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Theta-burst LTP

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Larson, John, Munkácsy, Erin·2015·Brain Research

DOI 10.1016/j.brainres.2014.10.034PMC PMC4411212

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Abstract

This review covers the spatial and temporal rules governing induction of hippocampal long-term potentiation (LTP) by theta-burst stimulation. Induction of LTP in field CA1 by high frequency stimulation bursts that resemble the burst discharges (complex-spikes) of hippocampal pyramidal neurons involves a multiple-step mechanism. A single burst is insufficient for LTP induction because it evokes both excitatory and inhibitory currents that partially cancel and limit postsynaptic depolarization. Bursts repeated at the frequency (~5 Hz) of the endogenous theta rhythm induce maximal LTP, primarily because this frequency disables feed-forward inhibition and allows sufficient postsynaptic depolarization to activate voltage-sensitive NMDA receptors. The disinhibitory process, referred to as "priming", involves presynaptic GABA autoreceptors that inhibit GABA release. Activation of NMDA receptors allows a calcium flux into dendritic spines that serves as the proximal trigger for LTP. We include new data showing that theta-burst stimulation is more efficient than other forms of stimulation for LTP induction. In addition, we demonstrate that associative interactions between synapses activated during theta-bursts are limited to major dendritic domains since such interactions occur within apical or basal dendritic trees but not between them. We review evidence that recordings of electrophysiological responses during theta burst stimulation can help to determine if experimental manipulations that affect LTP do so by affecting events antecedent to the induction process, such as NMDA receptor activation, or downstream signaling cascades that result from postsynaptic calcium fluxes. Finally, we argue that theta-burst LTP represents a minimal model for stable, non-decremental LTP that is more sensitive to a variety of experimental manipulations than is LTP induced by other stimulation paradigms. This article is part of a Special Issue entitled SI: Brain and Memory.

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Long‐lasting potentiation of synaptic transmission in the dentate area of the unanaesthetized rabbit following stimulation of the perforant path
Bliss, T. V. P., & Gardner-Medwin, A. R. (1973) · The Journal of Physiology · doi:10.1113/jphysiol.1973.sp010274 · Cited by 7,424
The hippocampus as a cognitive map
Passingham, R. E. (1979) · Neuroscience · doi:10.1016/0306-4522(79)90015-0 · Cited by 5,128
Theta Burst Stimulation of the Human Motor Cortex
Huang, Y.-Z., Edwards, M. J., Rounis, E., Bhatia, K. P., & Rothwell, J. C. (2005) · Neuron · doi:10.1016/j.neuron.2004.12.033 · Cited by 4,158
Hippocampal electrical activity and voluntary movement in the rat
Vanderwolf, C. H. (1969) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(69)90092-3 · Cited by 1,928
HIPPOCAMPAL ELECTRICAL ACTIVITY IN AROUSAL
Green, J. D., & Arduini, A. (1954) · Journal of Neurophysiology · doi:10.1152/jn.1954.17.6.533 · Cited by 1,396
Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats
Ranck, J. B. (1973) · Experimental Neurology · doi:10.1016/0014-4886(73)90290-2 · Cited by 1,322
Cleavage of proBDNF by tPA/Plasmin Is Essential for Long-Term Hippocampal Plasticity
Pang, P. T., Teng, H. K., Zaitsev, E., Woo, N. T., Sakata, K., Zhen, S., Teng, K. K., Yung, W.-H., Hempstead, B. L., & Lu, B. (2004) · Science · doi:10.1126/science.1100135 · Cited by 1,136
The Spike-Timing Dependence of Plasticity
Feldman, D. E. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.001 · Cited by 1,071
Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation
Larson, J., Wong, D., & Lynch, G. (1986) · Brain Research · doi:10.1016/0006-8993(86)90579-2 · Cited by 1,037
Self-citation
Analysis of Sniffing of the Albino Rat 1)
Welker, W. (1964) · Behaviour · doi:10.1163/156853964x00030 · Cited by 845
Two components of long-term potentiation induced by different patterns of afferent activation
Grover, L. M., & Teyler, T. J. (1990) · Nature · doi:10.1038/347477a0 · Cited by 708
Paired‐pulse depression of monosynaptic GABA‐mediated inhibitory postsynaptic responses in rat hippocampus.
Davies, C. H., Davies, S. N., & Collingridge, G. L. (1990) · The Journal of Physiology · doi:10.1113/jphysiol.1990.sp018080 · Cited by 702
Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation
Diamond, D. M., Bennett, M. C., Fleshner, M., & Rose, G. M. (1992) · Hippocampus · doi:10.1002/hipo.450020409 · Cited by 688
Intrinsic Oscillations of Neocortex Generated by Layer 5 Pyramidal Neurons
Silva, L. R., Amitai, Y., & Connors, B. W. (1991) · Science · doi:10.1126/science.1824881 · Cited by 682
GABAB autoreceptors regulate the induction of LTP
Davies, C. H., Starkey, S. J., Pozza, M. F., & Collingridge, G. L. (1991) · Nature · doi:10.1038/349609a0 · Cited by 615
Induction of synaptic potentiation in hippocampus by patterned stimulation involves two events
Larson, J., & Lynch, G. (1986) · Science · doi:10.1126/science.3704635 · Cited by 597 · cited 4×
“The first clue was that either a single burst or multiple bursts repeated at long intervals (Z2 s) were almost always ineffective (Larson and Lynch, 1986; Rose and Dunwiddie, 1986).”
BackgroundInfluentialSelf-citation
Water associated zero maze: a novel rat test for long term traumatic re-experiencing
Ritov, G., & Richter‐Levin, G. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00001 · Cited by 580
Hebbian synapses in hippocampus.
Kelso, S. R., Ganong, A. H., & Brown, T. H. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.14.5326 · Cited by 555
Feed‐forward dendritic inhibition in rat hippocampal pyramidal cells studied in vitro
Alger, B. E., & Nicoll, R. A. (1982) · The Journal of Physiology · doi:10.1113/jphysiol.1982.sp014255 · Cited by 528
Long-term potentiation of the perforant path-granule cell synapse in the rat hippocampus
Douglas, R. M., & Goddard, G. V. (1975) · Brain Research · doi:10.1016/0006-8993(75)90697-6 · Cited by 521
Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of θ-rhythm
Pavlides, C., Greenstein, Y. J., Grudman, M., & Winson, J. (1988) · Brain Research · doi:10.1016/0006-8993(88)91499-0 · Cited by 485
Neurotrophins and Time: Different Roles for TrkB Signaling in Hippocampal Long-Term Potentiation
Kang, H., Welcher, A. A., Shelton, D., & Schuman, E. M. (1997) · Neuron · doi:10.1016/s0896-6273(00)80378-5 · Cited by 481
Co-regulation of long-term potentiation and experience-dependent synaptic plasticity in visual cortex by age and experience
Kirkwood, A., Lee, H., & Bear, M. F. (1995) · Nature · doi:10.1038/375328a0 · Cited by 430
Stimulation on the Positive Phase of Hippocampal Theta Rhythm Induces Long-Term Potentiation That Can Be Depotentiated by Stimulation on the Negative Phase in Area CA1 In Vivo
Hölscher, C., Anwyl, R., & Rowan, M. J. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-16-06470.1997 · Cited by 411
Stimulation in Hippocampal Region CA1 in Behaving Rats Yields Long-Term Potentiation when Delivered to the Peak of Theta and Long-Term Depression when Delivered to the Trough
Hyman, J. M., Wyble, B., Goyal, V., Rossi, C. A., & Hasselmo, M. E. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-37-11725.2003 · Cited by 404
Stable hippocampal long-term potentiation elicited by ‘theta’ pattern stimulation
Staubli, U. V., & LYNCH, G. S. (1987) · Brain Research · doi:10.1016/0006-8993(87)91605-2 · Cited by 353
The Dendritic Branch Is the Preferred Integrative Unit for Protein Synthesis-Dependent LTP
Govindarajan, A., Israely, I., Huang, S.-Y., & Tonegawa, S. (2011) · Neuron · doi:10.1016/j.neuron.2010.12.008 · Cited by 349
Some Forms of cAMP-Mediated Long-Lasting Potentiation Are Associated with Release of BDNF and Nuclear Translocation of Phospho-MAP Kinase
Patterson, S. L., Pittenger, C., Morozov, A., Martin, K. C., Scanlin, H., Drake, C., & Kandel, E. R. (2001) · Neuron · doi:10.1016/s0896-6273(01)00443-3 · Cited by 334
Facilitation of the Induction of Long-term Potentiation by GABA B Receptors
Mott, D. D., & Lewis, D. V. (1991) · Science · doi:10.1126/science.1675489 · Cited by 331
Learning‐related patterns of CA1 spike trains parallel stimulation parameters optimal for inducing hippocampal long‐term potentiation
Otto, T., Eichenbaum, H., Wible, C. G., & Wiener, S. I. (1991) · Hippocampus · doi:10.1002/hipo.450010206 · Cited by 311
Cross-frequency interaction of the eye-movement related LFP signals in V1 of freely viewing monkeys
Ito, J., Maldonado, P., & Grün, S. (2013) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2013.00001 · Cited by 309
Use-dependent depression of IPSPs in rat hippocampal pyramidal cells in vitro
McCarren, M., & Alger, B. E. (1985) · Journal of Neurophysiology · doi:10.1152/jn.1985.53.2.557 · Cited by 295
Exposure to Acute Stress Blocks the Induction of Long-Term Potentiation of the Amygdala–Prefrontal Cortex Pathway In Vivo
Maroun, M., & Richter-Levin, G. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-11-04406.2003 · Cited by 293
Alterations in synaptic transmission and long-term potentiation in hippocampal slices from young and aged PDAPP mice
Larson, J., LYNCH, G. S., Games, D., & Seubert, P. A. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01698-4 · Cited by 291
Self-citation
Temporal relationship between sniffing and the limbic theta rhythm during odor discrimination reversal learning
Macrides, F., Eichenbaum, H., & Forbes, W. B. (1982) · Journal of Neuroscience · doi:10.1523/jneurosci.02-12-01705.1982 · Cited by 278
Associative long-term potentiation in hippocampal slices.
Barrionuevo, G., & Brown, T. H. (1983) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.80.23.7347 · Cited by 273
Dose-Dependent Effects of Theta Burst rTMS on Cortical Excitability and Resting-State Connectivity of the Human Motor System
Nettekoven, C., Volz, L. J., Kutscha, M., Pool, E.-M., Rehme, A. K., Eickhoff, S. B., Fink, G. R., & Grefkes, C. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.4993-13.2014 · Cited by 264
Role of N-methyl-D-aspartate receptors in the induction of synaptic potentiation by burst stimulation patterned after the hippocampal θ-rhythm
Larson, J., & LYNCH, G. S. (1988) · Brain Research · doi:10.1016/0006-8993(88)91388-1 · Cited by 245
Self-citation
Relative Contribution of Endogenous Neurotrophins in Hippocampal Long-Term Potentiation
Chen, G., Kolbeck, R., Barde, Y., Bonhoeffer, T., & Kossel, A. H. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-18-07983.1999 · Cited by 243
Induction of hippocampal long-term potentiation using physiologically patterned stimulation
Rose, G., & Dunwiddie, T. V. (1986) · Neuroscience Letters · doi:10.1016/0304-3940(86)90487-8 · Cited by 238
Long-Term Potentiation of Thalamocortical Transmission in the Adult Visual CortexIn Vivo
Heynen, A. J., & Bear, M. F. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-24-09801.2001 · Cited by 220
Effects of 5-HT3 receptor antagonism on hippocampal theta rhythm, memory, and LTP induction in the freely moving rat
Staubli, U. V., & Xu, F. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-03-02445.1995 · Cited by 219
Characteristics of hippocampal primed burst potentiation in vitro and in the awake rat
Diamond, D. M., Dunwiddie, T., & Rose, G. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-11-04079.1988 · Cited by 218
Long-term potentiation : a debate of current issues
Baudry, M., & Davis, J. L. (1991) · Cited by 216
A General Model of Synaptic Transmission and Short-Term Plasticity
Pan, B., & Zucker, R. S. (2009) · Neuron · doi:10.1016/j.neuron.2009.03.025 · Cited by 195
Factors regulating the magnitude of long-term potentiation induced by theta pattern stimulation
Arai, A., & LYNCH, G. S. (1992) · Brain Research · doi:10.1016/0006-8993(92)90181-8 · Cited by 192
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
Sniffing and whisking in rodents
Deschênes, M., Moore, J., & Kleinfeld, D. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.11.013 · Cited by 186
Hippocampal plasticity induced by primed burst, but not long‐term potentiation, stimulation is impaired in area CA1 of aged fischer 344 rats
Moore, C. I., Browning, M. D., & Rose, G. M. (1993) · Hippocampus · doi:10.1002/hipo.450030106 · Cited by 184
Lonf-term potentiation in the dentate gyrus is preferentially induced at theta rhythm periodicity
Greenstein, Y. J., Pavlides, C., & Winson, J. (1988) · Brain Research · doi:10.1016/0006-8993(88)91358-3 · Cited by 184
Psychological stress repeatedly blocks hippocampal primed burst potentiation in behaving rats
Diamond, D. M., Fleshner, M., & Rose, G. M. (1994) · Behavioural Brain Research · doi:10.1016/0166-4328(94)90032-9 · Cited by 182
Endogenous Serine Protease Inhibitor Modulates Epileptic Activity and Hippocampal Long-Term Potentiation
Lüthi, A., van der Putten, H., Botteri, F., Mansuy, I., Meins, M., Frey, U., Sansig, G., Portet, C., Schmutz, M., Schröder, M. S., et al. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-12-04688.1997 · Cited by 176
Evidence for synaptic potentiation in a cortical network during learning
Roman, F. S., Staubli, U. V., & LYNCH, G. S. (1987) · Brain Research · doi:10.1016/0006-8993(87)90089-8 · Cited by 174
Impairment of L-type Ca2+Channel-Dependent Forms of Hippocampal Synaptic Plasticity in Mice Deficient in the Extracellular Matrix Glycoprotein Tenascin-C
Evers, M. R., Salmen, B., Bukalo, O., Rollenhagen, A., Bösl, M. R., Morellini, F., Bartsch, U., Dityatev, A., & Schachner, M. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-16-07177.2002 · Cited by 172
Hippocampal long-lasting potentiation produced by pairing single volleys and brief conditioning tetani evoked in separate afferents
Gustafsson, B., & Wigström, H. (1986) · Journal of Neuroscience · doi:10.1523/jneurosci.06-06-01575.1986 · Cited by 168
Differential Conditioning of Associative Synaptic Enhancement in Hippocampal Brain Slices
Kelso, S. R., & Brown, T. H. (1986) · Science · doi:10.1126/science.3952501 · Cited by 167
Alterations of Endocannabinoid Signaling, Synaptic Plasticity, Learning, and Memory in Monoacylglycerol Lipase Knock-out Mice
Pan, B., Wang, W., Zhong, P., Blankman, J. L., Cravatt, B. F., & Liu, Q.-S. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2075-11.2011 · Cited by 160
NMDA-dependent induction of long-term potentiation in afferent and association fiber systems of piriform cortex in vitro
Kanter, E. D., & Haberly, L. B. (1990) · Brain Research · doi:10.1016/0006-8993(90)91337-g · Cited by 158
Long-Term Potentiation Is Impaired in Middle-Aged Rats: Regional Specificity and Reversal by Adenosine Receptor Antagonists
Rex, C. S., Kramár, E. A., Colgin, L. L., Lin, B., Gall, C. M., & LYNCH, G. S. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0880-05.2005 · Cited by 144
Serotonin blocks the long-term potentiation induced by primed burst stimulation in the CA1 region of rat hippocampal slices
Corradetti, R., Ballerini, L., Pugliese, A. M., & Pepeu, G. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90140-w · Cited by 141
Impairment of Select Forms of Spatial Memory and Neurotrophin-Dependent Synaptic Plasticity by Deletion of Glial Aquaporin-4
Skucas, V. A., Mathews, I. B., Yang, J., Cheng, Q., Treister, A. K., Duffy, Á., Verkman, A. S., Hempstead, B. L., Wood, M. A., Binder, D. K., et al. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.6249-10.2011 · Cited by 138
Saccades during visual exploration align hippocampal 3–8 Hz rhythms in human and non-human primates
Hoffman, K. L., Dragan, M. C., Leonard, T. K., Micheli, C., Montefusco‐Siegmund, R., & Valiante, T. A. (2013) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2013.00043 · Cited by 137
Theta pattern stimulation and the induction of LTP: the sequence in which synapses are stimulated determines the degree to which they potentiate
Larson, J., & LYNCH, G. S. (1989) · Brain Research · doi:10.1016/0006-8993(89)90007-3 · Cited by 128
Self-citation
Hippocampal synaptic plasticity is modulated by theta rhythm in the fascia dentata of adult and aged freely behaving rats
Orr, G. W., RAO, G. R., Houston, F. P., McNaughton, B. L., & Barnes, C. A. (2001) · Hippocampus · doi:10.1002/hipo.1079 · Cited by 125
Hippocampal excitability phase-locked to the theta rhythm in walking rats
Rudell, A. P., Fox, S. E., & Ranck, J. B. (1980) · Experimental Neurology · doi:10.1016/0014-4886(80)90068-0 · Cited by 122
Theta burst stimulation is optimal for induction of LTP at both apical and basal dendritic synapses on hippocampal CA1 neurons
Capocchi, G., Zampolini, M., & Larson, J. (1992) · Brain Research · doi:10.1016/0006-8993(92)91715-q · Cited by 121
Self-citation
Theta reset produces optimal conditions for long‐term potentiation
McCartney, H., Johnson, A. D., Weil, Z. M., & Givens, B. S. (2004) · Hippocampus · doi:10.1002/hipo.20019 · Cited by 117
Temporal relationships between hippocampal slow waves and exploratory sniffing in hamsters
Macrides, F. (1975) · Behavioral Biology · doi:10.1016/s0091-6773(75)90419-8 · Cited by 116
Short-term synaptic enhancement and long-term potentiation in neocortex.
Castro‐Alamancos, M. A., & Connors, B. W. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.3.1335 · Cited by 116
The olfactory bulb theta rhythm follows all frequencies of diaphragmatic respiration in the freely behaving rat
Rojas‐Líbano, D., Frederick, D. E., EgaÃ±a, J. I., & Kay, L. M. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00214 · Cited by 111
Benzodiazepines block long-term potentiation in slices of hippocampus and piriform cortex
del Cerro, S., Jung, M., & Lynch, G. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90071-9 · Cited by 106
Neocortical Long-Term Potentiation and Experience-Dependent Synaptic Plasticity Require α-Calcium/Calmodulin-Dependent Protein Kinase II Autophosphorylation
Hardingham, N. R., Glazewski, S., Pakhotin, P. I., Mizuno, K., Chapman, P. F., Giese, K.-P., & Fox, K. D. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-11-04428.2003 · Cited by 101
Long‐term potentiation of monosynaptic EPSPS in rat piroform cortex in vitro
Jung, M., Larson, J., & Lynch, G. (1990) · Synapse · doi:10.1002/syn.890060307 · Cited by 101
Self-citation
Differences between synaptic plasticity thresholds result in new timing rules for maximizing long-term potentiation
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
Enhanced intrinsic excitability and EPSP-spike coupling accompany enriched environment-induced facilitation of LTP in hippocampal CA1 pyramidal neurons
Malik, R., & Chattarji, S. (2011) · Journal of Neurophysiology · doi:10.1152/jn.01009.2011 · Cited by 96
Effects of matrix metalloproteinase inhibition on short‐ and long‐term plasticity of schaffer collateral/CA1 synapses
Meighan, P. C., Meighan, S. E., Davis, C. J., Wright, J. W., & Harding, J. W. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.04682.x · Cited by 95
LTP in hippocampal area CA1 is induced by burst stimulation over a broad frequency range centered around deltaPreprint
Grover, L. M., Kim, E., Cooke, J. D., & Holmes, W. R. (2009) · Learning & Memory · doi:10.1101/lm.1179109 · Cited by 93
Kinase Suppressor of Ras1 Compartmentalizes Hippocampal Signal Transduction and Subserves Synaptic Plasticity and Memory Formation
Shalin, S. C., Hernandez, C. M., Dougherty, M. K., Morrison, D. K., & Sweatt, J. D. (2006) · Neuron · doi:10.1016/j.neuron.2006.04.029 · Cited by 90
Metabotropic Glutamate Receptors Are Involved in Long-Term Potentiation in Isolated Slices of Rat Medial Frontal Cortex
Vickery, R. M., Morris, S. H., & Bindman, L. J. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.78.6.3039 · Cited by 82
GABA Transporter-1 Activity Modulates Hippocampal Theta Oscillation and Theta Burst Stimulation-Induced Long-Term Potentiation
Gong, N., Li, Y., Cai, G.-Q., Niu, R.-F., Fang, Q., Wu, K., Chen, Z., Lin, L., Xu, L., Fei, J., et al. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.4643-09.2009 · Cited by 79
Parallel augmentation of hippocampal long-term potentiation, theta rhythm, and contextual fear conditioning in water-deprived rats.
Maren, S., DeCola, J. P., Swain, R. A., Fanselow, M. S., & al, E. (1994) · Behavioral Neuroscience · doi:10.1037//0735-7044.108.1.44 · Cited by 77
Spatial overlap between populations of synapses determines the extent of their associative interaction during the induction of long-term potentiation and depression
White, G., Levy, W. B., & Steward, O. (1990) · Journal of Neurophysiology · doi:10.1152/jn.1990.64.4.1186 · Cited by 77
Modulation of AMPA receptor kinetics differentially influences synaptic plasticity in the hippocampus
Arai, A., Xia, Y., & Suzuki, É. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2003.10.033 · Cited by 76
Long lasting synaptic potentiation in the rat dentate gyrus following brief high frequency stimulation
Douglas, R. M. (1977) · Brain Research · doi:10.1016/0006-8993(77)90733-8 · Cited by 76
Spatial Distribution of Potentiated Synapses in Hippocampus: Dependence on Cellular Mechanisms and Network Properties
Yeckel, M. F., & Berger, T. W. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-01-00438.1998 · Cited by 75
Synaptic Depolarization Is More Effective than Back-Propagating Action Potentials during Induction of Associative Long-Term Potentiation in Hippocampal Pyramidal Neurons
Hardie, J. B., & Spruston, N. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.6000-08.2009 · Cited by 72
Impairment of in vivo theta‐burst long‐term potentiation and network excitability in the dentate gyrus of synaptopodin‐deficient mice lacking the spine apparatus and the cisternal organelle
Jedlička, P., Schwarzacher, S. W., Winkels, R., Kienzler, F., Frotscher, M., Bramham, C. R., Schultz, C., Orth, C. B., & Deller, T. (2008) · Hippocampus · doi:10.1002/hipo.20489 · Cited by 72
Adenosine modulates synaptic plasticity in hippocampal slices from aged rats
Costenla, A. R., de Mendonça, A., & Ribeiro, J. A. (1999) · Brain Research · doi:10.1016/s0006-8993(99)02194-0 · Cited by 72
Long-term potentiation of synaptic transmission in the adult mouse insular cortex: multielectrode array recordings
Liu, M., Kang, S. J., Shi, T., Koga, K., Zhang, M., Collingridge, G. L., Kaang, B., & Zhuo, M. (2013) · Journal of Neurophysiology · doi:10.1152/jn.01104.2012 · Cited by 71
Learning induces neurotrophin signaling at hippocampal synapses
Chen, L. Y., Rex, C. S., Sanaiha, Y., LYNCH, G. S., & Gall, C. M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0912973107 · Cited by 65
Non-Hebbian properties of long-term potentiation enable high-capacity encoding of temporal sequences.
Granger, R., Whitson, J., Larson, J., & Lynch, G. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.21.10104 · Cited by 64
Self-citation
Variation in Effective Stimulus Patterns for Induction of Long-Term Potentiation Across Different Layers of Rat Entorhinal Cortex
Yun, S. H., Mook‐Jung, I., & Jung, M. W. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-05-j0003.2002 · Cited by 63
Respiratory cycle entrainment of septal neurons mediates the fast coupling of sniffing rate and hippocampal theta rhythm
Tsanov, M., Chah, E., Reilly, R. B., & O’Mara, S. M. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12449 · Cited by 58
Differences in the magnitude of long-term potentiation produced by theta burst and high frequency stimulation protocols matched in stimulus number
Hernandez, R. V., Navarro, M. M., Rodriguez, W. A., Martinez, J. L., & LeBaron, R. G. (2005) · Brain Research Protocols · doi:10.1016/j.brainresprot.2005.02.003 · Cited by 56
Activity-induced depression of synaptic inhibition during LTP-inducing patterned stimulation.
Pacelli, G. J., Su, W., & Kelso, S. (1989) · Brain Research · doi:10.1016/0006-8993(89)91273-0 · Cited by 55
Adrenalectomy reduces the threshold for hippocampal primed burst potentiation in the anesthetized rat
Diamond, D. M., Bennett, M. C., Engstrøm, D. A., Fleshner, M., & Rose, G. (1989) · Brain Research · doi:10.1016/0006-8993(89)90919-0 · Cited by 48
Evidence that associative interactions between synapses during the induction of long-term potentiation occur within local dendritic domains.
White, G., Levy, W. B., & Steward, O. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.7.2368 · Cited by 40
SDZ ENS 163, a selective muscarinic M1 receptor agonist, facilitates the induction of long-term potentiation in rat hippocampal slices
Boddeke, E., Enz, A., & Shapiro, G. (1992) · European Journal of Pharmacology · doi:10.1016/0014-2999(92)90457-f · Cited by 38
Activity‐induced decreased in early and late inhibitory synaptic conductances in hippocampus
Pacelli, G. J., Su, W., & Kelso, S. R. (1991) · Synapse · doi:10.1002/syn.890070102 · Cited by 35
Entorhinal cortex long-term potentiation evoked by theta-patterned stimulation of associative fibers in the isolated in vitro guinea pig brain
de Curtis, M., & Llinás, R. R. (1993) · Brain Research · doi:10.1016/0006-8993(93)91391-5 · Cited by 31
Differences in the refractory properties of two distinct inhibitory circuitries in field CA1 of the hippocampus
Arai, A., Silberg, J. J., & LYNCH, G. S. (1995) · Brain Research · doi:10.1016/0006-8993(95)01137-4 · Cited by 28
Induction and transient suppression of long-term potentiation in the peri- and postrhinal cortices following theta-related stimulation of hippocampal field CA1
Cousens, G. A., & Otto, T. A. (1998) · Brain Research · doi:10.1016/s0006-8993(97)01151-7 · Cited by 28
Stimulus pattern dependence of the Alzheimer's disease amyloid-β 42 peptide's inhibition of long term potentiation in mouse hippocampal slices
Smith, J. P., Lal, V., Bowser, D. N., Cappai, R., Masters, C. L., & Ciccotosto, G. D. (2009) · Brain Research · doi:10.1016/j.brainres.2009.03.007 · Cited by 27
GABAB receptors mediate disinhibition and facilitate long-term potentiation in the dentate gyrus.
Mott, D. D., & Lewis, D. V. (1992) · PubMed · Cited by 26
The motor cortex: a network tuned to 7-14 Hz
Castro‐Alamancos, M. A. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00021 · Cited by 23
No requirement of TRPV1 in long-term potentiation or long-term depression in the anterior cingulate cortex
Liu, M., & Zhuo, M. (2014) · Molecular Brain · doi:10.1186/1756-6606-7-27 · Cited by 18
The effects of single and multiple episodes of theta patterned or high frequency stimulation on synaptic transmission from hippocampal area CA1 to the subiculum in rats
Commins, S., Anderson, M. I., Gigg, J., & O’Mara, S. M. (1999) · Neuroscience Letters · doi:10.1016/s0304-3940(99)00486-3 · Cited by 14
Pharmacological and deprivation-induced reinstatement of juvenile-like long-term potentiation in the primary auditory cortex of adult rats
Hogsden, J. L., Rosen, L. G., & Dringenberg, H. C. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.04.002 · Cited by 12
Unilateral hippocampal ablation at birth causes a reduction in contralateral LTP
van Praag, H., Chun, D. E., Black, I. B., & Staubli, U. V. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00287-x · Cited by 11

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1 of the 110 references couldn’t be matched to a known paper.

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Bliss, 1973, Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path, J. Physiol., 232, 331, 10.1113/jphysiol.1973.sp010273 · DOI · Paper page

Sorted by citations

Structure, Function, and Pharmacology of Glutamate Receptor Ion Channels
Hansen, K. B., Wollmuth, L. P., Bowie, D., Furukawa, H., Menniti, F. S., Sobolevsky, A. I., Swanson, G. T., Swanger, S. A., Greger, I. H., Nakagawa, T., et al. (2021) · Pharmacological Reviews · doi:10.1124/pharmrev.120.000131 · Cited by 686
Modulating Human Memory via Entrainment of Brain Oscillations
Hanslmayr, S., Axmacher, N., & Inman, C. S. (2019) · Trends in Neurosciences · doi:10.1016/j.tins.2019.04.004 · Cited by 264
Theta-Burst Transcranial Magnetic Stimulation for Posttraumatic Stress Disorder
Philip, N. S., Barredo, J., Aiken, E., Larson, V., Jones, R. N., Shea, M. T., Greenberg, B. D., & van ’t Wout-Frank, M. (2019) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2019.18101160 · Cited by 183
Noninvasive theta-burst stimulation of the human striatum enhances striatal activity and motor skill learning
Wessel, M. J., Beanato, E., Popa, T., Windel, F., Vassiliadis, P., Menoud, P., Beliaeva, V., Violante, I. R., Abderrahmane, H., Dzialecka, P., et al. (2023) · Nature Neuroscience · doi:10.1038/s41593-023-01457-7 · Cited by 173
The next generation of approaches to investigate the link between synaptic plasticity and learning
Humeau, Y., & Choquet, D. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0480-6 · Cited by 158

See all 285

Authors: Larson, J., & Munkácsy, E.
Affiliations: University of Illinois Chicago (US)
The University of Texas at San Antonio Health Science Center (US)
Corresponding author: Larson, John
ORCID: Munkácsy, Erin
Venue: Brain Research
Publisher: Elsevier BV
Published: 2015-09
Volume: 1621
Pages: 38-50
ISSN: 0006-8993 (ISSN-L)
DOI: 10.1016/j.brainres.2014.10.034
PMC: PMC4411212
OpenAlex: W1974528572
Cited by: 285
References: 110
Citations by year: 2026: 18 · 2025: 29 · 2024: 37 · 2023: 26 · 2022: 38 · 2021: 41 · 2020: 23 · 2019: 23 · 2018: 23 · 2017: 11 · 2016: 12 · 2015: 4
FWCI: 1.03
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (am, 158 d)
Locations: Brain Research (acceptedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: NIH (DC005793, T32 AG021890)
Department of Defense (USAMRMC 10917352)
UIC Honors College, UIC College of Liberal Arts and Sciences
Glenn Foundation for Medical Research
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Keywords: theta burst stimulation, long-term potentiation, hippocampus, CA1, feedforward inhibition, disinhibition, NMDA receptor, dendritic calcium signaling, dendritic domains, synaptic plasticity
MeSH terms: Animals, Electric Stimulation, Hippocampus, Humans, Membrane Potentials, Synapses, Long-Term Potentiation, Pyramidal Cells

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