题名

A Requirement of Low-Threshold Calcium Spike for Induction of Spike-Timing-Dependent Plasticity at Corticothalamic Synapses on Relay Neurons in the Ventrobasal Nucleus of Rat Thalamus

DOI

10.4077/CJP.2012.BAA047

作者

Ching-Lung Hsu;Hsiu-Wen Yang;Cheng-Tung Yen;Ming-Yuan Min

关键词

corticothalamic (CT) synapse ; long-term potentiation (LTP) ; low-threshold calcium spike ; somatosensory ; ventrobasal nucleus (VBN)

期刊名称

The Chinese Journal of Physiology

卷期/出版年月

55卷6期(2012 / 12 / 31)

页次

380 - 389

内容语文

英文

英文摘要

Relay neurons in sensory thalamus transmit somatosensory information to cerebral cortex and receive sensory and feedback corticothalamic (CT) synaptic inputs. Their duality of firing modes, in bursts and continuous, underlies state dependence of thalamic information transfer, but the impact of different firing patterns on synaptic plasticity was rarely explored. To address this issue, we made whole-cell recording from relay neurons in the ventrobasal nucleus (VBN) of rat thalamus and compared synaptic plasticity induced by pairing CT-EPSP with two different types of burst spiking: low-threshold spike (LTS)-burst spiking triggered at Vm~-70 mV, and high-frequency spiking induced at Vm~-55 mV. The latter mimics natural burst spiking of relay neurons without activation of LTS. We found that, while backpropagating APs alone were not sufficient, low-threshold calcium spike was required for the induction of spike-timing-dependent LTP at CT synapses. Our results reveal a novel role of the calcium spike plays in the induction of long-term plasticity of CT synapse. Considering the dendritic origin of LTS, this study also implies potential physiological regulations over synaptic plasticity in thalamus. We propose that this form of synaptic plasticity may be involved in the dynamic fine-tuning of thalamocortical information relay.

主题分类 醫藥衛生 > 基礎醫學
参考文献
  1. Bal, T.,McCormick, D.A.(1993).Mechanisms of oscillatory activity in guinea-pig nucleus reticularis thalami in vitro: a mammalian pacemaker.J. Physiol.,468,669-691.
  2. Dan, Y.,Poo, M.M.(2004).Spike timing-dependent plasticity of neural circuits.Neuron,44,23-30.
  3. Deschênes, M.,Veinante, P.,Zhang, Z.W.(1998).The organization of corticothalamic projections: reciprocity versus parity.Brain Res. Rev.,28,286-308.
  4. Destexhe, A.(2000).Modelling corticothalamic feedback and the gating of the thalamus by the cerebral cortex.J. Pysiol. (Paris),94,391-410.
  5. Destexhe, A.,Neubig, M.,Ulrich, D.,Huguenard, J.(1998).Dendritic low-threshold calcium currents in thalamic relay cells.J. Neurosci.,18,3574-3588.
  6. Ergenzinger, E.R.,Glasier, M.M.,Hahm, J.O.,Pons, T.P.(1998).Cortically induced thalamic plasticity in the primate somatosensory system.Nat. Neurosci.,1,226-229.
  7. George, M.S.,Abbott, L.F.,Siegelbaum, S.A.(2009).HCN hyperpolarization-activated cation channels inhibit subthreshold EPSPs through interactions with M-Type K+ channels.Nat. Neurosci.,12,577-584.
  8. Hoffman D.A.,Magee, J.C.,Colbert, C.M.,Johnston, D.(1997).K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons.Nature,387,869-875.
  9. Hsu, C.L.,Yang, H.W.,Yen, C.T.,Min, M.Y.(2010).Comparison of synaptic transmission and plasticity between sensory and cortical synapses on relay neurons in the ventrobasal nucleus of the rat thalamus.J. Physiol.,588,4347-4363.
  10. Jahnsen, H.,Llinás, R.(1984).Electrophysiological properties of guinea-pig thalamic neurones: an in vitro study.J. Physiol.,349,205-226.
  11. Jones, E.G.(2007).The thalamus.Cambridge:Cambridge University Press.
  12. Killackey, H.P.,Sherman, S.M.(2003).Corticothalamic projections from the rat primary somatosensory cortex.J. Neurosci.,23,7381-7384.
  13. Krupa, D.J.,Ghazanfar, A.A.,Nicolelis, M.A.(1999).Immediate thalamic sensory plasticity depends on corticothalamic feedback.Proc. Natl. Acad. Sci. USA,96,8200-8205.
  14. Landisman, C.E.,Connors, B.W.(2007).VPM and PoM nuclei of the rat somatosensory thalamus: intrinsic neuronal properties and corticothalamic feedback.Cereb. Cortex,17,2853-2865.
  15. Le Masson, G.,Renaus-Le Masson, S.,Debay, D.,Bal, T.(2002).Feedback inhibition controls spike transfer in hybrid thalamic circuit.Nature,417,854-858.
  16. Lisman, J.,Spruston, N.(2005).Postsynaptic depolarization requirements for LTP and LTD: a critique of spike timing-dependent plasticity.Nat. Neurosci.,8,839-841.
  17. Liu, X.B.,Honda, C.N.,Jones, E.G.(1995).Distribution of four types of synapse on physiologically identified relay neurons in the ventral posterior thalamic nucleus of the cat.J. Comp. Neurol.,352,69-91.
  18. Magee, J.C.,Johnston, D.(1997).A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons.Science,275,209-213.
  19. Markram, H.,Lübke, J.,Frotscher, M.,Sakmann, B.(1997).Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs.Science,275,213-215.
  20. McCormick, D.A.,Feeser, H.R.(1990).Functional implications of burst firing and single spike activity in lateral geniculate relay neurons.Neuroscience,39,103-113.
  21. Mckay, B.E.,McRory, J.E.,Molineux, M.L.,Hamid, J.,Snutch, T.P.,Zamponi, G.W.,Turner, R.W.(2006).Cav3 T-type calcium channel isoforms differentially distribute to somatic and dendritic compartments in rat central neurons.Eur. J. Neurosci.,24,2581-2594.
  22. Miyata, M.,Imoto, K.(2006).Different composition of glutamate receptors in corticothalamic and lemniscal synaptic responses and their roles in the firing responses of ventrobasal thalamic neurons in juvenile mice.J. Physiol.,575,161-174.
  23. Munsch, T.,Budde, T.,Pape, H.C.(1997).Voltage-activated intracellular calcium transients in thalamic relay cells and interneurons.Neuroreport,8,2411-2418.
  24. Murphy, P.C.,Sillito, A.M.(1987).Corticofugal feedback influences the generation of length tuning in the visual pathway.Nature,329,727-729.
  25. Peschanski, M.,Lee, C.L.,Ralston, H.J.(1984).The structural organization of the ventrobasal complex of the rat as revealed by the analysis of physiologically characterized neurons injected intracellularly with horseradish peroxidase.Brain Res.,297,63-74.
  26. Reichova, I.,Sherman, S.M.(2004).Somatosensory corticothalamic projections: distinguishing drivers from modulators.J. Neurophysiol.,92,2185-2197.
  27. Rouiller, E.M.,Welker, E.(2000).A comparative analysis of the morphology of corticothalamic projections in mammals.Brain Res. Bull.,53,727-741.
  28. Sherman, S.M.(2010).Tonic and burst firing: dual modes of thalamocortical relay.Trends Neurosci.,24,122-126.
  29. Sherman, S.M.(2005).Thalamic relays and cortical functioning.Prog. Brain Res.,149,107-126.
  30. Sjöström, P.J.,Turrigiano, G.G.,Nelson, S.B.(2001).Rate, timing, and cooperativity jointly determine cortical synaptic plasticity.Neuron,32,1149-1164.
  31. Špacek, J.,Lieberman, A.R.(1974).Ultrastructure and three-dimensional organization of synaptic glomeruli in rat somatosensory thalamus.J. Anat.,117,487-516.
  32. Stuart, G.J.,Häusser, M.(2001).Dendritic coincidence detection of EPSPs and action potentials.Nat. Neurosci.,4,63-71.
  33. Van Horn, S.C.,Sherman, S.M.(2004).Differences in projection patterns between large and small corticothalamic terminals.J. Comp. Neurol.,475,406-415.
  34. Williams, S.R.,Stuart, G.J.(2000).Action potential backpropagation and somato-dendritic distribution of ion channels in thalamocortical neurons.J. Neurosci.,20,1307-1317.
  35. Wolfart, J.,Debay, D.,Le Masson, G.,Destexhe, A.,Bal, T.(2005).Synaptic background activity controls spike transfer from thalamus to cortex.Nat. Neurosci.,8,1760-1767.
  36. Zhou, Q.,Godwin, D.W.,O'Malley, D.M.,Adams, P.R.(1997).Visualization of calcium influx through channels that shape the burst and tonic firing modes of thalamic relay neurons.J. Neurophysiol.,77,2816-2825.