Perforant path activation modulates the induction of long-term potentiation of the schaffer collateral—hippocampal CA1 response: theoretical and experimental analyses
Open accessAbstract
In one computational model of hippocampal function, the entorhinal cortical input to CA1 is hypothesized to play a key role in the ability of CA1 to decode CA3 recodings. Here, we develop a modification of this CA1 decoder hypothesis that is applicable to several computational theories of hippocampal function, and then we electrophysiologically investigate one assumption of this new hypothesis. First, using biologically realistic estimates, we calculate that CA3-induced CA1 excitation is too high and that inhibition plausibly plays a role in this CA1 decoder model. Thus motivated, we turn to a physiological demonstration to substantiate the plausibility of the proposed mechanism. Using the rat hippocampal slice, we examine an interlaminar interaction between the distal perforant path input to hippocampal CA1 stratum moleculare and the more proximal Schaffer collateral input to stratum radiatum. Perforant path activation provides sufficient inhibition to block homosynaptic long-term potentiation elicited by a suitably strong stratum radiatum input. For this interlaminar interaction to be most effective, perforant path activation must both precede and follow Schaffer collateral activation. Perforant path-evoked inhibition in CA1 can thus serve as a viable mechanism in the learned decoder theory of hippocampal CA1.
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
Cites
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?
The weak excitatory drive of cortical inputs to CA1 neurons likely restricts these inputs to a modulatory role in regulating CA1 output.
“The weak excitatory drive of the cortical inputs to CA1 neurons likely restricts these inputs to a modulatory role in regulating CA1 output, for example, providing instructive signals for the induction of plasticity at the more potent CA3 inputs (Dudman et al., 2007; Judge and Hasselmo, 2004; Levy et al., 1998; Remondes and Schuman, 2002).”
From Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop (2010) · cites this paper as Levy et al., 1998
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Interneurons of the hippocampus
Freund, T. F., & Buzsáki, G. (1998) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:4 · Cited by 3,423 · see citing works
Geometric determinants of the place fields of hippocampal neurons
O'Keefe, J., & Burgess, N. (1996) · Nature · doi:10.1038/381425a0 · Cited by 1,166 · see citing works
Hippocampal conjunctive encoding, storage, and recall: Avoiding a trade‐off
O'Reilly, R. C., & McClelland, J. L. (1994) · Hippocampus · doi:10.1002/hipo.450040605 · Cited by 914 · see citing works
Synaptic enhancement in fascia dentata: Cooperativity among coactive afferents
McNaughton, B. L., Douglas, R. M., & Goddard, G. V. (1978) · Brain Research · doi:10.1016/0006-8993(78)90030-6 · Cited by 647 · see citing works
Gustafsson, B., Wigstrom, H., Abraham, W., & Huang, Y. (1987) · The Journal of Neuroscience · doi:10.1523/jneurosci.07-03-00774.1987 · Cited by 583 · see citing works
Synapses as associative memory elements in the hippocampal formation
Levy, W. B., & Steward, O. (1979) · Brain Research · doi:10.1016/0006-8993(79)91003-5 · Cited by 557 · see citing works
Self-citationHebbian 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 · 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
A model of hippocampal function
Burgess, N., Recce, M., & O'Keefe, J. (1994) · Neural Networks · doi:10.1016/s0893-6080(05)80159-5 · Cited by 393 · see citing works
Place cells and silent cells in the hippocampus of freely-behaving rats
Thompson, L. T., & Best, P. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-07-02382.1989 · Cited by 337 · see citing works
Lacaille, J., & Schwartzkroin, P. (1988) · The Journal of Neuroscience · doi:10.1523/jneurosci.08-04-01411.1988 · Cited by 270 · see citing works
Fox, S. E., & Ranck, J. B. (1975) · Experimental Neurology · doi:10.1016/0014-4886(75)90213-7 · Cited by 262 · see citing works
A Computational Approach to Hippocampal Function
Levy, W. B. (1989) · The Psychology of learning and motivation/The psychology of learning and motivation · doi:10.1016/s0079-7421(08)60113-9 · Cited by 228 · see citing works
Self-citationEntorhinal projections to the hippocampal CA1 region in the rat: an underestimated pathway
Witter, M. P., Griffioen, A. W., Jorritsma-Byham, B., & Krijnen, J. L. M. (1988) · Neuroscience Letters · doi:10.1016/0304-3940(88)90350-3 · Cited by 212 · see citing works
Colbert, C. M., & Levy, W. B. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.68.1.1 · Cited by 158 · see citing works
Self-citationUltrastructure of stratum lacunosum moleculare interneurons of hippocampal CA1 region
Kunkel, D. D., Lacaille, J., & Schwartzkroin, P. A. (1988) · Synapse · doi:10.1002/syn.890020405 · Cited by 133 · see citing works
Rolls, E. T. (1989) · Addison-Wesley Longman Publishing Co., Inc. eBooks · Cited by 132 · see citing works
Dendritic morphology of CA1 pyramidal neurones from the rat hippocampus: II. Spine distributions
Bannister, N. J., & Larkman, A. U. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903600112 · Cited by 128 · see citing works
Inhibitory modulation of long-term potentiation: Evidence for a postsynaptic locus of control
Douglas, R. M., Goddard, G. V., & Riives, M. L. (1982) · Brain Research · doi:10.1016/0006-8993(82)90221-9 · Cited by 123 · see citing works
Trommald, M., Jensen, V., & Andersen, P. N. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903530208 · Cited by 106 · see citing works
Lambert, N. A., Borroni, A. M., Grover, L. M., & Teyler, T. J. (1991) · Journal of Neurophysiology · doi:10.1152/jn.1991.66.5.1538 · Cited by 88 · see citing works
Desmond, N. L., Scott, C. A., Jane, J. A., & Levy, W. B. (1994) · Hippocampus · doi:10.1002/hipo.450040509 · Cited by 63 · see citing works
Self-citationWeak excitation and simultaneous inhibition induce long-term depression in hippocampal CA1 neurons
Yang, X., Connor, J. A., & Faber, D. S. (1994) · Journal of Neurophysiology · doi:10.1152/jn.1994.71.4.1586 · Cited by 63 · see citing works
Empson, R. M., & Heinemann, U. (1995) · Hippocampus · doi:10.1002/hipo.450050203 · Cited by 52 · see citing works
Soltész, I. (1995) · Hippocampus · doi:10.1002/hipo.450050206 · Cited by 27 · see citing works
Holmes, W. R., & Levy, W. B. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.78.1.103 · Cited by 20 · see citing works
Self-citationLevy, W. B., Colbert, C. M., & Desmond, N. L. (1995) · Hippocampus · doi:10.1002/hipo.450050209 · Cited by 19 · see citing works
Self-citation21 Low synaptic convergence of CA3 collaterals on CA1 pyramidal cells suggests few release sites
Andersen, P. N., Trommald, M., & Jensen, V. (1994) · Advances in second messenger and phosphoprotein research · doi:10.1016/s1040-7952(06)80024-8 · Cited by 13 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- R. Parks and D. Levine). MIT Press, Cambridge, MA.
- Levy, W.B, C.M. Colbert, and N.L. Desmond. 1990. Elemental adaptive processes of neurons and synapses: A statistical/computational perspective. In Neuroscience and connectionist theory (ed. M.A. Gluck and D.E. Rumelhart), pp. 187-235.
Cited by
Sorted by citations
Strong CA2 Pyramidal Neuron Synapses Define a Powerful Disynaptic Cortico-Hippocampal Loop
Chevaleyre, V., & Siegelbaum, S. A. (2010) · Neuron · doi:10.1016/j.neuron.2010.04.013 · Cited by 324 · see citing works
The Corticohippocampal Circuit, Synaptic Plasticity, and MemoryPreprint
Basu, J., & Siegelbaum, S. A. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a021733 · Cited by 244 · see citing works
Dudman, J. T., Tsay, D., & Siegelbaum, S. A. (2007) · Neuron · doi:10.1016/j.neuron.2007.10.020 · Cited by 192 · see citing works
Direct cortical input modulates plasticity and spiking in CA1 pyramidal neurons
Remondes, M., & Schuman, E. M. (2002) · Nature · doi:10.1038/416736a · Cited by 189 · see citing works
Theta Phase Modulates Multiple Layer-Specific Oscillations in the CA1 Region
Scheffer-Teixeira, R., Belchior, H., Caixeta, F. V., Souza, B. C., Ribeiro, S. T. G., & Tort, A. B. L. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr319 · Cited by 138 · see citing works
Basu, J., Srinivas, K. V., Cheung, S. K., Taniguchi, H., Huang, Z. J., & Siegelbaum, S. A. (2013) · Neuron · doi:10.1016/j.neuron.2013.07.001 · Cited by 122 · see citing works
Kajiwara, R., Wouterlood, F. G., Sah, A., Boekel, A. J., Baks‐te‐Bulte, L., & Witter, M. P. (2007) · Hippocampus · doi:10.1002/hipo.20385 · Cited by 107 · see citing works
Revisiting the role of the hippocampal mossy fiber synapse
Urban, N. N., Henze, D. A., & Barrionuevo, G. (2001) · Hippocampus · doi:10.1002/hipo.1055 · Cited by 94 · see citing works
Rapid erasure of hippocampal memory following inhibition of dentate gyrus granule cells
Madroñal, N., Delgado-Garcia, J. M., Fernández-Guizán, A., Chatterjee, J., Köhn, M., Mattucci, C., Jain, A., Tsetsenis, T., Illarionova, A., Grinevich, V., et al. (2016) · Nature Communications · doi:10.1038/ncomms10923 · Cited by 88 · see citing works
Functional division of hippocampal area CA1 via modulatory gating of entorhinal cortical inputs
Ito, H., & Schuman, E. M. (2011) · Hippocampus · doi:10.1002/hipo.20909 · Cited by 79 · see citing works
Frequency-dependent gating of synaptic transmission and plasticity by dopamine
Ito, H. (2007) · Frontiers in Neural Circuits · doi:10.3389/neuro.04.001.2007 · Cited by 77 · see citing works
Patterned Activity in Stratum Lacunosum Moleculare Inhibits CA1 Pyramidal Neuron Firing
Dvorak-Carbone, H., & Schuman, E. M. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.82.6.3213 · Cited by 71 · see citing works
Piskorowski, R. A., & Chevaleyre, V. (2011) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0769-4 · Cited by 65 · see citing works
Speed, H. E., & Dobrunz, L. E. (2008) · Hippocampus · doi:10.1002/hipo.20496 · Cited by 56 · see citing works
Long-Term Depression of Temporoammonic-CA1 Hippocampal Synaptic Transmission
Dvorak-Carbone, H., & Schuman, E. M. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.81.3.1036 · Cited by 52 · see citing works
de Asis, E. D., Nguyen-Vu, T. B., Arumugam, P. U., Chen, H., Cassell, A. M., Andrews, R. J., Yang, C. Y., & Li, J. (2009) · Biomedical Microdevices · doi:10.1007/s10544-009-9295-7 · Cited by 50 · see citing works
Opioid-Mediated Facilitation of Long-Term Depression in Rat Hippocampus
Wagner, J. J., Etemad, L. R., & Thompson, A. M. (2001) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)38816-0 · Cited by 50 · see citing works
Luo, X., McGregor, G., Irving, A. J., & Harvey, J. (2015) · eNeuro · doi:10.1523/eneuro.0007-15.2015 · Cited by 47 · see citing works
Aksoy‐Aksel, A., & Manahan‐Vaughan, D. (2013) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2013.00005 · Cited by 48 · see citing works
Tsukamoto, M., Yasui, T., Yamada, M. K., Nishiyama, N., Matsuki, N., & Ikegaya, Y. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2002.033803 · Cited by 44 · see citing works
McGregor, G., Irving, A. J., & Harvey, J. (2017) · The FASEB Journal · doi:10.1096/fj.201601293rr · Cited by 40 · see citing works
Frequency-dependent signal transmission and modulation by neuromodulators
Ito, H. (2008) · Frontiers in Neuroscience · doi:10.3389/neuro.01.027.2008 · Cited by 38 · see citing works
Hippocampal Phase Precession from Dual Input Components
Chance, F. S. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.2786-12.2012 · Cited by 40 · see citing works
Direct Cortical Inputs Erase Long-Term Potentiation at Schaffer Collateral Synapses
Izumi, Y., & Zorumski, C. F. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.3346-08.2008 · Cited by 37 · see citing works
Wöhrl, R., von Haebler, D., & Heinemann, U. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05274.x · Cited by 36 · see citing works
Judge, S. J., & Hasselmo, M. E. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00848.2003 · Cited by 36 · see citing works
Wöhrl, R., Eisenach, S., Manahan‐Vaughan, D., Heinemann, U., & von Haebler, D. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05899.x · Cited by 33 · see citing works
Mercier, M. S., Magloire, V., Cornford, J. H., & Kullmann, D. M. (2022) · The Journal of Physiology · doi:10.1113/jp282753 · Cited by 22 · see citing works
Jha, A., & Panchal, S. S. (2017) · Journal of Applied Biomedicine · doi:10.1016/j.jab.2017.05.001 · Cited by 22 · see citing works
Long-term Potentiation at Temporoammonic Path-CA1 Synapses in Freely Moving Rats
Gonzalez, J., Villarreal, D. M., Morales, I. S., & Derrick, B. E. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2016.00002 · Cited by 20 · see citing works
Background potassium concentrations and epileptiform discharges
Möddel, G., Gorji, A., & Speckmann, E. ‐. (2002) · Brain Research · doi:10.1016/s0006-8993(02)03741-1 · Cited by 17 · see citing works
Characteristics of the functioning of the hippocampal formation in waking and paradoxical sleep
Silkis, I. G. (2009) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-009-9163-1 · Cited by 16 · see citing works
Świetlik, D. (2018) · Complexity · doi:10.1155/2018/1297150 · Cited by 15 · see citing works
Izumi, Y., & Zorumski, C. F. (2016) · PLoS ONE · doi:10.1371/journal.pone.0149034 · Cited by 13 · see citing works
Synaptic Plasticity: A Unifying Model to Address Some Persisting Questions
Michmizos, D., Koutsouraki, E., Asprodini, E. K., & Balogiannis, S. (2011) · International Journal of Neuroscience · doi:10.3109/00207454.2011.556283 · Cited by 11 · see citing works
Silkis, I. G. (2003) · Neuroscience and Behavioral Physiology · doi:10.1023/a:1023960402109 · Cited by 8 · see citing works
Longden, K. D., & Willshaw, D. J. (2007) · Network Computation in Neural Systems · doi:10.1080/09548980701587100 · Cited by 3 · see citing works
Constraining the function of CA1 in associative memory models of the hippocampus
Longden, K. D. (2005) · ERA · Cited by 2 · see citing works
Silkis, I. G. (2016) · Neurochemical Journal · doi:10.1134/s181971241601013x · Cited by 2 · see citing works
Leptin Induces a Novel Form of NMDA Receptor- Dependent LTP at Hippocampal Temporoammonic-
Luo, X. M., McGregor, G., Irving, A. J., & Harvey, J. (2015)
- Authors
- Levy, W. B., Desmond, N. L., & Zhang, D. X.
- Affiliations
- University of Virginia (US)
- ORCID
- Levy, W B
- Venue
- Learning & Memory
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 1998
- Volume
- 4
- Issue
- 6
- Pages
- 510-518
- ISSN
- 1072-0502 (ISSN-L)
- 1549-5485
- OpenAlex
- W2018646762
- Cited by
- 43
- References
- 29
- Citations by year
- 2023: 1 · 2022: 1 · 2018: 1 · 2017: 2 · 2016: 4 · 2015: 3 · 2013: 2 · 2012: 2
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Learning & Memory (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01mh050670-03, 5r01ns015488-19, 5k02mh000622-09)
- National Institute of Mental Health (R01 MH50670, KO2 MH00622)
- National Institute of Neurological Disorders and Stroke (R01 NS15488)
- 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 › Neural dynamics and brain function
- Keywords
- perforant path, Schaffer collaterals, hippocampal CA1, long-term potentiation, stratum moleculare, stratum radiatum, entorhinal cortex, rat hippocampal slices
- MeSH terms
- Animals, Conditioning, Psychological, Electric Stimulation, Electrophysiology, Hippocampus, Male, Models, Neurological, Rats, Sprague-Dawley, Long-Term Potentiation, Perforant Pathway, Excitatory Postsynaptic Potentials, 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