Cited by 144Neuroscience and Neuropharmacology ResearchMemory and Neural MechanismsNeural dynamics and brain function

The DOI matches its Crossref record; 86 of the 86 references it cites were found in a registry or an index.

Theta-Frequency Synaptic Potentiation in CA1 In Vitro Distinguishes Cognitively Impaired from Unimpaired Aged Fischer 344 Rats

Open access

Tombaugh, Geoffrey C., Rowe, Wayne B., Chow, Ana R., Michael, Timothy H., Rose, Gregory M.·2002·The Journal of Neuroscience

DOI 10.1523/jneurosci.22-22-09932.2002PMC PMC6757825

Open this paper in CoChat — free account Open PDF

Abstract

Hippocampal-dependent learning and memory deficits have been well documented in aging rodents. The results of several recent studies have suggested that these deficits arise from weakened synaptic plasticity within the hippocampus. In the present study, we examined the relationship between hippocampal long-term potentiation (LTP) in vitro and spatial learning in aged (24-26 months) Fischer 344 rats. We found that LTP induced in the CA1 region using theta-frequency stimulation (5 Hz) is selectively impaired in slices from a subpopulation of aged rats that had shown poor spatial learning in the Morris water maze. LTP at 5 Hz in aged rats that did not show learning deficits was similar to that seen in young (4-6 months) controls. We also found that 5 Hz LTP amplitude strongly correlated with individual learning performance among aged rats. The difference in 5 Hz LTP magnitude among aged rats was not attributable to an altered response to 5 Hz stimulation or to differences in the NMDA receptor-mediated field EPSP. In addition, no performance-related differences in LTP were seen when LTP was induced with 30 or 70 Hz stimulation protocols. Finally, both 5 Hz LTP and spatial learning in learning-impaired rats were enhanced with the selective muscarinic M2 antagonist BIBN-99 (5,11-dihydro-8-chloro-11-[[4-[3-[(2,2-dimethyl-1-oxopentyl)ethylamino]propyl]-1-piperidinyl]acetyl]-6H-pyrido[2,3-b][1,4]benzodiazepin-6-one). These findings reinforce the idea that distinct types of hippocampal LTP offer mechanistic insight into age-associated cognitive decline.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1523/jneurosci.22-22-09932.2002

Cites

86 of 86 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

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
Place navigation impaired in rats with hippocampal lesions
Morris, R. G. M., Garrud, P., Rawlins, J. N. P., & O'Keefe, J. (1982) · Nature · doi:10.1038/297681a0 · Cited by 6,340
Synaptic Plasticity and Memory: An Evaluation of the Hypothesis
Martin, S. J., Grimwood, P. D., & Morris, R. G. M. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.649 · Cited by 2,794
Muscarinic suppression of a novel voltage-sensitive K+ current in a vertebrate neurone
Brown, D. A., & Adams, P. R. (1980) · Nature · doi:10.1038/283673a0 · Cited by 1,447
GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus
Freund, T. F., & Antal, M. (1988) · Nature · doi:10.1038/336170a0 · Cited by 1,283
Subregion- and Cell Type–Restricted Gene Knockout in Mouse Brain
Tsien, J. Z., Chen, D. F., Gerber, D., Tom, C., Mercer, E. H., Anderson, D. J., Mayford, M., Kandel, E. R., & Tonegawa, S. (1996) · Cell · doi:10.1016/s0092-8674(00)81826-7 · Cited by 1,280
Spatial learning with a minislab in the dorsal hippocampus.
Moser, M., Moser, E. I., Forrest, E., Andersen, P. N., & Morris, R. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.21.9697 · Cited by 944
Identification and localization of muscarinic acetylcholine receptor proteins in brain with subtype-specific antibodies
Levey, A. I., Kitt, C. A., Wf, S., Price, D., & Brann, M. R. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-10-03218.1991 · Cited by 920
ELECTROPHYSIOLOGY OF HIPPOCAMPAL NEURONS: II. AFTER-POTENTIALS AND REPETITIVE FIRING
Kandel, E. R., & Spencer, W. A. (1961) · Journal of Neurophysiology · doi:10.1152/jn.1961.24.3.243 · Cited by 687
Ibotenate Lesions of Hippocampus and/or Subiculum: Dissociating Components of Allocentric Spatial Learning
Morris, R., Schenk, F., Tweedie, F., & Jarrard, L. E. (1990) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1990.tb00014.x · Cited by 666
Preserved neuron number in the hippocampus of aged rats with spatial learning deficits.
Rapp, P. R., & Gallagher, M. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.18.9926 · Cited by 658
Age-related defects in spatial memory are correlated with defects in the late phase of hippocampal long-term potentiation in vitro and are attenuated by drugs that enhance the cAMP signaling pathway
Bach, M. E., Barad, M., Son, H., Zhuo, M., Lü, Y.-F., Shih, R., Mansuy, I. M., Hawkins, R. D., & Kandel, E. R. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.9.5280 · Cited by 571
Selective activation of Ca2+-activated K+ channels by co-localized Ca2+ channels in hippocampal neurons
Marrion, N. V., & Tavalin, S. J. (1998) · Nature · doi:10.1038/27674 · Cited by 546
Interneurons containing calretinin are specialized to control other interneurons in the rat hippocampus
Gulyás, A. I., Hájos, N., & Freund, T. F. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-10-03397.1996 · Cited by 512
Spatial learning and motor deficits in aged rats
Gage, F. H., Dunnett, S. B., & Björklund, A. (1984) · Neurobiology of Aging · doi:10.1016/0197-4580(84)90084-8 · Cited by 507
Prolonged Ca 2+ -Dependent Afterhyperpolarizations in Hippocampal Neurons of Aged Rats
Landfield, P. W., & Pitler, T. A. (1984) · Science · doi:10.1126/science.6494926 · Cited by 495
Gating of CaMKII by cAMP-Regulated Protein Phosphatase Activity During LTP
Blitzer, R. D., Connor, J. H., Brown, G. P., Wong, T., Shenolikar, S., Iyengar, R., & Landau, E. M. (1998) · Science · doi:10.1126/science.280.5371.1940 · Cited by 445
Circuit-Specific Alterations in Hippocampal Synaptophysin Immunoreactivity Predict Spatial Learning Impairment in Aged Rats
Smith, T. D., Adams, M. M., Gallagher, M., Morrison, J. H., & Rapp, P. R. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-17-06587.2000 · Cited by 397
Disinhibition of rat hippocampal pyramidal cells by GABAergic afferents from the septum.
Tóth, K., Freund, T. F., & Miles, R. (1997) · The Journal of Physiology · doi:10.1113/jphysiol.1997.sp022033 · Cited by 395
Natural patterns of activity and long-term synaptic plasticity
Paulsen, O. (2000) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00076-3 · Cited by 354
An age comparison of the rates of acquisition and forgetting of spatial information in relation to long-term enhancement of hippocampal synapses.
Barnes, C. A., & McNaughton, B. L. (1985) · Behavioral Neuroscience · doi:10.1037//0735-7044.99.6.1040 · Cited by 337
Normal aging: regionally specific changes in hippocampal synaptic transmission
Barnes, C. A. (1994) · Trends in Neurosciences · doi:10.1016/0166-2236(94)90029-9 · Cited by 334
Postsynaptic CAMP pathway gates early LTP in hippocampal CA1 region
Blitzer, R. D., Wong, T., Nouranifar, R., Iyengar, R., & Landau, E. M. (1995) · Neuron · doi:10.1016/0896-6273(95)90018-7 · Cited by 326
ERK Plays a Regulatory Role in Induction of LTP by Theta Frequency Stimulation and Its Modulation by β-Adrenergic Receptors
Winder, D. G., Martin, K. C., Muzzio, I. A., Rohrer, D. K., Chruscinski, A. J., Kobilka, B. K., & Kandel, E. R. (1999) · Neuron · doi:10.1016/s0896-6273(00)81124-1 · Cited by 326
Involvement of hippocampal synaptic plasticity in age-related memory decline
Foster, T. C. (1999) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00017-x · Cited by 322
Long-term potentiation: What's learning got to do with it?
Shors, T. J., & Matzel, L. D. (1997) · Behavioral and Brain Sciences · doi:10.1017/s0140525x97001593 · Cited by 320
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
Electrophysiology of Hippocampal Neurons
Schwartzkroin, P. A., & Mueller, A. L. (1987) · Cerebral cortex · doi:10.1007/978-1-4615-6616-8_8 · Cited by 299
Increased Susceptibility to Induction of Long-Term Depression and Long-Term Potentiation Reversal during Aging
Norris, C. M., Korol, D. L., & Foster, T. C. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-17-05382.1996 · Cited by 295
Activity-Dependent β-Adrenergic Modulation of Low Frequency Stimulation Induced LTP in the Hippocampal CA1 Region
Thomas, M. J., Moody, T. D., Makhinson, M., & O’Dell, T. J. (1996) · Neuron · doi:10.1016/s0896-6273(00)80179-8 · Cited by 287
Nimodipine increases excitability of rabbit CA1 pyramidal neurons in an age- and concentration-dependent manner
Moyer, J. R., Thompson, L. T., Black, J., & Disterhoft, J. F. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.68.6.2100 · Cited by 287
Reversal of Age-Related Alterations in Synaptic Plasticity by Blockade of L-Type Ca2+Channels
Norris, C. M., Halpain, S., & Foster, T. C. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-09-03171.1998 · Cited by 271
A Hippocampal NR2B Deficit Can Mimic Age-Related Changes in Long-Term Potentiation and Spatial Learning in the Fischer 344 Rat
Clayton, D. A., Mesches, M. H., Álvarez, E., Bickford, P. C., & Browning, M. D. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-09-03628.2002 · Cited by 261
Apical Dendritic Location of Slow Afterhyperpolarization Current in Hippocampal Pyramidal Neurons: Implications for the Integration of Long-Term Potentiation
Sah, P., & Bekkers, J. M. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-15-04537.1996 · Cited by 255
IPSPs modulate spike backpropagation and associated [Ca2+]i changes in the dendrites of hippocampal CA1 pyramidal neurons
Tsubokawa, H., & Ross, W. N. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.76.5.2896 · Cited by 246
Ionic basis of spike after‐depolarization and burst generation in adult rat hippocampal CA1 pyramidal cells.
Azouz, R., Jensen, M. S., & Yaari, Y. (1996) · The Journal of Physiology · doi:10.1113/jphysiol.1996.sp021302 · Cited by 243
Strain-dependent Differences in LTP and Hippocampus-dependent Memory in Inbred MicePreprint
Nguyen, P., Abel, T. G., Kandel, E. R., & Bourtchouladze, R. (2000) · Learning & Memory · doi:10.1101/lm.7.3.170 · Cited by 242
Aging Differentially Alters Forms of Long-Term Potentiation in Rat Hippocampal Area CA1
Shankar, S., Teyler, T. J., & Robbins, N. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.1.334 · Cited by 227
Postsynaptic bursting is essential for ‘Hebbian’ induction of associative long‐term potentiation at excitatory synapses in rat hippocampus
Pike, F. G., Meredith, R. M., Olding, A. W. A., & Paulsen, O. (1999) · The Journal of Physiology · doi:10.1111/j.1469-7793.1999.0571p.x · Cited by 227
Age-related alterations in potentiation in the CA1 region in F344 rats
Deupree, D. L., Bradley, J., & Turner, D. A. (1993) · Neurobiology of Aging · doi:10.1016/0197-4580(93)90009-z · Cited by 219
Distinct interneuron types express m2 muscarinic receptor immunoreactivity on their dendrites or axon terminals in the hippocampus
Hájos, N., Papp, E., Acsády, L., Levey, A. I., & Freund, T. F. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00300-x · Cited by 211
Facilitation of acetylcholine release and cognitive performance by an M(2)-muscarinic receptor antagonist in aged memory-impaired
Quirion, R., Wilson, A. L., Rowe, W. B., Aubert, I., Richard, J., Doods, H. N., Parent, A., White, N. M., & Meaney, M. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-02-01455.1995 · Cited by 205
Self-citation
Aging Changes in Voltage-Gated Calcium Currents in Hippocampal CA1 Neurons
Campbell, L. W., Hao, S., Thibault, O., Blalock, E. M., & Landfield, P. W. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-19-06286.1996 · Cited by 200
Caloric restriction prevents age-related deficits in LTP and in NMDA receptor expression
Eckles-Smith, K., Clayton, D. A., Bickford, P. C., & Browning, M. D. (2000) · Molecular Brain Research · doi:10.1016/s0169-328x(00)00088-7 · Cited by 195
Calcium-dependent afterhyperpolarization and learning in young and aging hippocampus
Disterhoft, J. F., Thompson, L. T., Moyer, J. R., & Mogul, D. J. (1996) · Life Sciences · doi:10.1016/0024-3205(96)00320-7 · Cited by 190
Postsynaptic Complex Spike Bursting Enables the Induction of LTP by Theta Frequency Synaptic Stimulation
Thomas, M. J., Watabe, A. M., Moody, T. D., Makhinson, M., & O’Dell, T. J. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-18-07118.1998 · Cited by 189
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
Self-citation
Relationship Between Venous Pressure and tissue Volume During Venous Congestion Plethysmography in Man
Christ, F., Gamble, J., Baschnegger, H., & GARTSIDE, I. B. (1997) · The Journal of Physiology · doi:10.1111/j.1469-7793.1997.463bh.x · Cited by 182
Muscarinic receptors mediating depression and long‐term potentiation in rat hippocampus.
Auerbach, J. M., & Segal, M. (1996) · The Journal of Physiology · doi:10.1113/jphysiol.1996.sp021323 · Cited by 168
Muscarinic Modulation of Spike Backpropagation in the Apical Dendrites of Hippocampal CA1 Pyramidal Neurons
Tsubokawa, H., & Ross, W. N. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-15-05782.1997 · Cited by 157
Region‐specific age effects on AMPA sensitivity: Electrophysiological evidence for loss of synaptic contacts in hippocampal field CA1
Barnes, C. A., RAO, G. R., Foster, T. C., & McNaughton, B. L. (1992) · Hippocampus · doi:10.1002/hipo.450020413 · Cited by 157
The effects of high Mg2+-to-Ca2+ ratios on frequency potentiation in hippocampal slices of young and aged rats
Landfield, P. W., Pitler, T. A., & Applegate, M. D. (1986) · Journal of Neurophysiology · doi:10.1152/jn.1986.56.3.797 · Cited by 157
Cognitive functioning in very old age
Bäckman, L., Small, B. J., Wåhlin, Å., & Larsson, M. U. (1999) · Cited by 146
Age-Related Decrease in the N-Methyl-d-AspartateR-Mediated Excitatory Postsynaptic Potential in Hippocampal Region CA1
Barnes, C. A., RAO, G. R., & Shen, J. (1997) · Neurobiology of Aging · doi:10.1016/s0197-4580(97)00044-4 · Cited by 144
Effects of the NMDA antagonist 2AP5 on complex spike discharge by hippocampal pyramidal cells
Abraham, W. C., & Kairiss, E. W. (1988) · Neuroscience Letters · doi:10.1016/0304-3940(88)90477-6 · Cited by 144
Systemic Administration of a Nerve Growth Factor Conjugate Reverses Age-Related Cognitive Dysfunction and Prevents Cholinergic Neuron Atrophy
Bäckman, C. M., Rose, G. M., Hoffer, B. J., Henry, M. A., Bartus, R. T., Friden, P. M., & Granholm, A. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-17-05437.1996 · Cited by 140
Self-citation
Spatial performance correlates with in vitro potentiation in young and aged Fischer 344 rats
Deupree, D. L., Turner, D. A., & Watters, C. L. (1991) · Brain Research · doi:10.1016/0006-8993(91)90164-q · Cited by 131
Reference and working memory of rats following hippocampal damage induced by transient forebrain ischemia
Davis, H. P., Tribuna, J., Pulsinelli, W. A., & Volpe, B. T. (1986) · Physiology & Behavior · doi:10.1016/0031-9384(86)90195-2 · Cited by 121
Alterations in the balance of protein kinase/phosphatase activities parallel reduced synaptic strength during aging.
Norris, C., Halpain, S., & Foster, T. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.3.1567 · Cited by 110
Hippocampal dependent learning ability correlates with N‐methyl‐D‐aspartate (NMDA) receptor levels in CA3 neurons of young and aged rats
Adams, M. M., Smith, T. D., Moga, D. E., Gallagher, M., Wang, Y., Wolfe, B. B., Rapp, P. R., & Morrison, J. H. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1099 · Cited by 110
Selective muscarinic antagonists differentially affect in vivo acetylcholine release and memory performances of young and aged rats
Vannucchi, M. G., Scali, C., Kopf, S. R., Pepeu, G., & Casamenti, F. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00091-2 · Cited by 108
Somatic Colocalization of Rat SK1 and D class (Cav 1.2) L-type Calcium Channels in Rat CA1 Hippocampal Pyramidal Neurons
Bowden, S. E. H., Fletcher, S., Loane, D. J., & Marrion, N. V. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-20-j0006.2001 · Cited by 103
Deficits in the expression of the NR2B subunit in the hippocampus of aged Fisher 344 rats
Clayton, D. (2001) · Neurobiology of Aging · doi:10.1016/s0197-4580(00)00196-2 · Cited by 99
Reactivity to novelty in cognitively-impaired and cognitively-unimpaired aged rats and young rats
Rowe, W. B., Spreekmeester, E., Meaney, M. J., Quirion, R., & Rochford, J. M. (1998) · Neuroscience · doi:10.1016/s0306-4522(97)00464-8 · Cited by 98
Self-citation
Functional integrity of NMDA-dependent LTP induction mechanisms across the lifespan of F-344 rats.Preprint
Barnes, C. A., Rao, G., & McNaughton, B. L. (1996) · Learning & Memory · doi:10.1101/lm.3.2-3.124 · Cited by 97
Impaired Recognition of the Goal Location during Spatial Navigation in Rats with Hippocampal Lesions
Hollup, S., Kjelstrup, K. B., Hoff, J., Moser, M., & Moser, E. I. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-12-04505.2001 · Cited by 91
Localization of M2 muscarinic acetylcholine receptor protein in cholinergic and non-cholinergic terminals in rat hippocampus
Rouse, S. T., Edmunds, S. M., Yi, H. L., Gilmor, M. L., & Levey, A. I. (2000) · Neuroscience Letters · doi:10.1016/s0304-3940(00)01011-9 · Cited by 85
In vitro autoradiography of hippocampal excitatory amino acid binding in aged Fischer 344 rats: Relationship to performance on the Morris water maze.
Clark, A. S., Magnusson, K. R., & Cotman, C. W. (1992) · Behavioral Neuroscience · doi:10.1037//0735-7044.106.2.324 · Cited by 79
Acetyl-l-carnitine: Behavioral, electrophysiological, and neurochemical effects
Davis, S., Markowska, A. L., Wenk, G. L., & Barnes, C. A. (1993) · Neurobiology of Aging · doi:10.1016/0197-4580(93)90030-f · Cited by 71
Therapeutic potential of CNS-active M2 antagonists: Novel structures and pharmacology
Doods, H. N., Quirion, R., Mihm, G., Engel, W., Rudolf, K. D., Entzeroth, M., Schiavi, G. B., Ladinsky, H., Bechtel, W. D., Ensinger, H. A., et al. (1993) · Life Sciences · doi:10.1016/0024-3205(93)90307-o · Cited by 67
Aging‐Related Increases in Voltage‐Sensitive, Inactivating Calcium Currents in Rat Hippocampus Implications for Mechanisms of Brain Aging and Alzheimer's Disease
Landfield, P. W., CAMPBELL, L. W., Hao, S., & KERR, D. S. (1989) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1989.tb12495.x · Cited by 56
Biomarkers of age and aging
McClearn, G. E. (1997) · Experimental Gerontology · doi:10.1016/s0531-5565(96)00067-8 · Cited by 53
Activation of the pharmacologically defined M3 muscarinic receptor depolarizes hippocampal pyramidal cells
Pitler, T. A., & Alger, B. E. (1990) · Brain Research · doi:10.1016/0006-8993(90)90137-z · Cited by 53
Influence of diet restriction on NMDA receptor subunits and learning during aging
Magnusson, K. R. (2001) · Neurobiology of Aging · doi:10.1016/s0197-4580(00)00258-x · Cited by 52
Functional Specificity of Gαqand Gα11in the Cholinergic and Glutamatergic Modulation of Potassium Currents and Excitability in Hippocampal Neurons
Krause, M., Offermanns, S., Stocker, M., & Pedarzani, P. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-03-00666.2002 · Cited by 50
Post-injury administration of BIBN 99, a selective muscarinic M2 receptor antagonist, improves cognitive performance following traumatic brain injury in rats
Pike, G. B., & Hamm, R. J. (1995) · Brain Research · doi:10.1016/0006-8993(95)00448-y · Cited by 46
Burst characteristics of hippocampal complex spike cells in the awake rat
Suzuki, S. S., & Smith, G. K. (1985) · Experimental Neurology · doi:10.1016/0014-4886(85)90267-5 · Cited by 43
Antisense oligodeoxynucleotides against the muscarinic m2, but not m4, receptor supports its role as autoreceptors in the rat hippocampus
Kitaichi, K., Hori, T., Srivastava, L. K., & Quirion, R. (1999) · Molecular Brain Research · doi:10.1016/s0169-328x(99)00047-9 · Cited by 43
Characterization of BIBN 99: A lipophilic and selective muscarinic M2 receptor antagonist
Doods, H. N., Entzeroth, M., Ziegler, H., Schiavi, G. B., Engel, W. W., Mihm, G., Rudolf, K. D., & Eberlein, W. G. (1993) · European Journal of Pharmacology · doi:10.1016/0014-2999(93)90005-3 · Cited by 41
A protein phosphatase is involved in the cholinergic suppression of the Ca2+-activated K+ current sIAHP in hippocampal pyramidal neurons
Krause, M., & Pedarzani, P. (2000) · Neuropharmacology · doi:10.1016/s0028-3908(99)00227-0 · Cited by 33
Short-term reverberant memory model of hippocampal field CA3
Wiebe, S. P., St�ubli, U. V., & Ambros-Ingerson, J. (1997) · Hippocampus · doi:10.1002/(sici)1098-1063(1997)7:6 · Cited by 33
NMDA Receptor Activation in the Aged Rat: Electrophysiological Investigations in the CA1 Area of the Hippocampal Slice Ex Vivo
Billard, J., Jouvenceau, A., Lamour, Y. A., & Dutar, P. (1997) · Neurobiology of Aging · doi:10.1016/s0197-4580(97)00104-8 · Cited by 26
Effects of nucleus basalis lesion on muscarinic receptor subtypes
Bogdanović, N., Islam, A., Nilsson, L. N. G., Bergstr�m, L., Winblad, B. G., & Adem, A. (1993) · Experimental Brain Research · doi:10.1007/bf00228691 · Cited by 16
Kinetics of Muscarinic Reduction ofIsAHPin Hippocampal Neurons: Effects of Acetylcholinesterase Inhibitors
Zhang, Y., Carlen, P. L., & Zhang, L. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.78.6.2999 · Cited by 9
Untitled work
Mattson, M. (1999) · doi:10.1002/(sici)1097-4547(19991001)58:1
Untitled work
Bumsted (1999) · doi:10.1002/(sici)1096-9861(19990125)403:4

Sorted by citations

Neural plasticity in the ageing brain
Burke, S. N., & Barnes, C. A. (2005) · Nature reviews. Neuroscience · doi:10.1038/nrn1809 · Cited by 1,709
Neuroinflammatory TNFα Impairs Memory via Astrocyte Signaling
Habbas, S., Santello, M., Becker, D., Stubbe, H., Zappia, G., Liaudet, N., Klaus, F. R., Kollias, G., Fontana, A., Pryce, C. R., et al. (2015) · Cell · doi:10.1016/j.cell.2015.11.023 · Cited by 347
Immune dysregulation and cognitive vulnerability in the aging brain: Interactions of microglia, IL-1β, BDNF and synaptic plasticity
Patterson, S. L. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.12.020 · Cited by 291
Age matters
McCutcheon, J. E., & Marinelli, M. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06648.x · Cited by 299
Brain-Derived Neurotrophic Factor Rescues Synaptic Plasticity in a Mouse Model of Fragile X Syndrome
Lauterborn, J. C., Rex, C. S., Kramár, E. A., Chen, L. Y., Pandyarajan, V., LYNCH, G. S., & Gall, C. M. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2624-07.2007 · Cited by 244

See all 144

Authors: Tombaugh, G. C., Rowe, W. B., Chow, A. R., Michael, T. H., & Rose, G. M.
ORCID: Rose, Gregory M.
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2002-11-15
Volume: 22
Issue: 22
Pages: 9932-9940
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.22-22-09932.2002
PMC: PMC6757825
OpenAlex: W1597519089
Cited by: 144
References: 86
Citations by year: 2026: 1 · 2025: 2 · 2024: 5 · 2023: 4 · 2022: 4 · 2021: 7 · 2020: 4 · 2019: 4 · 2018: 6 · 2017: 7 · 2016: 5 · 2015: 7 · 2014: 5 · 2013: 13 · 2012: 9
FWCI: 2.10
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Journal of Neuroscience (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
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: long-term potentiation, hippocampal CA1, aging, age-related cognitive decline, spatial learning, Morris water maze, M2 muscarinic receptor, NMDA receptor, synaptic plasticity, hippocampal slices
MeSH terms: Age Factors, Animals, Behavior, Animal, Cognition Disorders, Dibenzazepines, Electric Stimulation, Hippocampus, Male, Synaptic Transmission, Pyridines, Rats, Inbred F344, Reaction Time, Receptors, Muscarinic, Theta Rhythm, Receptors, N-Methyl-D-Aspartate, Long-Term Potentiation, Muscarinic Antagonists, Maze Learning, Excitatory Postsynaptic Potentials, Receptor, Muscarinic M2, Rats, 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.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Theta-Frequency Synaptic Potentiation in CA1 In Vitro Distinguishes Cognitively Impaired from Unimpaired Aged Fischer 344 Rats

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks