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Cited by 151Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchNeural dynamics and brain function

Bidirectional synaptic plasticity rapidly modifies hippocampal representations

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Milstein, Aaron D, Li, Yiding, Bittner, Katie C, Grienberger, Christine, Soltesz, Ivan, Magee, Jeffrey C, Romani, Sandro·2021·eLife
DOI 10.7554/elife.73046PMC PMC8776257

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Abstract

Learning requires neural adaptations thought to be mediated by activity-dependent synaptic plasticity. A relatively non-standard form of synaptic plasticity driven by dendritic calcium spikes, or plateau potentials, has been reported to underlie place field formation in rodent hippocampal CA1 neurons. Here, we found that this behavioral timescale synaptic plasticity (BTSP) can also reshape existing place fields via bidirectional synaptic weight changes that depend on the temporal proximity of plateau potentials to pre-existing place fields. When evoked near an existing place field, plateau potentials induced less synaptic potentiation and more depression, suggesting BTSP might depend inversely on postsynaptic activation. However, manipulations of place cell membrane potential and computational modeling indicated that this anti-correlation actually results from a dependence on current synaptic weight such that weak inputs potentiate and strong inputs depress. A network model implementing this bidirectional synaptic learning rule suggested that BTSP enables population activity, rather than pairwise neuronal correlations, to drive neural adaptations to experience.

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  • BTSP is NMDAR dependent and, unlike classical LTP, has a coincidence time window of seconds rather than milliseconds.

    “It is NMDAR dependent, but unlike classical LTP the coincidence time window is seconds, not milliseconds.”

    From Synaptic memory and CaMKII (2023) · cites this paper as [103]

    The Introduction describes BTSP as acting within a seconds-long window, and the Results section on initial membrane voltage says BTSP induction requires NMDA-type glutamate receptors, citing prior work and reporting an experiment consistent with that requirement. The Discussion contrasts BTSP with the short-timescale synchrony of traditional Hebbian plasticity, but our copy does not specify a millisecond coincidence window for classical LTP. (LLM, conf=0.83)

    Experimental — accuracy not yet measured

  • Behavioral timescale synaptic plasticity (BTSP) is responsible for the rapid formation of hippocampal place fields.

    “behavioral timescale synaptic plasticity (BTSP) (103–106), which is responsible for the rapid formation of hippocampal place fields.”

    From Synaptic memory and CaMKII (2023) · cites this paper as [103]

  • The finding that strong hyperpolarization before the plateau potential blunts the potentiation favors the CaMKII partial activation mechanism but does not rule out the metabotropic mechanism.

    “The finding that strong hyperpolarization before the plateau potential blunts the potentiation (103) favors the former but does not rule out the latter.”

    From Synaptic memory and CaMKII (2023) · cites this paper as [103]

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Research works printed but not linked: 95

  1. Abraham WC 2008 Metaplasticity: tuning synapses and networks for plasticity Nature Reviews. Neuroscience 9 387 10.1038/nrn2356 18401345 · DOI
  2. Abraham A Pedregosa F Eickenberg M Gervais P Mueller A Kossaifi J Gramfort A Thirion B Varoquaux G 2014 Machine learning for neuroimaging with scikit-learn Frontiers in Neuroinformatics 8 14 10.3389/fninf.2014.00014 24600388 PMC3930868 · DOI
  3. Artola A Bröcher S Singer W 1990 Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex Nature 347 69 72 10.1038/347069a0 1975639 · DOI
  4. Beaulieu-Laroche L Harnett MT 2018 Dendritic Spines Prevent Synaptic Voltage Clamp Neuron 97 75 82 10.1016/j.neuron.2017.11.016 29249288 · DOI · Paper page
  5. Bi GQ Poo MM 1998 Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type The Journal of Neuroscience 18 10464 10472 10.1523/JNEUROSCI.18-24-10464.1998 9852584 PMC6793365 · DOI · Paper page
  6. Bittner KC Grienberger C Vaidya SP Milstein AD Macklin JJ Suh J Tonegawa S Magee JC 2015 Conjunctive input processing drives feature selectivity in hippocampal CA1 neurons Nature Neuroscience 18 1133 1142 10.1038/nn.4062 26167906 PMC4888374 · DOI · Paper page
  7. Bittner KC Milstein AD Grienberger C Romani S Magee JC 2017 Behavioral time scale synaptic plasticity underlies CA1 place fields Science 357 1033 1036 10.1126/science.aan3846 28883072 PMC7289271 · DOI · Paper page
  8. Bono J Clopath C 2017 Modeling somatic and dendritic spike mediated plasticity at the single neuron and network level Nature Communications 8 706 10.1038/s41467-017-00740-z 28951585 PMC5615054 · DOI
  9. Bostock E Muller RU Kubie JL 1991 Experience-dependent modifications of hippocampal place cell firing Hippocampus 1 193 205 10.1002/hipo.450010207 1669293 · DOI
  10. Bourboulou R Marti G Michon F-X El Feghaly E Nouguier M Robbe D Koenig J Epsztein J 2019 Dynamic control of hippocampal spatial coding resolution by local visual cues eLife 8 e44487 10.7554/eLife.44487 30822270 PMC6397000 · DOI
  11. Brandalise F Gerber U 2014 Mossy fiber-evoked subthreshold responses induce timing-dependent plasticity at hippocampal CA3 recurrent synapses PNAS 111 4303 4308 10.1073/pnas.1317667111 24550458 PMC3964078 · DOI
  12. Brzosko Z Schultz W Paulsen O 2015 Retroactive modulation of spike timing-dependent plasticity by dopamine eLife 4 e09685 10.7554/eLife.09685 26516682 PMC4626806 · DOI
  13. Brzosko Z Zannone S Schultz W Clopath C Paulsen O 2017 Sequential neuromodulation of Hebbian plasticity offers mechanism for effective reward-based navigation eLife 6 e27756 10.7554/eLife.27756 28691903 PMC5546805 · DOI
  14. Butler WN Hardcastle K Giocomo LM 2019 Remembered reward locations restructure entorhinal spatial maps Science 363 1447 1452 10.1126/science.aav5297 30923222 PMC6516752 · DOI · Paper page
  15. Buzsáki G Moser EI 2013 Memory, navigation and theta rhythm in the hippocampal-entorhinal system Nature Neuroscience 16 130 138 10.1038/nn.3304 23354386 PMC4079500 · DOI · Paper page
  16. Chandra N Barkai E 2018 A non-synaptic mechanism of complex learning: Modulation of intrinsic neuronal excitability Neurobiology of Learning and Memory 154 30 36 10.1016/j.nlm.2017.11.015 29196146 · DOI
  17. Clopath C Büsing L Vasilaki E Gerstner W 2010 Connectivity reflects coding: a model of voltage-based STDP with homeostasis Nature Neuroscience 13 344 352 10.1038/nn.2479 20098420 · DOI
  18. Clopath C Gerstner W 2010 Voltage and Spike Timing Interact in STDP - A Unified Model Frontiers in Synaptic Neuroscience 2 25 10.3389/fnsyn.2010.00025 21423511 PMC3059665 · DOI
  19. Cohen JD Bolstad M Lee AK 2017 Experience-dependent shaping of hippocampal CA1 intracellular activity in novel and familiar environments eLife 6 e23040 10.7554/eLife.23040 28742496 PMC5526666 · DOI
  20. Cone I Shouval HZ 2021 Behavioral Time Scale Plasticity of Place Fields: Mathematical Analysis Frontiers in Computational Neuroscience 15 640235 10.3389/fncom.2021.640235 33732128 PMC7959845 · DOI
  21. Diamantaki M Coletta S Nasr K Zeraati R Laturnus S Berens P Preston-Ferrer P Burgalossi A 2018 Manipulating Hippocampal Place Cell Activity by Single-Cell Stimulation in Freely Moving Mice Cell Reports 23 32 38 10.1016/j.celrep.2018.03.031 29617670 · DOI · Paper page
  22. Dupret D O’Neill J Pleydell-Bouverie B Csicsvari J 2010 The reorganization and reactivation of hippocampal maps predict spatial memory performance Nature Neuroscience 13 995 1002 10.1038/nn.2599 20639874 PMC2923061 · DOI · Paper page
  23. Froemke RC Poo MM Dan Y 2005 Spike-timing-dependent synaptic plasticity depends on dendritic location Nature 434 221 225 10.1038/nature03366 15759002 · DOI
  24. Fyhn M Hafting T Treves A Moser MB Moser EI 2007 Hippocampal remapping and grid realignment in entorhinal cortex Nature 446 190 194 10.1038/nature05601 17322902 · DOI · Paper page
  25. Gerstner W Lehmann M Liakoni V Corneil D Brea J 2018 Eligibility Traces and Plasticity on Behavioral Time Scales: Experimental Support of NeoHebbian Three-Factor Learning Rules Frontiers in Neural Circuits 12 53 10.3389/fncir.2018.00053 30108488 PMC6079224 · DOI
  26. Golding NL Staff NP Spruston N 2002 Dendritic spikes as a mechanism for cooperative long-term potentiation Nature 418 326 331 10.1038/nature00854 12124625 · DOI
  27. Golding NL Mickus TJ Katz Y Kath WL Spruston N 2005 Factors mediating powerful voltage attenuation along CA1 pyramidal neuron dendrites The Journal of Physiology 568 69 82 10.1113/jphysiol.2005.086793 16002454 PMC1474764 · DOI
  28. Graupner M Brunel N 2007 STDP in a bistable synapse model based on CaMKII and associated signaling pathways PLOS Computational Biology 3 e221 10.1371/journal.pcbi.0030221 18052535 PMC2098851 · DOI
  29. Graupner M Brunel N 2012 Calcium-based plasticity model explains sensitivity of synaptic changes to spike pattern, rate, and dendritic location PNAS 109 3991 3996 10.1073/pnas.1109359109 22357758 PMC3309784 · DOI
  30. Grienberger C Milstein AD Bittner KC Romani S Magee JC 2017 Inhibitory suppression of heterogeneously tuned excitation enhances spatial coding in CA1 place cells Nature Neuroscience 20 417 426 10.1038/nn.4486 28114296 · DOI
  31. Guerguiev J Lillicrap TP Richards BA 2017 Towards deep learning with segregated dendrites eLife 6 e22901 10.7554/eLife.22901 29205151 PMC5716677 · DOI
  32. Harvey CD Collman F Dombeck DA Tank DW 2009 Intracellular dynamics of hippocampal place cells during virtual navigation Nature 461 941 946 10.1038/nature08499 19829374 PMC2771429 · DOI
  33. He K Huertas M Hong SZ Tie X Hell JW Shouval H Kirkwood A 2015 Distinct Eligibility Traces for LTP and LTD in Cortical Synapses Neuron 88 528 538 10.1016/j.neuron.2015.09.037 26593091 PMC4660261 · DOI
  34. Hengen KB Torrado Pacheco A McGregor JN Van Hooser SD Turrigiano GG 2016 Neuronal Firing Rate Homeostasis Is Inhibited by Sleep and Promoted by Wake Cell 165 180 191 10.1016/j.cell.2016.01.046 26997481 PMC4809041 · DOI
  35. Herring BE Nicoll RA 2016 Long-Term Potentiation: From CaMKII to AMPA Receptor Trafficking Annual Review of Physiology 78 351 365 10.1146/annurev-physiol-021014-071753 26863325 · DOI · Paper page
  36. Hill AJ 1978 First occurrence of hippocampal spatial firing in a new environment Experimental Neurology 62 282 297 10.1016/0014-4886(78)90058-4 729680 · DOI
  37. Hollup SA Molden S Donnett JG Moser MB Moser EI 2001 Accumulation of hippocampal place fields at the goal location in an annular watermaze task The Journal of Neuroscience 21 1635 1644 10.1523/JNEUROSCI.21-05-01635.2001 11222654 PMC6762966 · DOI
  38. Inglebert Y Aljadeff J Brunel N Debanne D 2020 Synaptic plasticity rules with physiological calcium levels PNAS 117 33639 33648 10.1073/pnas.2013663117 33328274 PMC7777146 · DOI
  39. Jacob V Brasier DJ Erchova I Feldman D Shulz DE 2007 Spike timing-dependent synaptic depression in the in vivo barrel cortex of the rat The Journal of Neuroscience 27 1271 1284 10.1523/JNEUROSCI.4264-06.2007 17287502 PMC3070399 · DOI
  40. Jarsky T Roxin A Kath WL Spruston N 2005 Conditional dendritic spike propagation following distal synaptic activation of hippocampal CA1 pyramidal neurons Nature Neuroscience 8 1667 1676 10.1038/nn1599 16299501 · DOI
  41. Jedlicka P Benuskova L Abraham WC 2015 A Voltage-Based STDP Rule Combined with Fast BCM-Like Metaplasticity Accounts for LTP and Concurrent “Heterosynaptic” LTD in the Dentate Gyrus In Vivo PLOS Computational Biology 11 e1004588 10.1371/journal.pcbi.1004588 26544038 PMC4636250 · DOI
  42. Jezek K Henriksen EJ Treves A Moser EI Moser MB 2011 Theta-paced flickering between place-cell maps in the hippocampus Nature 478 246 249 10.1038/nature10439 21964339 · DOI · Paper page
  43. Keck T Toyoizumi T Chen L Doiron B Feldman DE Fox K Gerstner W Haydon PG Hübener M Lee H-K Lisman JE Rose T Sengpiel F Stellwagen D Stryker MP Turrigiano GG van Rossum MC 2017 Integrating Hebbian and homeostatic plasticity: the current state of the field and future research directions Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 372 20160158 10.1098/rstb.2016.0158 28093552 PMC5247590 · DOI
  44. Koester HJ Sakmann B 1998 Calcium dynamics in single spines during coincident pre- and postsynaptic activity depend on relative timing of back-propagating action potentials and subthreshold excitatory postsynaptic potentials PNAS 95 9596 9601 10.1073/pnas.95.16.9596 9689126 PMC21384 · DOI
  45. Lee JS Briguglio JJ Cohen JD Romani S Lee AK 2020 The Statistical Structure of the Hippocampal Code for Space as a Function of Time, Context, and Value Cell 183 620 635 10.1016/j.cell.2020.09.024 33035454 · DOI
  46. Leutgeb S Leutgeb JK Barnes CA Moser EI McNaughton BL Moser M-B 2005 Independent codes for spatial and episodic memory in hippocampal neuronal ensembles Science 309 619 623 10.1126/science.1114037 16040709 · DOI
  47. Lillicrap TP Santoro A Marris L Akerman CJ Hinton G 2020 Backpropagation and the brain Nature Reviews. Neuroscience 21 335 346 10.1038/s41583-020-0277-3 32303713 · DOI · Paper page
  48. Lynch GS Dunwiddie T Gribkoff V 1977 Heterosynaptic depression: a postsynaptic correlate of long-term potentiation Nature 266 737 739 10.1038/266737a0 195211 · DOI · Paper page
  49. Magee JC Johnston D 1997 A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons Science 275 209 213 10.1126/science.275.5297.209 8985013 · DOI
  50. Magee JC 1998 Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons The Journal of Neuroscience 18 7613 7624 10.1523/JNEUROSCI.18-19-07613.1998 9742133 PMC6793032 · DOI · Paper page
  51. Magee JC Grienberger C 2020 Synaptic Plasticity Forms and Functions Annual Review of Neuroscience 43 95 117 10.1146/annurev-neuro-090919-022842 32075520 · DOI · Paper page
  52. Malinow R Miller JP 1986 Postsynaptic hyperpolarization during conditioning reversibly blocks induction of long-term potentiation Nature 320 529 530 10.1038/320529a0 3008000 · DOI
  53. Mansuy IM 2003 Calcineurin in memory and bidirectional plasticity Biochemical and Biophysical Research Communications 311 1195 1208 10.1016/j.bbrc.2003.10.046 14623305 · DOI
  54. Markram H Lübke J Frotscher M Sakmann B 1997 Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs Science 275 213 215 10.1126/science.275.5297.213 8985014 · DOI · Paper page
  55. Mehta MR Barnes CA McNaughton BL 1997 Experience-dependent, asymmetric expansion of hippocampal place fields PNAS 94 8918 8921 10.1073/pnas.94.16.8918 9238078 PMC23195 · DOI
  56. Mehta MR 2004 Cooperative LTP can map memory sequences on dendritic branches Trends in Neurosciences 27 69 72 10.1016/j.tins.2003.12.004 15106650 · DOI
  57. Mehta MR 2015 From synaptic plasticity to spatial maps and sequence learning Hippocampus 25 756 762 10.1002/hipo.22472 25929239 · DOI
  58. Mendez P Stefanelli T Flores CE Muller D Lüscher C 2018 Homeostatic Plasticity in the Hippocampus Facilitates Memory Extinction Cell Reports 22 1451 1461 10.1016/j.celrep.2018.01.025 29425501 · DOI
  59. Migliore M Hoffman DA Magee JC Johnston D 1999 Role of an A-type K+ conductance in the back-propagation of action potentials in the dendrites of hippocampal pyramidal neurons Journal of Computational Neuroscience 7 5 15 10.1023/a:1008906225285 10481998 · DOI
  60. Milstein AD Bloss EB Apostolides PF Vaidya SP Dilly GA Zemelman BV Magee JC 2015 Inhibitory Gating of Input Comparison in the CA1 Microcircuit Neuron 87 1274 1289 10.1016/j.neuron.2015.08.025 26402609 · DOI
  61. Mizuseki K Royer S Diba K Buzsáki G 2012 Activity dynamics and behavioral correlates of CA3 and CA1 hippocampal pyramidal neurons Hippocampus 22 1659 1680 10.1002/hipo.22002 22367959 PMC3718552 · DOI
  62. Monaco JD Rao G Roth ED Knierim JJ 2014 Attentive scanning behavior drives one-trial potentiation of hippocampal place fields Nature Neuroscience 17 725 731 10.1038/nn.3687 24686786 PMC4036486 · DOI · Paper page
  63. Muller SZ Zadina AN Abbott LF Sawtell NB 2019 Continual Learning in a Multi-Layer Network of an Electric Fish Cell 179 1382 1392 10.1016/j.cell.2019.10.020 31735497 PMC6986370 · DOI
  64. Nakazawa K McHugh TJ Wilson MA Tonegawa S 2004 NMDA receptors, place cells and hippocampal spatial memory Nature Reviews. Neuroscience 5 361 372 10.1038/nrn1385 15100719 · DOI · Paper page
  65. Oja E 1982 A simplified neuron model as a principal component analyzer Journal of Mathematical Biology 15 267 273 10.1007/BF00275687 7153672 · DOI · Paper page
  66. O’Keefe J Conway DH 1978 Hippocampal place units in the freely moving rat: why they fire where they fire Experimental Brain Research 31 573 590 10.1007/BF00239813 658182 · DOI
  67. Palmer L Murayama M Larkum M 2012 Inhibitory Regulation of Dendritic Activity in vivo Frontiers in Neural Circuits 6 26 10.3389/fncir.2012.00026 22654734 PMC3360463 · DOI
  68. Payeur A Guerguiev J Zenke F Richards B Naud R 2020 Burst-Dependent Synaptic Plasticity Can Coordinate Learning in Hierarchical Circuits bioRxiv 10.1101/2020.03.30.015511 33986551 · DOI
  69. Pi H-J Hangya B Kvitsiani D Sanders JI Huang ZJ Kepecs A 2013 Cortical interneurons that specialize in disinhibitory control Nature 503 521 524 10.1038/nature12676 24097352 PMC4017628 · DOI · Paper page
  70. Rasmussen CE Williams CKI 2006 Gaussian Processes for Machine Learning. Adaptive Computation and Machine Learning MIT Press
  71. Richards BA Lillicrap TP 2019a Dendritic solutions to the credit assignment problem Current Opinion in Neurobiology 54 28 36 10.1016/j.conb.2018.08.003 30205266 · DOI
  72. Richards BA Lillicrap TP Beaudoin P Bengio Y Bogacz R Christensen A Clopath C Costa RP de Berker A Ganguli S Gillon CJ Hafner D Kepecs A Kriegeskorte N Latham P Lindsay GW Miller KD Naud R Pack CC Poirazi P Roelfsema P Sacramento J Saxe A Scellier B Schapiro AC Senn W Wayne G Yamins D Zenke F Zylberberg J Therien D Kording KP 2019b A deep learning framework for neuroscience Nature Neuroscience 22 1761 1770 10.1038/s41593-019-0520-2 31659335 PMC7115933 · DOI · Paper page
  73. Royer S Zemelman BV Losonczy A Kim J Chance F Magee JC Buzsáki G 2012 Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition Nature Neuroscience 15 769 775 10.1038/nn.3077 22446878 PMC4919905 · DOI · Paper page
  74. Sacramento J 2018 Advances in Neural Information Processing Systems MIT Press
  75. Sajikumar S Frey JU 2004 Late-associativity, synaptic tagging, and the role of dopamine during LTP and LTD Neurobiology of Learning and Memory 82 12 25 10.1016/j.nlm.2004.03.003 15183167 · DOI
  76. Schiller J Schiller Y 2001 NMDA receptor-mediated dendritic spikes and coincident signal amplification Current Opinion in Neurobiology 11 343 348 10.1016/s0959-4388(00)00217-8 11399433 · DOI
  77. Schulz JM Redgrave P Reynolds JNJ 2010 Cortico-striatal spike-timing dependent plasticity after activation of subcortical pathways Frontiers in Synaptic Neuroscience 2 23 10.3389/fnsyn.2010.00023 21423509 PMC3059678 · DOI
  78. Sheffield MEJ Adoff MD Dombeck DA 2017 Increased Prevalence of Calcium Transients across the Dendritic Arbor during Place Field Formation Neuron 96 490 504 10.1016/j.neuron.2017.09.029 29024668 PMC5642299 · DOI
  79. Shouval HZ Wang SS-H Wittenberg GM 2010 Spike timing dependent plasticity: a consequence of more fundamental learning rules Frontiers in Computational Neuroscience 4 19 10.3389/fncom.2010.00019 20725599 PMC2922937 · DOI
  80. Sjöström PJ Rancz EA Roth A Häusser M 2008 Dendritic excitability and synaptic plasticity Physiological Reviews 88 769 840 10.1152/physrev.00016.2007 18391179 · DOI
  81. Song S Miller KD Abbott LF 2000 Competitive Hebbian learning through spike-timing-dependent synaptic plasticity Nature Neuroscience 3 919 926 10.1038/78829 10966623 · DOI
  82. Stachenfeld KL Botvinick MM Gershman SJ 2017 The hippocampus as a predictive map Nature Neuroscience 20 1643 1653 10.1038/nn.4650 28967910 · DOI · Paper page
  83. Stefanelli T Bertollini C Lüscher C Muller D Mendez P 2016 Hippocampal Somatostatin Interneurons Control the Size of Neuronal Memory Ensembles Neuron 89 1074 1085 10.1016/j.neuron.2016.01.024 26875623 · DOI
  84. Stuart GJ Häusser M 2001 Dendritic coincidence detection of EPSPs and action potentials Nature Neuroscience 4 63 71 10.1038/82910 11135646 · DOI
  85. Takahashi H Magee JC 2009 Pathway interactions and synaptic plasticity in the dendritic tuft regions of CA1 pyramidal neurons Neuron 62 102 111 10.1016/j.neuron.2009.03.007 19376070 · DOI
  86. Titley HK Brunel N Hansel C 2017 Toward a Neurocentric View of Learning Neuron 95 19 32 10.1016/j.neuron.2017.05.021 28683265 PMC5519140 · DOI
  87. Turrigiano GG Nelson SB 2004 Homeostatic plasticity in the developing nervous system Nature Reviews. Neuroscience 5 97 107 10.1038/nrn1327 14735113 · DOI · Paper page
  88. Tyan L Chamberland S Magnin E Camiré O Francavilla R David LS Deisseroth K Topolnik L 2014 Dendritic inhibition provided by interneuron-specific cells controls the firing rate and timing of the hippocampal feedback inhibitory circuitry The Journal of Neuroscience 34 4534 4547 10.1523/JNEUROSCI.3813-13.2014 24671999 PMC6608127 · DOI · Paper page
  89. Xu N Harnett MT Williams SR Huber D O’Connor DH Svoboda K Magee JC 2012 Nonlinear dendritic integration of sensory and motor input during an active sensing task Nature 492 247 251 10.1038/nature11601 23143335 · DOI
  90. Yagishita S Hayashi-Takagi A Ellis-Davies GCR Urakubo H Ishii S Kasai H 2014 A critical time window for dopamine actions on the structural plasticity of dendritic spines Science 345 1616 1620 10.1126/science.1255514 25258080 PMC4225776 · DOI · Paper page
  91. Yang SN Tang YG Zucker RS 1999 Selective induction of LTP and LTD by postsynaptic [Ca2+]i elevation Journal of Neurophysiology 81 781 787 10.1152/jn.1999.81.2.781 10036277 · DOI · Paper page
  92. Zaremba JD Diamantopoulou A Danielson NB Grosmark AD Kaifosh PW Bowler JC Liao Z Sparks FT Gogos JA Losonczy A 2017 Impaired hippocampal place cell dynamics in a mouse model of the 22q11.2 deletion Nature Neuroscience 20 1612 1623 10.1038/nn.4634 28869582 PMC5763006 · DOI
  93. Zenke F Hennequin G Gerstner W 2013 Synaptic plasticity in neural networks needs homeostasis with a fast rate detector PLOS Computational Biology 9 e1003330 10.1371/journal.pcbi.1003330 24244138 PMC3828150 · DOI
  94. Zhao X Wang Y Spruston N Magee JC 2020 Membrane potential dynamics underlying context-dependent sensory responses in the hippocampus Nature Neuroscience 23 881 891 10.1038/s41593-020-0646-2 32451487 · DOI
  95. Ziv Y Burns LD Cocker ED Hamel EO Ghosh KK Kitch LJ El Gamal A Schnitzer MJ 2013 Long-term dynamics of CA1 hippocampal place codes Nature Neuroscience 16 264 266 10.1038/nn.3329 23396101 PMC3784308 · DOI · Paper page

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Sorted by citations

Authors
Milstein, A. D., Li, Y., Bittner, K. C., Grienberger, C., Soltesz, I., Magee, J. C., & Romani, S.
Affiliations
  • Rutgers, The State University of New Jersey (US)
  • Howard Hughes Medical Institute (US)
  • Department of Neurosurgery and Stanford Neurosciences Institute, Stanford University School of Medicine
Corresponding author
  • Magee, Jeffrey C
  • Romani, Sandro
ORCID
Venue
eLife
Publisher
eLife Sciences Publications, Ltd
Published
2021-12-09
Volume
10
ISSN
2050-084X (ISSN-L)
DOI
10.7554/elife.73046
PMC
PMC8776257
OpenAlex
W4225490719
Cited by
151
References
13
Citations by year
2026: 30 · 2025: 43 · 2024: 33 · 2023: 23 · 2022: 16 · 2021: 5 · 2020: 1
FWCI
10.13
Type
journal article
Language
en
Open access
Licence
Locations
  • eLife (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Institutes of Health (U19NS104590)
  • National Institute of Mental Health (R01MH121979)
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
bidirectional synaptic plasticity, hippocampal CA1, place fields, dendritic calcium spikes, plateau potentials, synaptic potentiation and depression, population activity, spatial learning, neural representations
MeSH terms
Action Potentials, Animals, Computer Simulation, Dendrites, Female, Hippocampus, Learning, Male, Neuronal Plasticity, Neurons, Synapses, Mice

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