Augmenting saturated LTP by broadly spaced episodes of theta-burst stimulation in hippocampal area CA1 of adult rats and mice
Open accessAbstract
Hippocampal long-term potentiation (LTP) is a model system for studying cellular mechanisms of learning and memory. Recent interest in mechanisms underlying the advantage of spaced over massed learning has prompted investigation into the effects of distributed episodes of LTP induction. The amount of LTP induced in hippocampal area CA1 by one train (1T) of theta-burst stimulation (TBS) in young Sprague-Dawley rats was further enhanced by additional bouts of 1T given at 1-h intervals. However, in young Long-Evans (LE) rats, 1T did not initially saturate LTP. Instead, a stronger LTP induction paradigm using eight trains of TBS (8T) induced saturated LTP in hippocampal slices from both young and adult LE rats as well as adult mice. The saturated LTP induced by 8T could be augmented by another episode of 8T following an interval of at least 90 min. The success rate across animals and slices in augmenting LTP by an additional episode of 8T increased significantly with longer intervals between the first and last episodes, ranging from 0% at 30- and 60-min intervals to 13–66% at 90- to 180-min intervals to 90–100% at 240-min intervals. Augmentation above initially saturated LTP was blocked by the N-methyl-d-aspartate (NMDA) glutamate receptor antagonist d-2-amino-5-phosphonovaleric acid (d-APV). These findings suggest that the strength of induction and interval between episodes of TBS, as well as the strain and age of the animal, are important components in the augmentation of LTP.
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Subsequent spaced trains of theta-burst stimuli, with intervals of 60 minutes or more between trains, were needed for optimal reinforcement of LTP in rat hippocampal slices.
“subsequent spaced trains of theta-burst stimuli, with intervals of 60 minutes or more between the trains, were needed for optimal reinforcement of LTP46.”
From The right time to learn: Mechanisms and optimization of spaced learning (2016) · cites this paper as [46]
The required refractory period of about 1 hour between successive theta-burst stimuli to induce progressive increments in hippocampal LTP may be in line with the variant that short intervals are insufficient for consolidation and consequent summation of memory traces.
“The required refractory period of ~1 hour between successive theta-burst stimuli to induce progressive increments in hippocampal LTP46,47 may be in line with the first of these variants, which is that short intervals are insufficient for consolidation and consequent summation of memory traces.”
From The right time to learn: Mechanisms and optimization of spaced learning (2016) · cites this paper as [46]
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Cites
Bliss, T. V. P., & Gardner-Medwin, A. R. (1973) · The Journal of Physiology · doi:10.1113/jphysiol.1973.sp010274 · Cited by 7,460 · see citing works
Metaplasticity: the plasticity of synaptic plasticity
Abraham, W. C., & Bear, M. F. (1996) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)80018-x · Cited by 1,783 · see citing works
The physiology and pharmacology of hippocampal formation theta rhythms
Bland, B. H. (1986) · Progress in Neurobiology · doi:10.1016/0301-0082(86)90019-5 · Cited by 1,039 · see citing works
Larson, J., Wong, D., & Lynch, G. (1986) · Brain Research · doi:10.1016/0006-8993(86)90579-2 · Cited by 1,037 · see citing works
Guzowski, J. F., Lyford, G. L., Stevenson, G. D., Houston, F. P., McGaugh, J. L., Worley, P. F., & Barnes, C. A. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-11-03993.2000 · Cited by 992 · see citing works
Steward, O., Wallace, C. S., Lyford, G., & Worley, P. (1998) · Neuron · doi:10.1016/s0896-6273(00)80591-7 · Cited by 845 · see citing works
Do thin spines learn to be mushroom spines that remember?
Bourne, J., & Harris, K. M. (2007) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2007.04.009 · Cited by 843 · see citing works
Self-citationThe synaptic plasticity and memory hypothesis: encoding, storage and persistence
Takeuchi, T., Duszkiewicz, A. J., & Morris, R. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0288 · Cited by 664 · see citing works
Locally dynamic synaptic learning rules in pyramidal neuron dendrites
Harvey, C. D., & Svoboda, K. (2007) · Nature · doi:10.1038/nature06416 · Cited by 625 · see citing works
Impaired Spatial Learning after Saturation of Long-Term Potentiation
Moser, E. I., Krobert, K. A., Moser, M.-B., & Morris, R. G. M. (1998) · Science · doi:10.1126/science.281.5385.2038 · Cited by 505 · see citing works
Messaoudi, E., Kanhema, T., Soule, J. D., Tiron, A., Dagytė, G., da Silva, B., & Bramham, C. R. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2883-07.2007 · Cited by 452 · see citing works
The Influence of Prior Synaptic Activity on the Induction of Long-Term Potentiation
Huang, Y.-Y., Colino, A., Selig, D. K., & Malenka, R. C. (1992) · Science · doi:10.1126/science.1346729 · Cited by 412 · see citing works
Metaplasticity: A new vista across the field of synaptic plasticity
Abraham, W. C., & Tate, W. P. (1997) · Progress in Neurobiology · doi:10.1016/s0301-0082(97)00018-x · Cited by 354 · see citing works
Reymann, K. G., & Frey, J. U. (2007) · Neuropharmacology · doi:10.1016/j.neuropharm.2006.07.026 · Cited by 331 · see citing works
Bourne, J. N., & Harris, K. M. (2011) · Hippocampus · doi:10.1002/hipo.20768 · Cited by 318 · see citing works
Self-citationLocal protein synthesis, actin dynamics, and LTP consolidation
Bramham, C. R. (2008) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2008.09.013 · Cited by 301 · see citing works
Über das Gedächtnis. Untersuchungen zur experimentellen Psychologie
Ebbinghaus, H. (2018) · Cited by 286 · see citing works
Developmental onset of long‐term potentiation in area CA1 of the rat hippocampus.
Harris, K. M., & Teyler, T. J. (1984) · The Journal of Physiology · doi:10.1113/jphysiol.1984.sp015005 · Cited by 252 · see citing works
Self-citationA Unified Model of the Presynaptic and Postsynaptic Changes During LTP at CA1 Synapses
Lisman, J., & Raghavachari, S. (2006) · Science's STKE · doi:10.1126/stke.3562006re11 · Cited by 241 · see citing works
A cellular mechanism for targeting newly synthesized mRNAs to synaptic sites on dendrites
Steward, O., & Worley, P. F. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.131146398 · Cited by 225 · see citing works
Independent Sources of Quantal Variability at Single Glutamatergic Synapses
Franks, K. M., Stevens, C. F., & Sejnowski, T. J. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-08-03186.2003 · Cited by 224 · see citing works
LTP saturation and spatial learning disruption: effects of task variables and saturation levels
Barnes, C. A., Jung, M., McNaughton, B. L., Korol, D., Andreasson, K. I., & Worley, P. F. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-10-05793.1994 · Cited by 219 · see citing works
Pharmacology of Ampakine Modulators: From AMPA Receptors to Synapses and Behavior
Arai, A., & Kessler, M. (2007) · Current Drug Targets · doi:10.2174/138945007780618490 · Cited by 211 · see citing works
Synaptic evidence for the efficacy of spaced learning
Kramár, E. A., Babayan, A. H., Gavin, C. F., Cox, C. D., Jafari, M., Gall, C. M., Rumbaugh, G., & Lynch, G. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1120700109 · Cited by 192 · see citing works
A Monte Carlo Model Reveals Independent Signaling at Central Glutamatergic Synapses
Franks, K. M., Bartol, T. M., & B, T. J. S. A. (2002) · Biophysical Journal · doi:10.1016/s0006-3495(02)75248-x · Cited by 175 · see citing works
Lynch, M. A. (1998) · Progress in Neurobiology · doi:10.1016/s0301-0082(98)00054-9 · Cited by 171 · see citing works
Heterosynaptic metaplasticity in the hippocampus in vivo : A BCM-like modifiable threshold for LTP
Abraham, W. C., Mason‐Parker, S. E., Bear, M. F., Webb, S. V., & Tate, W. P. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.181342098 · Cited by 170 · see citing works
Foster, T. C. (2012) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2012.01.007 · Cited by 159 · see citing works
Steward, O. (2002) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2002.4102 · Cited by 152 · see citing works
Chapter 17 Chapter The nature and causes of hippocampal long-term potentiation
LYNCH, G. S., Kessler, M., Arai, A., & Larson, J. (1990) · Progress in brain research · doi:10.1016/s0079-6123(08)61253-4 · Cited by 140 · see citing works
Bliss, T. V. P., & Lømo, T. (1973) · The Journal of Physiology · doi:10.1113/jphysiol.1973.sp010273 · Cited by 135 · see citing works
Selective immunolesions of hippocampal cholinergic input fail to impair spatial working memory
McMahan, R. W., Sobel, T. J., & Baxter, M. G. (1997) · Hippocampus · doi:10.1002/(sici)1098-1063(1997)7:2 · Cited by 109 · see citing works
Anatomical and Electrophysiological Comparison of CA1 Pyramidal Neurons of the Rat and Mouse
Routh, B. N., Johnston, D., Harris, K. M., & Chitwood, R. A. (2009) · Journal of Neurophysiology · doi:10.1152/jn.00082.2009 · Cited by 103 · see citing works
Self-citationFields, R. D. (2005) · Scientific American · doi:10.1038/scientificamerican0205-74 · Cited by 101 · see citing works
Lynch, G., Kramár, E. A., Babayan, A. H., Rumbaugh, G., & Gall, C. M. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.07.006 · Cited by 97 · see citing works
Synaptic plasticity in early aging
LYNCH, G. S., Rex, C. S., & Gall, C. M. (2006) · Ageing Research Reviews · doi:10.1016/j.arr.2006.03.008 · Cited by 97 · see citing works
Jensen, F. E., & Harris, K. M. (1989) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(89)90146-5 · Cited by 93 · see citing works
Self-citationFrey, U., Schollmeier, K., Reymann, K. G., & Seidenbecher, T. (1995) · Neuroscience · doi:10.1016/0306-4522(95)00117-2 · Cited by 93 · see citing works
Integrin Dynamics Produce a Delayed Stage of Long-Term Potentiation and Memory Consolidation
Babayan, A. H., Kramár, E. A., Barrett, R. M., Jafari, M., Häettig, J., Chen, L. Y., Rex, C. S., Lauterborn, J. C., Wood, M. A., Gall, C. M., et al. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.2024-12.2012 · Cited by 93 · see citing works
Rapid manifestation of reactive astrogliosis in acute hippocampal brain slices
Takano, T., He, W. J., Han, X., Wang, F., Xu, Q., Wang, X., Bush, N. A. O., Cruz, N. F., Dienel, G. A., & Nedergaard, M. (2013) · Glia · doi:10.1002/glia.22588 · Cited by 88 · see citing works
Kirov, S. A., Goddard, C. A., & Harris, K. M. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2004.07.039 · Cited by 87 · see citing works
Self-citationAge differences in a circadian influence on hippocamapl LTP
Harris, K. M., & Teyler, T. J. (1983) · Brain Research · doi:10.1016/0006-8993(83)91284-2 · Cited by 85 · see citing works
Self-citationA molecular brake controls the magnitude of long-term potentiation
Wang, Y., Zhu, G., Briz, V., Hsu, Y., Bi, X., & Baudry, M. (2014) · Nature Communications · doi:10.1038/ncomms4051 · Cited by 82 · see citing works
Nanoscale analysis of structural synaptic plasticity
Bourne, J. N., & Harris, K. M. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.10.019 · Cited by 78 · see citing works
Self-citationYoung, J. Z., & Nguyen, P. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0909-05.2005 · Cited by 76 · see citing works
Bell, M. E., Bourne, J. N., Chirillo, M. A., Mendenhall, J. M., Kuwajima, M., & Harris, K. M. (2014) · Journal of Comparative Neurology · doi:10.1002/cne.23646 · Cited by 72 · see citing works
Self-citationBarr, D., Lambert, N., Hoyt, K., Moore, S., & Wilson, W. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-07-05402.1995 · Cited by 70 · see citing works
Bourne, J. N., Sorra, K. E., Hurlburt, J. L., & Harris, K. M. (2006) · Hippocampus · doi:10.1002/hipo.20238 · Cited by 70 · see citing works
Self-citationDiana, G., Domenici, M. R., Loizzo, A., de Carolis, A. S., & Sagratella, S. (1994) · Neuroscience Letters · doi:10.1016/0304-3940(94)90618-1 · Cited by 66 · see citing works
Bourne, J. N., Chirillo, M. A., & Harris, K. M. (2013) · The Journal of Comparative Neurology · doi:10.1002/cne.23384 · Cited by 65 · see citing works
Self-citationBowden, J. B., Abraham, W. C., & Harris, K. (2011) · Hippocampus · doi:10.1002/hipo.20972 · Cited by 62 · see citing works
Self-citationCao, G., & Harris, K. M. (2011) · Journal of Neurophysiology · doi:10.1152/jn.00780.2011 · Cited by 47 · see citing works
Self-citationJackson, P., Suppes, T., & Harris, K. (1993) · Journal of Neurophysiology · doi:10.1152/jn.1993.70.4.1412 · Cited by 46 · see citing works
Self-citationYilmaz, E., Miyamae, T., Braun, A. E., & Thiels, E. (2010) · Hippocampus · doi:10.1002/hipo.20838 · Cited by 41 · see citing works
Bourne, J. N., Kirov, S. A., Sorra, K. E., & Harris, K. M. (2006) · Neuropharmacology · doi:10.1016/j.neuropharm.2006.06.020 · Cited by 40 · see citing works
Self-citationManahan‐Vaughan, D. (2000) · Neuropharmacology · doi:10.1016/s0028-3908(00)00016-2 · Cited by 38 · see citing works
Manahan‐Vaughan, D., & Schwegler, H. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00007 · Cited by 31 · see citing works
Mechanism based approaches for rescuing and enhancing cognition
LYNCH, G. S. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00143 · Cited by 30 · see citing works
SnapShot: Local Protein Translation in Dendrites
Dieck, S. T., Hanus, C., & Schuman, E. M. (2014) · Neuron · doi:10.1016/j.neuron.2014.02.009 · Cited by 25 · see citing works
MOONEY, R. D., Crnko-Hoppenjans, T. A., Ke, M., Bennett‐Clarke, C. A., Lane, R. D., Chiaia, N. L., & Rhoades, R. W. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980330)393:1 · Cited by 20 · see citing works
Self-citationHabib, D., Tsui, C. K. Y., Rosen, L. G., & Dringenberg, H. C. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht174 · Cited by 15 · see citing works
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Stanford Neuromodulation Therapy (SNT): A Double-Blind Randomized Controlled Trial
Cole, E. J., Phillips, A. L., Bentzley, B. S., Stimpson, K. H., Nejad, R., Barmak, F., Veerapal, C., Khan, N., Cherian, K., Felber, E., et al. (2022) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2021.20101429 · Cited by 795 · see citing works
The right time to learn: Mechanisms and optimization of spaced learning
Smolen, P., Zhang, Y., & Byrne, J. H. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2015.18 · Cited by 326 · see citing works
Form and function of sleep spindles across the lifespan
Clawson, B. C., Durkin, J., & Aton, S. J. (2016) · Neural Plasticity · doi:10.1155/2016/6936381 · Cited by 178 · see citing works
“This represents a significant gap in the literature, as puberty and adolescence are times of significant change in both body and brain development,marking the transition from childhood to adulthood.”
BackgroundDirect current stimulation boosts hebbian plasticity in vitro
Kronberg, G., Rahman, A., Sharma, M., Bikson, M., & Parra, L. C. (2019) · Brain stimulation · doi:10.1016/j.brs.2019.10.014 · Cited by 153 · see citing works
Smith, H., Bourne, J. N., Cao, G., Chirillo, M. A., Ostroff, L. E., Watson, D. J., & Harris, K. M. (2016) · eLife · doi:10.7554/elife.15275 · Cited by 146 · see citing works
Self-citationChirillo, M. A., Waters, M. S., Lindsey, L. F., Bourne, J. N., & Harris, K. M. (2019) · Scientific Reports · doi:10.1038/s41598-019-40520-x · Cited by 84 · see citing works
Self-citationPatriarchi, T., Buonarati, O. R., & Hell, J. W. (2018) · The EMBO Journal · doi:10.15252/embj.201899771 · Cited by 65 · see citing works
Long-term potentiation expands information content of hippocampal dentate gyrus synapses
Bromer, C., Bartol, T. M., Bowden, J. B., Hubbard, D. D., Hanka, D. C., Gonzalez, P. V., Kuwajima, M., Mendenhall, J. M., Parker, P. H., Abraham, W. C., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1716189115 · Cited by 59 · see citing works
Self-citationAccelerated intermittent theta burst stimulation in major depressive disorder: A systematic review.
Neuteboom, D., Zantvoord, J., Goya-Maldonado, R., Wilkening, J., Dols, A., van Exel, E. V., Lok, A., de Haan, L., & Scheepstra, K. (2023) · Psychiatry Research · doi:10.1016/j.psychres.2023.115429 · Cited by 54 · see citing works
Sex differences in synaptic plasticity underlying learning
Gall, C. M., Le, A. A., & LYNCH, G. S. (2021) · Journal of Neuroscience Research · doi:10.1002/jnr.24844 · Cited by 59 · see citing works
LTP enhances synaptogenesis in the developing hippocampus
Watson, D. J., Ostroff, L. E., Cao, G., Parker, P. H., Smith, H., & Harris, K. M. (2015) · Hippocampus · doi:10.1002/hipo.22536 · Cited by 54 · see citing works
Self-citationSpaced training rescues memory and ERK1/2 signaling in fragile X syndrome model mice
Seese, R. R., Wang, K., Yao, Y. Q., Lynch, G., & Gall, C. M. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1413335111 · Cited by 52 · see citing works
Hedrick, N. G., & Yasuda, R. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.06.002 · Cited by 53 · see citing works
Thomson, A. C., & Sack, A. T. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.599918 · Cited by 55 · see citing works
Sohn, M. N., Brown, J. C., Sharma, P., Ziemann, U., & McGirr, A. (2024) · Journal of Psychiatry and Neuroscience · doi:10.1503/jpn.230090 · Cited by 37 · see citing works
Cui, H., Ding, H., Hu, L., Zhao, Y., Shu, Y., & Voon, V. (2024) · Psychological Medicine · doi:10.1017/s0033291724002289 · Cited by 25 · see citing works
Wrightson, J. G., Cole, J., Sohn, M. N., & McGirr, A. (2023) · Neuropsychopharmacology · doi:10.1038/s41386-023-01575-7 · Cited by 23 · see citing works
Synapse-specific structural plasticity that protects and refines local circuits during LTP and LTD
Harris, K. M., Kuwajima, M., Flores, J. C., & Zito, K. (2024) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2023.0224 · Cited by 22 · see citing works
Self-citationMaking a lecture stick: The Effect of spaced instruction on knowledge retention in medical education
Timmer, M. C. J., Steendijk, P., Arend, S. M., & Versteeg, M. (2020) · Medical Science Educator · doi:10.1007/s40670-020-00995-0 · Cited by 20 · see citing works
Harris, K. M. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0735-19.2019 · Cited by 21 · see citing works
Self-citationDevelopmental onset of enduring long‐term potentiation in mouse hippocampus
Ostrovskaya, O. I., Cao, G., Eroğlu, Ç., & Harris, K. M. (2020) · Hippocampus · doi:10.1002/hipo.23257 · Cited by 15 · see citing works
Self-citationMarques, M., Reyes-García, S. Z., da Silva, J. E. M. C., Lopes-Silva, L. B., Andersen, M. L., Cavalheiro, É. A., Scorza, F. A., & Scorza, C. A. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00002 · Cited by 13 · see citing works
Goldenkoff, E. R., Deluisi, J. A., Lee, T. G., Hampstead, B. M., Taylor, S. F., Polk, T. A., & Vesia, M. (2024) · Clinical Neurophysiology · doi:10.1016/j.clinph.2024.08.005 · Cited by 9 · see citing works
Synaptic priming: A framework for pharmacotherapy in depression
Brown, K. A., Ajibola, M. I., Medeiros, G. C., & Gould, T. D. (2025) · Neuron · doi:10.1016/j.neuron.2025.09.010 · Cited by 9 · see citing works
Zhang, T. R., Askari, B., Kesici, A., Guilherme, E. M., Vila‐Rodriguez, F., & Snyder, J. S. (2022) · European Journal of Neuroscience · doi:10.1111/ejn.15891 · Cited by 9 · see citing works
Contributions of site- and sex-specific LTPs to everyday memory
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A synapse-specific refractory period for plasticity at individual dendritic spines
Flores, J. C., Sarkar, D., & Zito, K. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2410433122 · Cited by 8 · see citing works
Bakulin, I. S., Poydasheva, A. G., Zabirova, A. K., Suponeva, N. A., & Пирадов, М. А. (2022) · Annals of Clinical and Experimental Neurology · doi:10.54101/acen.2022.3.9 · Cited by 7 · see citing works
Pre- versus Post-synaptic Forms of LTP in Two Branches of the Same Hippocampal Afferent
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Panda, R., Deluisi, J. A., Lee, T. G., Davis, S., Muñoz-Orozco, I., Albin, R. L., & Vesia, M. (2024) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2024.1445595 · Cited by 6 · see citing works
Brosens, N., Simon, C., Kessels, H. W. H. G., Lucassen, P. J., & Krugers, H. J. (2023) · Journal of Neuroendocrinology · doi:10.1111/jne.13346 · Cited by 5 · see citing works
Phenobarbital does not worsen outcomes of neonatal hypoxia on hippocampal LTP on rats
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Bakulin, I. S., Poydasheva, A. G., Zabirova, A. K., Lagoda, D. Y., Rimkevichus, A. A., Zakharova, M. N., Suponeva, N. A., & Пирадов, М. А. (2022) · Neuromuscular Diseases · doi:10.17650/2222-8721-2022-12-3-26-35 · Cited by 3 · see citing works
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Moreno, A. R., & Paulsen, O. (2026) · Physiological Reviews · doi:10.1152/physrev.00028.2025 · Cited by 2 · see citing works
Liu, M., Jin, S., Liu, M., Yang, B., Wang, Q., Fan, C., Li, Z., & Wu, L. (2024) · Frontiers in Neurology · doi:10.3389/fneur.2024.1469877 · Cited by 2 · see citing works
Kirk, L. M., & Harris, K. M. (2016) · Encyclopedia of Life Sciences · doi:10.1002/9780470015902.a0000093.pub3 · Cited by 1 · see citing works
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LYNCH, G. S., & Gall, C. M. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.21109-7
Thomson, A. C. (2021) · doi:10.26481/dis.20210521at
Koçyiğit, D., Canpolat, İ. K. N., & Gürel, Ş. C. (2026) · Psychiatry Investigation · doi:10.30773/pi.2024.0215
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- Authors
- Cao, G., & Harris, K. M.
- Affiliations
- The University of Texas at Austin (US)
- Corresponding author
- Harris, Kristen M.
- Venue
- Journal of Neurophysiology
- Publisher
- American Physiological Society
- Published
- 2014-10-15
- Volume
- 112
- Issue
- 8
- Pages
- 1916-1924
- ISSN
- 0022-3077 (ISSN-L)
- 1522-1598
- PMC
- PMC4200006
- OpenAlex
- W2333605426
- Cited by
- 41
- References
- 60
- Citations by year
- 2026: 4 · 2025: 2 · 2024: 8 · 2023: 4 · 2022: 3 · 2021: 3 · 2020: 4 · 2019: 2 · 2018: 3 · 2017: 2 · 2016: 4 · 2015: 1 · 2014: 1
- FWCI
- 1.22
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Neurophysiology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (MH-095980, R01MH095980, R01MH104319)
- National Institute of Neurological Disorders and Stroke (NS21184, R01NS074644, R37NS021184, NS074644)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Neurology › Transcranial Magnetic Stimulation Studies
- Keywords
- long-term potentiation, theta burst stimulation, hippocampal CA1, NMDA receptor, D-APV, strain differences, age effects, learning and memory
- MeSH terms
- Age Factors, Animals, Electric Stimulation, Male, Mice, Inbred C57BL, Species Specificity, Time Factors, Rats, Sprague-Dawley, Long-Term Potentiation, Rats, Long-Evans, Mice, Rats, CA1 Region, Hippocampal
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