-213460-9.x5001-1 · Cited by 243 · see citing works
Hasselmo, M. E., & McClelland, J. L. (1999) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(99)80025-7 · Cited by 141 · see citing works
Two‐Phase Computational Model Training Long‐Term Memories in the Entorhinal‐Hippocampal Region
Lörincz, A., & Buzsáki, G. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06721.x · Cited by 117 · see citing works
Wallenstein, G. V., & Vago, D. R. (2001) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2001.4005 · Cited by 109 · see citing works
Oscillatory Activity in Entorhinal Neurons and Circuits: Mechanisms and Function
Dickson, C. T., Magistretti, J., Shalinsky, M. H., Hamam, B. N., & Alonso, Á. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06723.x · Cited by 104 · see citing works
Galani, R., Jarrard, L. E., Will, B. E., & Kelche, C. R. (1997) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1996.3745 · Cited by 86 · see citing works
Blokland, A., Honig, W., & Raaijmakers, W. G. M. (1992) · Psychopharmacology · doi:10.1007/bf02245886 · Cited by 85 · see citing works
A comparison of the effects of two inhibitors on brain cholinesterase
Hallak, M. E., & Giacobini, E. (1987) · Neuropharmacology · doi:10.1016/0028-3908(87)90143-2 · Cited by 76 · see citing works
Degroot, A., & Parent, M. B. (2000) · Learning & Memory · doi:10.1101/lm.32200 · Cited by 63 · see citing works
Hallak, M. E., & Giacobini, E. (1986) · Neurochemical Research · doi:10.1007/bf00965592 · Cited by 63 · see citing works
Ishikawa, K., McGaugh, J. L., & Sakata, H. (1996) · University of Groningen research database (University of Groningen / Centre for Information Technology) · Cited by 48 · see citing works
Todd, J., & Kesner, R. P. (1978) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077544 · Cited by 43 · see citing works
Self-citationNerve growth factor produces a temporary facilitation of recovery from entorhinal cortex lesions
Stein, D. G., & Will, B. E. (1983) · Brain Research · doi:10.1016/0006-8993(83)91291-x · Cited by 38 · see citing works
Mattio, T. G. (1986) · Neuropharmacology · doi:10.1016/0028-3908(86)90166-8 · Cited by 31 · see citing works
Muscarinic receptor subtypes and sexual behavior in female rats
Dohanich, G. P., McMullan, D. M., Cada, D. A., & Mangum, K. A. (1991) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(91)90598-v · Cited by 26 · see citing works
Myhrer, T. (1975) · Physiology & Behavior · doi:10.1016/0031-9384(75)90255-3 · Cited by 26 · see citing works
The representation of space in the primate hippocampus, and its role in memory
Rolls, E. T. (1998) · doi:10.1093/oso/9780198524533.003.0017 · Cited by 26 · see citing works
Yamamoto, T., Ohno, M., Kitajima, I., Yatsugi, S., & Ueki, S. (1993) · Physiology & Behavior · doi:10.1016/0031-9384(93)90003-x · Cited by 17 · see citing works
Glasier, M. M., Janis, L. S., & Stein, D. G. (1997) · Behavioral Neuroscience · doi:10.1037//0735-7044.111.1.225 · Cited by 10 · see citing works
Glasier, M. M., Janis, L. S., & Stein, D. G. (1997) · Behavioral Neuroscience · doi:10.1037/0735-7044.111.1.225 · Cited by 8 · see citing works
Flagged first, then by citations
Cited by
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
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
A computational theory of hippocampal function, and empirical tests of the theory
Rolls, E. T., & Kesner, R. P. (2006) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2006.04.005 · Cited by 608 · see citing works
Self-citationDeclarative memory consolidation: mechanisms acting during human sleep
Gais, S., & Born, J. (2004) · Learning & Memory · doi:10.1101/lm.80504 · Cited by 536 · see citing works
Dentate gyrus circuits for encoding, retrieval and discrimination of episodic memories
Hainmueller, T., & Bartos, M. (2020) · Nature reviews. Neuroscience · doi:10.1038/s41583-019-0260-z · Cited by 474 · see citing works
Cholinergic modulation of the hippocampal region and memory function
Haam, J., & Yakel, J. L. (2017) · Journal of Neurochemistry · doi:10.1111/jnc.14052 · Cited by 446 · see citing works
A computational theory of hippocampal function, and tests of the theory: New developments
Kesner, R. P., & Rolls, E. T. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.11.009 · Cited by 347 · see citing works
Self-citationA daytime nap containing solely non-REM sleep enhances declarative but not procedural memory
Tucker, M., HIROTA, Y., Wamsley, E. J., LAU, H., Chaklader, A., & Fishbein, W. I. (2006) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2006.03.005 · Cited by 349 · see citing works
Behavioral functions of the CA3 subregion of the hippocampusPreprint
Kesner, R. P. (2007) · Learning & Memory · doi:10.1101/lm.688207 · Cited by 337 · see citing works
Self-citationHunsaker, M. R., & Kesner, R. P. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.09.014 · Cited by 283 · see citing works
Self-citationThe cholinergic system and spatial learning
Deiana, S., Platt, B., & Riedel, G. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.11.036 · Cited by 245 · see citing works
Cognitive sequelae of head injury: involvement of basal forebrain and associated structures
Salmond, C. H. (2004) · Brain · doi:10.1093/brain/awh352 · Cited by 194 · see citing works
The role of metaplasticity mechanisms in regulating memory destabilization and reconsolidation
Finnie, P. S. B., & Nader, K. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.03.008 · Cited by 189 · see citing works
Cerebral cortex : principles of operation
Rolls, E. T. (2016) · doi:10.82444/warw.33712699 · Cited by 187 · see citing works
Cholinergic modulation of cognition: Insights from human pharmacological functional neuroimaging
Bentley, P., Driver, J., & Dolan, R. J. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.06.002 · Cited by 173 · see citing works
Acetylcholine and memory: A long, complex and chaotic but still living relationship
Micheau, J., & Marighetto, A. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.11.052 · Cited by 164 · see citing works
Acetylcholine bidirectionally regulates learning and memory
Huang, Q., Liao, C., Ge, F., Ao, J., & Liu, T. (2022) · Journal of Neurorestoratology · doi:10.1016/j.jnrt.2022.100002 · Cited by 165 · see citing works
Assini, F. L., Duzzioni, M., & Takahashi, R. N. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.06.005 · Cited by 161 · see citing works
Giocomo, L. M., & Hasselmo, M. E. (2007) · Molecular Neurobiology · doi:10.1007/s12035-007-0032-z · Cited by 165 · see citing works
Dannenberg, H., Pabst, M., Braganza, O., Schoch, S., Niediek, J., Bayraktar, M., Mormann, F., & Beck, H. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.4460-14.2015 · Cited by 143 · see citing works
Douchamps, V., Jeewajee, A., Blundell-Birtill, P., Burgess, N., & Lever, C. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.4483-12.2013 · Cited by 135 · see citing works
Cholinesterase inhibitors and memory
Pepeu, G., & Giovannini, M. G. (2009) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2009.11.018 · Cited by 134 · see citing works
Prefrontal and hippocampal contributions to encoding and retrieval of spatial memory
Churchwell, J. C., Morris, A. M., Musso, N. D., & Kesner, R. P. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.12.008 · Cited by 132 · see citing works
Self-citationRasch, B. H., Born, J., & Gais, S. (2006) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2006.18.5.793 · Cited by 137 · see citing works
Toxin-Induced Experimental Models of Learning and Memory Impairment
More, S. V., Kumar, H., Cho, D.-Y., Yun, Y.-S., & Choi, D. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17091447 · Cited by 105 · see citing works
Rogers, J. L., & Kesner, R. P. (2004) · Learning & Memory · doi:10.1101/lm.64604 · Cited by 103 · see citing works
Self-citationThe temporal attributes of episodic memory
Kesner, R. P., & Hunsaker, M. R. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.12.029 · Cited by 102 · see citing works
Self-citationNathan, P. J., Watson, J. M., Jesper, L., Davies, C. H., Peters, G., Dodds, C. M., Swirski, B., Lawrence, P., Bentley, G., O’Neill, B. V., et al. (2012) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145712000752 · Cited by 100 · see citing works
A process analysis of the CA3 subregion of the hippocampus
Kesner, R. P. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00078 · Cited by 98 · see citing works
Self-citationCholinesterase Inhibitors Ameliorate Behavioral Deficits Induced by MK-801 in Mice
Csernansky, J. G., Martin, M. V., Shah, R., Bertchume, A., Colvin, J., & Dong, H. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300761 · Cited by 99 · see citing works
A specific role for septohippocampal acetylcholine in memory?
Easton, A., Douchamps, V., Eacott, M. J., & Lever, C. (2012) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2012.07.022 · Cited by 99 · see citing works
Xu, P., Wang, K., Lü, C., Dong, L., Gao, L., Yan, M., Aibai, S., Yang, Y., & Liu, X. (2017) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2017/7426538 · Cited by 94 · see citing works
Krug, R., Jan Born, A., & Rasch, B. (2006) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2006.05.007 · Cited by 90 · see citing works
Modulation of Hippocampal Circuits by Muscarinic and Nicotinic Receptors
Dannenberg, H., Young, K., & Hasselmo, M. E. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00102 · Cited by 87 · see citing works
Song, T., Lin, H., Chen, C.-L., Wu, J., Liao, J., & Hu, M. (2014) · Free Radical Research · doi:10.3109/10715762.2014.920954 · Cited by 84 · see citing works
Jacobsen, L. K., Slotkin, T. A., Westerveld, M., Mencl, W. E., & Pugh, K. R. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300981 · Cited by 81 · see citing works
Kukolja, J., Thiel, C., & Fink, G. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0203-09.2009 · Cited by 77 · 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
Balancing Arc Synthesis, mRNA Decay, and Proteasomal Degradation
Soule, J. D., Alme, M. N., Myrum, C., Schubert, M., Kanhema, T., & Bramham, C. R. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.376491 · Cited by 71 · see citing works
Antonova, E., Parslow, D. M., Brammer, M. J., Simmons, A., Williams, S., Dawson, G. R., & Morris, R. G. (2010) · Journal of Psychopharmacology · doi:10.1177/0269881110379285 · Cited by 71 · see citing works
Haam, J., Zhou, J., Cui, G., & Yakel, J. L. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1712538115 · Cited by 63 · see citing works
Neuromodulatory signaling in hippocampus‐dependent memory retrieval
THOMAS, S. A. (2014) · Hippocampus · doi:10.1002/hipo.22394 · Cited by 64 · see citing works
Brain Plasticity and Genetic Factors
Pearson-Fuhrhop, K. M., Kleim, J., & Cramer, S. (2009) · Topics in Stroke Rehabilitation · doi:10.1310/tsr1604-282 · Cited by 75 · see citing works
Pharmacological Dissociation of Novelty Responses in the Human Brain
Bunzeck, N., Guitart‐Masip, M., Dolan, R. J., & Düzel, E. (2013) · Cerebral Cortex · doi:10.1093/cercor/bhs420 · Cited by 57 · see citing works
Muscarinic acetylcholine receptors act in synergy to facilitate learning and memoryPreprint
Leaderbrand, K., Chen, H. J., Corcoran, K. A., Guedea, A. L., Jovasevic, V., Wess, J., & Radulović, J. (2016) · Learning & Memory · doi:10.1101/lm.043133.116 · Cited by 58 · see citing works
Genetic Influences on Neural Plasticity
Pearson‐Fuhrhop, K. M., & Cramer, S. C. (2010) · PM&R · doi:10.1016/j.pmrj.2010.09.011 · Cited by 56 · see citing works
Chemicals used for the induction of Alzheimer’s disease-like cognitive dysfunctions in rodents
Mahdi, O., Baharuldin, M. T. H., Nor, N. H. M., Chiroma, S. M., Jagadeesan, S., & Moklas, M. A. M. (2019) · Biomedical Research and Therapy · doi:10.15419/bmrat.v6i11.575 · Cited by 51 · see citing works
Thomas, E. H. X., Snyder, P. J., Pietrzak, R. H., Jackson, C. E., Bednar, M. M., & Maruff, P. T. (2008) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2008.04.010 · Cited by 52 · see citing works
Fujishiro, H., Umegaki, H., Suzuki, Y., Kurotani, S., Yamaguchi, Y., & Iguchi, A. (2005) · Psychopharmacology · doi:10.1007/s00213-005-0072-x · Cited by 47 · see citing works
Pharmacological Findings on the Biochemical Bases of Memory Processes: A General View
Izquierdo, I., Cammarota, M., Medina, J., & Bevilaqua, L. (2004) · Journal of Neural Transplantation and Plasticity · doi:10.1155/np.2004.159 · Cited by 41 · see citing works
A Brief Review of Neurotoxicity Induced by Melamine
An, L., & Sun, W. (2017) · Neurotoxicity Research · doi:10.1007/s12640-017-9731-z · Cited by 46 · 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
Jacobson, T. K., Howe, M. D., Schmidt, B., Hinman, J. R., Escabı́, M. A., & Markus, E. J. (2013) · Journal of Neurophysiology · doi:10.1152/jn.00409.2012 · Cited by 44 · see citing works
A synaptic signal for novelty processing in the hippocampus
Gómez-Ocádiz, R., Trippa, M., Zhang, C.-L., Posani, L., Cocco, S., Monasson, R., & Schmidt‐Hieber, C. (2022) · Nature Communications · doi:10.1038/s41467-022-31775-6 · Cited by 40 · see citing works
Márquez, A. C., Vale-Martı́nez, A., Guillazo‐Blanch, G., & Martí‐Nicolovius, M. (2008) · Hippocampus · doi:10.1002/hipo.20530 · Cited by 41 · 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
Cholinergic influences on feature binding.
Botly, L. C. P., & Rosa, E. D. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.2.264 · Cited by 36 · see citing works
Hunsaker, M. R., Tran, G. T., & Kesner, R. P. (2008) · Hippocampus · doi:10.1002/hipo.20429 · Cited by 35 · see citing works
Self-citationLaursen, B., Mørk, A., Plath, N., Kristiansen, U., & Bastlund, J. F. (2013) · Brain Research · doi:10.1016/j.brainres.2013.10.055 · Cited by 33 · see citing works
Different effects of scopolamine on the retrieval of spatial memory and fear memory
Huang, Z., Wang, H., Rao, X., Zhong, G., Hu, W.-H., & Sheng, G. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.05.032 · Cited by 33 · see citing works
Hunsaker, M. R., Rogers, J. L., & Kesner, R. P. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.01.006 · Cited by 33 · see citing works
Self-citationModulation of CA3 Afferent Inputs by Novelty and Theta Rhythm
Villarreal, D. M., Gross, A. L., & Derrick, B. E. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3702-07.2007 · Cited by 33 · see citing works
Hummos, A., Franklin, C. C., & Nair, S. S. (2014) · Hippocampus · doi:10.1002/hipo.22324 · Cited by 32 · see citing works
Selective cholinergic immunolesioning affects synaptic plasticity in developing visual cortex
Kuczewski, N., Aztiria, E., Leanza, G., & Domenici, L. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04014.x · Cited by 32 · see citing works
Perirhinal cortex is necessary for acquiring, but not for retrieving object–place paired associationPreprint
Jo, Y. S., & Lee, I. (2010) · Learning & Memory · doi:10.1101/lm.1620410 · Cited by 32 · see citing works
Cholinergic Regulation of Hippocampal Theta Rhythm
Gu, Z., & Yakel, J. L. (2022) · Biomedicines · doi:10.3390/biomedicines10040745 · Cited by 31 · see citing works
Yousefi, B., Nasehi, M., Khakpai, F., & Zarrindast, M. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.08.006 · Cited by 32 · see citing works
Eskildsen, J., Redrobe, J. P., Sams, A. G., Dekermendjian, K., Laursen, M., Boll, J. B., Papke, R. L., Bundgaard, C., Frederiksen, K., & Bastlund, J. F. (2013) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/j.bmcl.2013.11.022 · Cited by 29 · see citing works
Pereira, P. M., Cosquer, B., Schimchowitsch, S., & Cassel, J. (2004) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2004.09.007 · Cited by 28 · see citing works
Association of short- and long-latency afferent inhibition with human behavior
Turco, C. V., Toepp, S. L., Foglia, S. D., Dans, P. W., & Nelson, A. J. (2021) · Clinical Neurophysiology · doi:10.1016/j.clinph.2021.02.402 · Cited by 27 · see citing works
Effects of Mulberry on The Central Nervous System: A Literature Review
Tam, D. N. H., Nam, N. H., Elhady, M. T., Tran, L., Hassan, O., Sadik, M., Tien, P. T. M., Elshafei, G., & Huy, N. T. (2020) · Current Neuropharmacology · doi:10.2174/1570159x18666200507081531 · Cited by 26 · see citing works
Gold, P. E., Countryman, R. A., Dukala, D., & Chang, Q. (2011) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2011.08.004 · Cited by 26 · 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
Bundel, D. D., Demaegdt, H., Lahoutte, T., Caveliers, V., Kersemans, K., Ceulemans, A.-G., Vauquelin, G., Clinckers, R., Vanderheyden, P., Michotte, Y. M., et al. (2009) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.06547.x · Cited by 25 · see citing works
Hypoxia modulates cholinergic but not opioid activation of G proteins in rat hippocampus
Hambrecht‐Wiedbusch, V. S., Vlisides, P. E., Row, B. W., Gozal, D., Baghdoyan, H. A., & Lydic, R. (2007) · Hippocampus · doi:10.1002/hipo.20312 · Cited by 23 · see citing works
Salcido, F. A. M., Torres-Flores, M. I., Ordaz, B., & Peña‐Ortega, F. (2022) · Glia · doi:10.1002/glia.24185 · Cited by 21 · see citing works
Blockade of muscarinic receptors impairs the retrieval of well-trained memory
Soma, S., Suematsu, N., & Shimegi, S. (2014) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2014.00063 · Cited by 20 · see citing works
Takahashi, K., Tsuji, M., Nakagawasai, O., Katsuyama, S., Miyagawa, K., Kurokawa, K., Mochida-Saito, A., Iwasa, M., Iwasa, H., Takeda, H., et al. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113283 · Cited by 19 · 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
Harel, B., Pietrzak, R. H., Snyder, P. J., & Maruff, P. T. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3072-2 · Cited by 21 · see citing works
Kusindarta, D. L., Wihadmadyatami, H., & Haryanto, A. T. (2018) · Veterinary World · doi:10.14202/vetworld.2018.135-140 · Cited by 18 · see citing works
Ahnaou, A., Biermans, R., & Drinkenburg, W. H. I. M. (2018) · Neural Plasticity · doi:10.1155/2018/4270263 · Cited by 17 · see citing works
Rashid, H., & Ahmed, T. (2019) · Pharmacological Reports · doi:10.1016/j.pharep.2019.02.004 · Cited by 16 · see citing works
Role of dCA3 efferents via the fimbria in the acquisition of a delay nonmatch to place task
Hunsaker, M. R., Allan, K. D., & Kesner, R. P. (2007) · Hippocampus · doi:10.1002/hipo.20288 · Cited by 16 · see citing works
Self-citationTemporal dynamics of cholinergic activity in the septo-hippocampal system
Kopsick, J. D., Hartzell, K., Lazaro, H., Nambiar, P., Hasselmo, M. E., & Dannenberg, H. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2022.957441 · Cited by 14 · see citing works
Honey and Alzheimer’s Disease—Current Understanding and Future Prospects
Shaikh, A., Ahmad, F., Teoh, S. L., Kumar, J., & Yahaya, M. F. (2023) · Antioxidants · doi:10.3390/antiox12020427 · Cited by 17 · see citing works
Paradoxical Sleep as a Tool for Understanding the Hippocampal Mechanisms of Contextual Memory
Silkis, I. G. (2009) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-009-9230-7 · Cited by 12 · see citing works
Hescham, S., Temel, Y., Casaca-Carreira, J., Arslantas, K., Yakkioui, Y., Blokland, A., & Jahanshahi, A. (2014) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2014.04.001 · Cited by 13 · see citing works
Pomara, N., Belzer, K., Sidtis, J. J., Hernando, R. T., & Pena, C. D. L. (2008) · American Journal of Geriatric Psychiatry · doi:10.1097/jgp.0b013e31815aff75 · Cited by 12 · see citing works
Liu, H., Wolters, A., Temel, Y., Alosaimi, F., Jahanshahi, A., & Hescham, S. (2022) · Neurobiology of Disease · doi:10.1016/j.nbd.2022.105797 · Cited by 11 · see citing works
Mohammed (2012) · American Journal of Applied Sciences · doi:10.3844/ajassp.2012.484.491 · Cited by 9 · see citing works
Moschonas, E. H., Capeci, H. E., Annas, E. M., Domyslawski, V. B., Steber, J. A., Donald, H. M., Genkinger, N. R., Rennerfeldt, P. L., Bittner, R. A., Vozzella, V. J., et al. (2024) · Journal of Neurotrauma · doi:10.1089/neu.2024.0173 · Cited by 8 · see citing works
Effect of sulfonamide derivatives of phenylglycine on scopolamine‐induced amnesia in rats
Ganeshpurkar, A., Singh, R., Tripathi, P., Alam, Q., Krishnamurthy, S., Kumar, A., & Singh, S. K. (2023) · Ibrain · doi:10.1002/ibra.12092 · Cited by 6 · see citing works
Acetylcholine Boosts Dendritic NMDA Spikes in a CA3 Pyramidal Neuron Model
Humphries, R., Mellor, J. R., & O’Donnell, C. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2021.11.014 · Cited by 8 · see citing works
Kassa, J., & Kunešová, G. (2006) · Neurotoxicity Research · doi:10.1007/bf03033306 · Cited by 7 · see citing works
Gómez-Ocádiz, R., Trippa, M., Posani, L., Cocco, S., Monasson, R., & Schmidt‐Hieber, C. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.02.24.432612 · Cited by 7 · see citing works
Acetylcholine‐sensitive control of long‐term synaptic potentiation in hippocampal CA3 neurons
Kassab, R. (2023) · Hippocampus · doi:10.1002/hipo.23533 · Cited by 7 · see citing works
Robles-Gómez, Á. A., Ordaz, B., Lorea-Hernández, J., & Peña-Ortega, F. (2023) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2023.1198299 · Cited by 8 · see citing works
Kniffin, A. R., Bangasser, D. A., & Parikh, V. (2023) · European Journal of Neuroscience · doi:10.1111/ejn.15999 · Cited by 6 · see citing works
- Authors
- Rogers, J. L., & Kesner, R. P.
- Affiliations
- University of Utah (US)
- Corresponding author
- Kesner, Raymond P
- Venue
- Neurobiology of Learning and Memory
- Publisher
- Elsevier BV
- Published
- 2003-11
- Volume
- 80
- Issue
- 3
- Pages
- 332-342
- ISSN
- 1074-7427 (ISSN-L)
- OpenAlex
- W2077816975
- Cited by
- 141
- References
- 32
- Citations by year
- 2026: 4 · 2025: 7 · 2024: 3 · 2023: 7 · 2022: 10 · 2021: 7 · 2020: 2 · 2019: 2 · 2018: 5 · 2017: 7 · 2016: 4 · 2015: 3 · 2014: 7 · 2013: 7 · 2012: 10
- FWCI
- 2.61
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neurobiology of Learning and Memory (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation
- National Institutes of Health
- National Institute of Mental Health (R1MH065314)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Keywords
- acetylcholine, hippocampus, spatial learning, memory encoding, memory retrieval, scopolamine, physostigmine, cholinergic modulation, memory consolidation, CA3, CA1, Hebb-Williams maze, cholinesterase inhibitors, anticholinergic agents
- MeSH terms
- Animals, Cholinergic Fibers, Cholinesterase Inhibitors, Female, Hippocampus, Learning, Memory, Physostigmine, Scopolamine, Space Perception, Muscarinic Agonists, Rats, Long-Evans, Rats
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