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Factors Affecting STDP in the Dendrites of CA1 Pyramidal Cells

  • Ausra Saudargiene
  • Bruce P. GrahamEmail author
Chapter
Part of the Springer Series in Computational Neuroscience book series (NEUROSCI)

Abstract

Synaptic spike-time-dependent plasticity (STDP) is a function of the membrane depolarisation at the synapse, which is determined not only by somatic spiking activity in the postsynaptic cell but also by the synaptic site in the dendrites (distance from the cell body) and other local synaptic activities, particularly at inhibitory synapses. These factors can result in spatio-temporal gradients of STDP in a single neuron. In a pair of modelling studies (Saudargiene A, Graham BP, Biosystems 130:37–50, 2015; Saudargiene A, et al., Hippocampus 25(2):208–218, 2015), we have examined these effects for inputs onto synaptic spines at different locations in the complex apical dendrites of a CA1 pyramidal cell. The first study (Saudargiene A, Graham BP, Biosystems 130:37–50, 2015) examines the temporal signal requirements for inducing long-term potentiation (LTP) or long-term depression (LTD) at a synapse on a spine located at different locations in the dendrites. It is also determined how dendritic inhibition can alter these signalling requirements. The second study (Saudargiene A, et al., Hippocampus 25(2):208–218, 2015) moves on to explore more physiological situations involving theta and gamma rhythms in the hippocampus.

Keywords

Spike-time-dependent plasticity (STDP) Long-term potentiation (LTP) Long-term depression (LTD) Dendrites Spines Inhibition Theta rhythm Gamma rhythm CA1 pyramidal cell Compartmental modelling 

References

  1. Badoual M, Zou Q, Davison AP, Rudolph M, Bal T, Frégnac Y, Destexhe A (2006) Biophysical and phenomenological models of multiple spike interactions in spike-timing dependent plasticity. Int J Neural Syst 16(2):79–97CrossRefGoogle Scholar
  2. Bar-Ilan L, Gidon A, Segev I (2013) The role of dendritic inhibition in shaping the plasticity of excitatory synapses. Front Neural Circuits 6(118):1–13Google Scholar
  3. Bi GQ, Poo MM (1998) Synaptic modifications in cultured Hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18:10464–10472CrossRefGoogle Scholar
  4. Bi GQ, Poo MM (2001) Synaptic modification by correlated activity: Hebb’s postulate revisited. Annu Rev Neurosci 24:139–166CrossRefGoogle Scholar
  5. Buchanan KA, Mellor JR (2010) The activity requirements for spike timing dependent plasticity in the hippocampus. Front Synaptic Neurosci 2(11):1–5Google Scholar
  6. Cutsuridis V (2011) GABA inhibition modulates NMDA-R mediated spike timing dependent plasticity (STDP) in a biophysical model. Neural Netw 24(1):29–42CrossRefGoogle Scholar
  7. Cutsuridis V (2012) Bursts shape the NMDA-R mediated spike timing dependent plasticity curve: role of burst interspike interval and GABAergic inhibition. Cogn Neurodyn 6(5):421–441CrossRefGoogle Scholar
  8. Cutsuridis V, Cobb S, Graham BP (2010) Encoding and retrieval in a model of the hippocampal CA1 microcircuit. Hippocampus 20(3):423–446Google Scholar
  9. Erreger K, Dravid SM, Banke TG, Wyllie DJ, Traynelis SF (2005) Subunit-specific gating controls rat NR1/NR2A and NR1/NR2B NMDA channel kinetics and synaptic signalling profiles. J Physiol 563(2):345–358CrossRefGoogle Scholar
  10. Froemke RC, Poo MM, Dan Y (2005) Spike-timing-dependent synaptic plasticity depends on dendritic location. Nature 434(7034):221–225CrossRefGoogle Scholar
  11. Froemke RC, Letzkus JJ, Kampa BM, Hang GB, Stuart GJ (2010) Dendritic synapse location and neocortical spike-timing dependent plasticity. Front Synaptic Neurosci 2(29):1–14Google Scholar
  12. Furber S, Temple S (2007) Neural systems engineering. J R Soc Interface 4:193–206CrossRefGoogle Scholar
  13. Golding NL, Staff NP, Spruston N (2002) Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 418(6895):326–331CrossRefGoogle Scholar
  14. Graham BP, Cutsuridis V, Hunter R (2010) Associative memory models of hippocampal areas CA1 and CA3. In: Cutsuridis V et al (ed) Hippocampal microcircuits, Springer Series in Computational Neuroscience 5 (first edition)CrossRefGoogle Scholar
  15. Graham BP, Saudargiene A, Cobb S (2014) Spine head calcium as a measure of summed postsynaptic activity for driving synaptic plasticity. Neural Comput 26:2194–2222CrossRefGoogle Scholar
  16. Graupner M, Brunel N (2007) STDP in a bistable synapse model based on CaMKII and associated signaling pathways. PLoS Computat Biol 3(11):e221CrossRefGoogle Scholar
  17. Graupner M, Brunel N (2012) Calcium-based plasticity model explains sensitivity of synaptic changes to spike pattern, rate, and dendritic location. Proc Natl Acad Sci U S A 109:3991–3996CrossRefGoogle Scholar
  18. Hardie J, Spruston N (2009) Synaptic depolarization is more effective than back-propagating action potentials during induction of associative long-term potentiation in hippocampal pyramidal neurons. J Neurosci 29:3233–3241CrossRefGoogle Scholar
  19. Hasselmo M, Bodelon C, Wyble B (2002a) A proposed function of the hippocampal theta rhythm: separate phases of encoding and retrieval of prior learning. Neural Comput 14:793–817CrossRefGoogle Scholar
  20. Hasselmo ME, Hay J, Ilyn M, Gorchetchnikov A (2002b) Neuromodulation, theta rhythm and rat spatial navigation. Neural Netw 15:689–707CrossRefGoogle Scholar
  21. Hyman JM, Wyble BP, Goyal V, Rossi CA, Hasselmo ME (2003) Stimulation in hippocampal region CA1 in behaving rates yields long-term potentiation when delivered to the peak of theta and long-term depression when delivered to the trough. J Neurosci 23:11725–11731CrossRefGoogle Scholar
  22. Judge SJ, Hasselmo ME (2004) Theta rhythmic stimulation of stratum lacunosum-moleculare in rat hippocampus contributes to associative LTP at a phase offset in stratum radiatum. J Neurophysiol 92:1615–1624CrossRefGoogle Scholar
  23. Klausberger T, Magill PJ, Marton LF, David J, Roberts B, Cobden PM, Buzsaki G, Somogyi P (2003) Brain-state and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421:844–848CrossRefGoogle Scholar
  24. Klausberger T, Marton LF, Baude A, Roberts JD, Magill PJ, Somogyi P (2004) Spike timing of dendrite-targeting bistratified cells during hippocampal network oscillations in vivo. Nat Neurosci 7:41–47CrossRefGoogle Scholar
  25. Letzkus JJ, Kampa BM, Stuart GJ (2006) Learning rules for spike timing dependent plasticity depend on dendritic synapse location. J Neurosci 26(41):10420–10429CrossRefGoogle Scholar
  26. Leung LS, Roth L, Canning KJ (1995) Entorhinal inputs to hippocampal CA1 and dentate gyrus in the rat: a current-source-density study. J Neurophysiol 73:2392–2403CrossRefGoogle Scholar
  27. Lisman J, Malenka RC, Nicoll RA, Malinow R (1997) Learning mechanisms: the case for CaM-KII. Science 276:2001–2002CrossRefGoogle Scholar
  28. Magee JC, Johnston DA (1997) Synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275(5297):209–213CrossRefGoogle Scholar
  29. Manns JR, Zilli EA, Ong KC, Hasselmo ME, Eichenbaum H (2007) Hippocampal CA1 spiking during encoding and retrieval: Relation to theta phase. Neurobiol Learn Mem 87:9–20CrossRefGoogle Scholar
  30. Markram H, Lübke J, Frotscher M, Sakmann B (1997) Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275:213–215CrossRefGoogle Scholar
  31. Markram H et al (2015) Reconstruction and simulation of neocortical microcircuitry. Cell 163(2):456–492CrossRefGoogle Scholar
  32. Mizuno T, Kanazawa I, Sakurai M (2001) Differential induction of LTP and LTD is not determined solely by instanteneous calcium concentration: an essential involvement of a temporal factor. Eur J Neurosci 14(4):701–708CrossRefGoogle Scholar
  33. Mizuseki K, Sirota A, Pastalkova E, Buzsaki G (2009) Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop. Neuron 64:267–280CrossRefGoogle Scholar
  34. Molyneaux BJ, Hasselmo ME (2002) GABAB presynaptic inhibition has an in vivo time constant sufficiently rapid to allow modulation at theta frequency. J Neurophysiol 87:1196–1205CrossRefGoogle Scholar
  35. Nishiyama M, Hong K, Mikoshiba K, Poo MM, Kato K (2000) Calcium stores regulate the polarity and input specificity of synaptic modification. Nature 408:584–588CrossRefGoogle Scholar
  36. Pfeil T, Grübl A, Jeltsch S, Müller E, Müller P, Petrovici MA, Schmuker M, Brüderle D, Schemmel J, Meier K (2013) Six networks on a universal neuromorphic computing substrate. Front Neurosci 7(11)Google Scholar
  37. Pi HJ, Lisman JE (2008) Coupled phosphatase and kinase switches produce the tristability required for long-term potentiation and long-term depression. J Neurosci 28(49):13132–13138CrossRefGoogle Scholar
  38. Poirazi P, Pissadaki E (2010) The making of a detailed CA1 pyramidal neuron model. In: Cutsuridis V et al (ed) Hippocampal Microcircuits, Springer Series in Computational Neuroscience 5 (first edition)CrossRefGoogle Scholar
  39. Poirazi P, Brannon T, Mel BW (2003) Arithmetic of subthreshold synaptic summation in a model CA1 pyramidal cell. Neuron 37:977–987CrossRefGoogle Scholar
  40. Rast A, Galluppi F, Davies S, Plana L, Patterson C, Sharp T, Lester D, Furber S (2011) Concurrent heterogeneous neural model simulation on real-time neuromimetic hardware. Neural Netw 24:961–978CrossRefGoogle Scholar
  41. Remy S, Spruston N (2007) Dendritic spikes induce single-burst long term potentiation. Proc Natl Acad Sci U S A 104:17192–17197CrossRefGoogle Scholar
  42. Saudargiene A, Graham BP (2015) Inhibitory control of site-specific synaptic plasticity in a model CA1 pyramidal neuron. Biosystems 130:37–50CrossRefGoogle Scholar
  43. Saudargiene A, Cobb S, Graham BP (2015) A computational study on plasticity during theta cycles at schaffer collateral synapses on CA1 pyramidal cells in the hippocampus. Hippocampus 25(2):208–218CrossRefGoogle Scholar
  44. Sjöström PJ, Häusser M (2006) A cooperative switch determines the sign of synaptic plasticity in distal dendrites of neocortical pyramidal neurons. Neuron 51(2):227–238CrossRefGoogle Scholar
  45. Sjöström PJ, Rancz EA, Roth A, Häusser M (2008) Dendritic excitability and synaptic plasticity. Physiol Rev 88(2):769–840CrossRefGoogle Scholar
  46. Strösslin T, Sheynikhovich D, Chavarriaga R, Gerstner W (2005) Robust self-localisation and navigation based on hippocampal place cells. Neural Netw 18:1125–1140CrossRefGoogle Scholar
  47. Tsukada M, Aihara T, Kobayashi Y, Shimazaki H (2005) Spatial analysis of spike timing- dependent LTP and LTD in the CA1 area of hippocampal slices using optical imaging. Hippocampus 15(1):104–109CrossRefGoogle Scholar
  48. Vargas-Caballero M, Robinson HP (2004) Fast and slow voltage-dependent dynamics of magnesium block in the NMDA receptor: the asymmetric trapping block model. J Neurosci 24(27):6171–6180CrossRefGoogle Scholar
  49. Wittenberg GM, Wang SS (2006) Malleability of spike-timing-dependent plasticity at the CA3–CA1 synapse. J Neurosci 26:6610–6617CrossRefGoogle Scholar
  50. Wyble BP, Linster C, Hasselmo ME (2000) Size of CA1-evoked synaptic potentials is related to theta rhythm phase in rat hippocampus. J Neurophysiol 83:2138–2144CrossRefGoogle Scholar
  51. Zilli EA, Hasselmo ME (2006) An analysis of the mean theta phase of population activity in a model of hippocampal region CA1. Network 7:277–297CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Laboratory of Biophysics and Bioinformatics, Neuroscience InstituteLithuanian University of Health SciencesKaunasLithuania
  2. 2.Division of Computing Science & MathematicsUniversity of StirlingStirlingUK

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